Animal Biodiversity and Conservation issue 25.2 (2002)

Formerly Miscel·lània Zoològica

2002

and

Animal Biodiversity Conservation 25.2

"Cepaea nemoralis Linneo" Fauna malacológica terrestre y de agua dulce de Cataluña, Dr. F. Haas; Treballs del Museu de Zoologia, 5 (1991). Làmina XLVI.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Ciències Naturals (Zoologia) Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail publicacionsmuseuciencies@mail.bcn.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Pere Abelló Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Javier Alba–Tercedor Univ. de Granada, Granada, Spain Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament–CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Michael J. Conroy Univ. of Georgia, Athens, USA Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo–Roura Univ. Pompeu Fabra, Barcelona, Spain Gary D. Grossman Univ. of Georgia, Athens, USA Damià Jaume IMEDEA–CSIC, Univ. de les Illes Balears, Spain Jordi Lleonart Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Jorge M. Lobo Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Pablo J. López–González Univ de Sevilla, Sevilla, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Montserrat Ramón Inst. de Ciències del Mar CMIMA­–CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Pedro Rincón Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Alfredo Salvador Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Ciències Naturals de Barcelona, Barcelona, Spain Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana–CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle–CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Jersey, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana–CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas–CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway Animal Biodiversity and Conservation 25.2, 2002 © 2002 Museu de Ciències Naturals (Zoologia), Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58 The journal is freely available online at: http://bcn.cat/ABC

Animal Biodiversity and Conservation 25.2 (2002)

1

Pronura bidoup n. sp.

(Collembola, Neanuridae, Neanurinae, Paleonurini) from southern Vietnam L. Deharveng1 & A. Smolis2

Deharveng, L. & Smolis, A., 2002. Pronura bidoup n. sp. (Collembola, Neanuridae, Neanurinae, Paleonurini) from southern Vietnam. Animal Biodiversity and Conservation, 25.2: 1–5.

Abstract Pronura bidoup n. sp. (Collembola, Neanuridae, Neanurinae, Paleonurini) from southern Vietnam.— A new species of Pronura Delamare Debouteville, 1953, Pronura bidoup n. sp. is described from the Bi Doup massif in southern Vietnam, where it is largely distributed above 1,350 m. The new species exhibits a combination of characters unusual for the genus: shift of chaeta f towards chaeta e on labium, large central reticulate plate on head, presence of microchaetae on furcal rest, reduced chaetotaxy of legs and abdominal segment VI. It is related to Pronura ornata Deharveng & Bedos, 1993 from high altitude in Thailand.

Key words: Pronura bidoup n. sp., Collembola, Neanuridae, Vietnam.

Resumen Pronura bidoup sp. n. (Collembola, Neanuridae, Neanurinae, Paleonurini) del sur de Vietnam.— Se describe una nueva especie de Pronura Delamare Debouteville, 1953, Pronura bidoup sp. n., del macizo Bi Doup, situado en el sur de Vietnam, donde se distribuye ampliamente por encima de los 1.350 m de altitud. Esta nueva especie presenta una serie de caracteres poco usuales para el género: desplazamiento de la queta f hacia la queta e en el labium, placa central grande reticulada en la cabeza, presencia de microquetas en la base de la furca, quetotaxia reducida en las patas y en el segmento abdominal VI. P. bidoup sp. n. está relacionada con P. ornata Deharveng y Bedos, 1993, que se encuentra a gran altitud en Tailandia.

Palabras clave: Pronura bidoup sp. n., Collembola, Neanuridae, Vietnam.

(Received: 7 III 02; Conditional acceptance: 7 V 02; Final acceptance: 6 VI 02) 1

Louis Deharveng, Museum National d’Histoire Naturelle, Laboratoire d’Entomologie, ESA 8043 du CNRS, 45 rue Buffon, 75005–Paris, France.

2 Adrian Smolis, Zoological Institute of Wroclaw Univ., Sienkiewicza 21, 50–335 Wroclaw, Poland.

1 2

E–mail: deharven@mnhn.fr E–mail: adek@biol.uni.wroc.pl

ISSN: 1578–665X

© 2002 Museu de Ciències Naturals

2

Introduction The Bi Doup massif above Dalat in southern Vietnam has retained large patches of undisturbed primary forest, which host a very rich Neanurinae fauna including more than 25 species, all new to science (Deharveng & Le Cong Kiet, pers. com.). In this paper, we describe Pronura bidoup n. sp., a morphologically remarkable species of the genus Pronura Delamare Debouteville, 1953, related to Pronura ornata Deharveng & Bedos, 1993, known from the top of Doi Inthanon, the highest mountain of Thailand.

Material and methods The terminology and abbreviations used in the text and the tables are standard conventions for taxonomic descriptions in the subfamily Neanurinae (DEHARVENG, 1983, modified).

Abbreviations used in the text and tables Types of chaetae: bms. Buried s–microchaeta; M. Macrochaeta; me. Mesochaeta; mi. Microchaeta; ms. S–microchaeta; or. Organite of antenna IV; S. S–chaeta; x. Labial papilla.

General morphology: abd. Abdominal segment; ant. Antennal segment; th. Thoracic segment.

Chaetal groups and tubercles on head: Af. Antenno–frontal; CL. Clypeal; De. Dorso–external; Di. Dorso–internal; DL. Dorso–lateral; L. Lateral ; Oc. Ocular; So. Subocular; Ve. Ventro–external; Vi. Ventro–internal; VL. Ventro–lateral.

Chaetal groups and tubercles on tergites: De. Dorso–external; Di. Dorso–internal; DL. Dorso– lateral; L. Lateral.

Chaetal groups and tubercles of sternites: Ag. Ante–genital; An. Anal; Fu. Furcal; Ve. Ventral; VL. Ventro–lateral.

Appendages: Cx. Coxa; Fe. Femur; Scx2. Subcoxa 2; Tr. Trochanter; Ti. Tibiotarsus; VT. Ventral tube.

Types are deposited in the Museum National d’Histoire Naturelle de Paris.

Results

Pronura bidoup n. sp. (tables 1, 2; figs. 1–6) Studied material Holotype female and one paratype female.

Vietnam, Lam Dong province, Bi Doup massif, Nui Gia Rich, 1hr 1/2 from Klong Lanh by foot, 1,440 m, litter, Berlese extraction, 18 XII 98, leg.

L. Deharveng & A. Bedos (sample VIET–689).

Types mounted on slides in Marc–André II. Additional specimens (leg. L. Deharveng & A. Bedos) Vietnam, Lam Dong province, Bi Doup massif: 1,545 m, litter, Berlese extraction, 28 II 97,

Deharveng & Smolis

8 specimens (sample VIET–281); ibid: 1,900 m, litter, Berlese extraction, 1 III 97, 2 specimens (samples VIET–302, VIET–304); ibid: near the school of Klong Lanh, 1,410 m, litter, Berlese extraction, 18 XII 98, 8 specimens (sample VIET–675). Vietnam, Lam Dong province, near Dalat, Cam Ly area, 1,380 m, litter, Berlese extraction, 16 XII 98, 2 specimens (samples VIET–657, VIET–665).

Description Length: 0.55 to 0.75 mm. Colour: white in alcohol.

Dorsal tubercles weak or absent; only the tubercles of head and of abd. V and VI, and the dorso– lateral tubercles of abd. II–IV are well developed; they are constituted by stronger secondary granules, with tertiary granules and slight reticulation on head. In some specimens, secondary granules are slightly stronger on the axial area of the tergites where Di chaetae are more or less grouped. Dorso–internal tubercles of abd. V not overhanging abd. VI. Homochaetotic clothing of smooth, slender, tapering and curved mesochaetae, with frequent asymmetries. S–chaetae on abd. I–V thin, 1.5 to 3 times longer than nearby mesochaetae.

Head (table 1, figs. 1, 2, 4). S–chaetae of ant. IV thick and rather short, like in P. ornata (figured in DEHARVENG & BEDOS, 1993); apical vesicle of ant.IV fused to the apex, hardly distinct. Buccal cone rather elongate compared to that of P. ornata; labrum rounded at the apex; labium with chaetae A, C, D, E, F, G, d, e and f, with f closer to e than to G, and a minute x papilla (fig. 4); chaeta c (or possibly d) not observed. Maxilla styliform, mandible tridentate. Ocelli either absent, or possibly 2+2 covered with primary granules and not clearly distinct from secondary granules. The clypeal, antennal, frontal and ocular tubercles are fused in a single central plate, with a complete set of chaetae (A, B, C, D, E, F, O, Oca, Ocm, Ocp), and 2 to 4 additional chaetae between A and B, often asymmetrically arranged. Laterally, the tubercles DL, L and So are fused in a unique plate.

Tergites (table 2, figs. 1, 5). No plurichaetosis nor additional S–chaetae. Strong and irregular integument bumps on abd. IV and sometimes on abd. II between and behind the dorso–external and dorso–lateral chaetal groups. Dorso–internal chaetae shift towards dorso–external ones on abd. V. One lateral chaeta L on abd. V, without tubercle. Abd. VI not bilobed, with an uneven chaeta and a reduced chaetotaxy.

Sternites and appendages. Chaeta M absent on tibiotarsi. Vestigial furcal microchaetae of the sternites of abd. III–IV very distinct, on a small smooth plate (fig. 6). Genital plate with 4–5 (female) or 6 (male) circumgenital chaetae, and 2 (female) or 4+4 (male) genital chaetae; no modified chaetae in the male (male specimen from VIET–281).

Derivatio nominis The new species is named after its type locality.

3

Animal Biodiversity and Conservation 25.2 (2002)

27 :m m

1

9 :m m

2–6

Figs. 1–6. 1, 2, 4–6. Pronura bidoup n. sp.: 1. Dorsal view; 2. Central plate on head; 4. Labium; 5.

Tubercle (Di + De + DL) on abd. V; 6. Furcal rest with its 6 microchaetae. 3. Pronura ornata Deharveng & Bedos, 1993, labium.

Figs. 1–6. 1, 2, 4–6. Pronura bidoup sp. n.: 1. Vista dorsal; 2. Placa central de la cabeza; 4. Labium; 5.

Tubérculo (Di + De + DL) del segmento abdominal V; 6. Base de la furca con 6 microquetas. 3. Pronura ornata Deharveng & Bedos, 1993, labium.

Deharveng & Smolis

4

Table 1. Cephalic chaetotaxy of Pronura bidoup n. sp.: G. Group of chaetae; Tu. Tubercle; N. Number of chaetae; Ty. Type of chaetae; * other chaetae not analysed on ant. IV. .

Tabla 1. Quetotaxia cefálica de Pronura bidoup sp. n.: G. Grupo de quetas; Tu. Tubérculo; N. Número de quetas; Ty. Tipo de queta; * en antena IV no se analizaron otras quetas.

G

Tu

N

Ty

CL + Af + 2Oc

yes

23–25

me

A, B, C, D, E, F, O, Oca, Ocm, Ocp and 2–4 additional chaetae

(yes)

1

me

Di1 De1, Di2, De2

Di De

yes

3

me

DL + L + So

yes

2

M

14

me

Vi

5

me

Ve

6–7

me

Prelabral

?

?

Labrum basal

2

me

Labrum distal Labium

2

me

2

M

1

M

F

8

me

A, C, D, E, G, d, e, f

1

x

Ant. I

7

me

Ant. II

11

me

Ant. III

16

me

2

S

Ant. IV*

Chaetae

S2, S5

3

ms

s1, s3, s4

8

S

S1 to S8

1

bms

or

Table 2. Post–cephalic chaetotaxy of Pronura bidoup n. sp.: * 1 mi on the upper valve and ?2 mi on the lateral valves.

Tabla 2. Quetotaxia postcefálica de Pronura bidoup sp. n.: * 1 mi en la valva superior y ?2 mi en las valvas laterales.

Di

De

DL

L

Scx2

Cx

Tr

Fe

Ti

Th. I

1

2

1

–

0

3

5

12

18

Th. II

3

3+S

3+S+ms

3

2

7

5

11

18

8

5

10

17

Th. III

3

3+S

3+S

3

2

Abd. I

2

2+S

2

3–(4)

VT: 4

Abd. II

2

2+S

2

3–(4)

Ve: 4–5 (Ve1 present)

Abd. III

2

2–(3)+S

2

3

Ve: 4

Fu: 3 me, 6 mi

Abd. IV

2

— (1+S, 3) ——

5

Ve: 8

VL: 4

Abd. V

——— (S+4–5) ——

1

Ag: 3

VL: 1

Abd. VI

(6+6+1) —————

Ve: 11

An: 1–2 mi*

5

Animal Biodiversity and Conservation 25.2 (2002)

Discussion

Acknowledgements

With its clothing of subequal chaetae, its strong ocular reduction, its large central plate and supernumerary chaetae on head and its reduced chaetotaxy on legs and abd. VI, Pronura bidoup n. sp. is close to Pronura ornata Deharveng & Bedos, 1993 from Doi Inthanon in northern Thailand. Both are limited to moutain forest habitats in their respective region. They differ in their labial chaetotaxy (chaeta f much closer to G than to e in ornata, closer to e than to G in bidoup), their furcal remnant (microchaetae present in bidoup, absent in ornata), and a number of chaetotaxic details. The labium of P. ornata is quite unusual among Paleonurini, with the chaeta f shift towards G like in several other unrelated species of Neanurinae with short buccal cones (like Coecoloba sp., figured in DEHARVENG, 1983).

As the two species share a number of singular characters among Paleonurini, we do not however consider this striking difference in labial chaetotaxy to be phyletically meaningful, though it would deserve deeper investigation.

Prof. Le Cong Kiet (University of Ho Chi Minh City, department of Ecology and Botany) and the Forest authorities of Dalat efficiently organised our expeditions to the Bi Doup massif. Université Paul Sabatier and Bourse Germaine Cousin of the Société Entomologique de France financially supported part of the field work. We also thank an anonymous reviewer for useful comments on an earlier version of the manuscript.

References DEHARVENG, L., 1983. Morphologie évolutive des Collemboles Neanurinae en particulier de la lignée néanurienne. Travaux du Laboratoire d’Écobiologie des Arthropodes édaphiques, Toulouse, 4: 1–63.

DEHARVENG, L. & BEDOS, A., 1993. New Paleonura and Pronura species (Collembola, Neanurinae) from Thailand. Zoologica Scripta, 22: 183–192.

DELAMARE DEBOUTTEVILLE, C., 1953. Collemboles du Kilimandjaro récoltés par le docteur George Salt. Ann. Mag. Hist. Nat., 12(6): 817–831.

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 25.2 (2002)

7

Limits to natural variation: implications for systemic management C. W. Fowler1 & L. Hobbs2

Fowler, C. W. & Hobbs, L., 2002. Limits to natural variation: implications for systemic management. Animal Biodiversity and Conservation, 25.2: 7–45.

Abstract Limits to natural variation: implications for systemic management.— Collectively, the tenets and principles of management emphasize the importance of recognizing and understanding limits. These tenets require the demonstration, measurement and practical use of information about limits to natural variation. It is important to identify limits so as not to incur the risks and loss of integrity when limits are exceeded. Thus, by managing within natural limits, humans (managers) simultaneously can achieve sustainability and minimize risk, as well as account for complexity. This is at the heart of systemic management. Systemic management embodies the basic tenets of management. One tenet requires that management ensure that nothing exceed the limits observed in its natural variation. This tenet is based on the principle that variation is constrained by a variety of limiting factors, many of which involve risks. Another tenet of management requires that such factors be considered simultaneously, exhaustively, and in proportion to their relative importance. These factors, in combination, make up the complexity that managers are required to consider in applying the basic principles of management. This combination of elements is reflected in observed limits to natural variation that account for each factor and its relative importance. This paper summarizes conclusions from the literature that has addressed the concept of limits to natural variation, especially in regard to management. It describes: 1. How such limits are inherent to complex systems; 2. How limits have been recognized to be important to the process of management; 3. How they can be used in management. The inherent limits include both those set by the context in which systems occur (extrinsic factors) as well as those set by the components and processes within systems (intrinsic factors). This paper shows that information about limits is of utility in guiding human action to fit humans within the normal range of natural variation. This is part of systemic management: finding an integral and sustainable place for humans in systems such as ecosystems and the biosphere. Another part of sustainability, however, involves action to promote systems capable of sustainably supporting humans and human activities, not only as individuals, but also as a species. It is important to distinguish what can and what can not be done in this regard.

Key words: Systemic management, Limits, Variation, Ecosystems, Single species, Resources.

Resumen Límites a la variación natural: implicaciones para el manejo o gestión sistémica.— En conjunto, los dogmas y principios del manejo enfatizan la importancia del reconocimiento y la comprensión de los límites. Estos principios requieren la demostración, medida y uso práctico de la información sobre los límites de la variación natural. Es importante identificar los límites para no incurrir en riesgos y pérdida de integridad cuando dichos límites se sobrepasan. Con el manejo dentro de unos límites naturales, el hombre (el responsable del manejo) puede conseguir simultáneamente sostenibilidad y minimización de riesgos, así como explicar la complejidad. Ésto está en el núcleo central del manejo sistémico. El manejo sistémico engloba los principios básicos de cualquier tipo de manejo. Uno de los principios requiere que el manejo asegure que nada exceda los límites observados en la variación natural. Este principio se basa en que la variación está condicionada por varios factores limitantes, muchos de los cuales conllevan riesgos. Otro principio del manejo requiere que estos factores sean considerados simultáneamente, exhaustivamente y en proporción a su importancia relativa.

Dichos factores, en combinación, constituyen la complejidad que los responsables del manejo deben considerar ISSN: 1578–665X

© 2002 Museu de Ciències Naturals

Fowler & Hobbs

8

al aplicar los principios básicos de su función controladora. Esta combinación de elementos se refleja en los límites observados en la variación natural referentes a cada factor natural y su importancia relativa. El presente artículo resume conclusiones extraídas de la literatura científica respecto el concepto de variación natural, especialmente en el ámbito del manejo describe: 1. En qué medida estos límites son inherentes a los sistemas complejos; 2. Cómo se ha reconocido la importancia de estos límites para el proceso de manejo; y 3. Cómo pueden utilizarse para el manejo. Los límites inherentes incluyen tanto los establecidos por el contexto donde los sistemas se desarrollan (factores extrínsecos) como los establecidos por los componentes y procesos internos de los sistemas (factores intrínsecos). La información sobre los límites es útil como guía de la acción humana para acomodar los seres humanos al espectro normal de la variación natural. Esto forma parte del manejo sistémico: encontrar un lugar integral y sostenible para el hombre en sistemas tales como los ecosistemas y la biosfera. Otra parte de la sostenibilidad, sin embargo, implica acciones destinadas a promover sistemas capaces de proporcionar apoyo sostenible al hombre y a sus actividades, no sólo como individuo sino también como especie. Es importante distinguir qué puede y que no puede hacerse a este respeto.

Palabras clave: Manejo o gestión sistémica, Límites, Variación, Ecosistemas, Especies individuales, Recursos.

(Received: 17 IV 02; Conditional acceptance: 30 VII 02; Final acceptance: 13 IX 02) 1

Charles Fowler, National Marine Mammal Laboratory, Alaska Fisheries Science Center, 7600 Sand Point Way N.E., Bin C15700, Seattle, Washington 98115–0070, U.S.A. 2 Larry Hobbs, P. O. Box 51, Big Pine, CA 93513, U.S.A. 1 2

E–mail: Charles.Fowler@noaa.gov E–mail: inlandwhale@schat.net

Animal Biodiversity and Conservation 25.2 (2002)

Introduction Considerable time and effort has been devoted to defining “ecosystem management” (e.g., VAN DYNE, 1969; CLARK & SAROKWASH, 1975; AGEE & JOHNSON, 1988a, 1988b; MITCHELL et al., 1990; COSTANZA, 1992; COSTANZA et al., 1992; GRUMBINE, 1992, 1994a, 1997; S LOCOMBE, 1993a, 1993b; WOODLEY et al., 1993; MAERZ, 1994; MOOTE et al., 1994; WOOD, 1994; ALPERT, 1995; LACKEY, 1995; MALONE, 1995; PASTOR, 1995; STANLEY, 1995; UNITED STATES INTERAGENCY ECOSYSTEM MANAGEMENT TASK FORCE, 1995; CHRISTENSEN et al., 1996; COOPERRIDER, 1996; MANGEL et al., 1996; NOSS, 1996; SAMPSON & KNOPF, 1996; SCHRAMM & HUBERT, 1996; NATIONAL M ARINE F ISHERIES S ERVICE ECOSYSTEM P RINCIPLES ADVISORY PANEL, 1998; COMMITTEE ON ECOSYSTEM MANAGEMENT FOR SUSTAINABLE MARINE FISHERIES, 1999; M C C ORMICK , 1999 and the references therein). This collective effort, in part, was a reaction to the trouble that is encountered in pursuing other forms of management, especially management historically practiced at the singlespecies level and particularly when management is aimed at non–human species rather than humans. These traditional approaches include resource management with approaches based on the concept of maximum sustainable yield (MSY, and its failures; L UDWIG et al., 1993; GOODLAND, 1995; CALLICOTT & MUMFORD, 1997; STRUHSAKER, 1998), pest and predator control, and crop management.

However, management cannot proceed by focusing on ecosystems to the exclusion of comparable consideration of species or individuals. A form of management is needed that includes consideration of individuals, species, and the biosphere —in other words, all of the various levels of biological organization.

These have to be considered in addition to ecosystems. If other levels of biological organization are excluded by restricting focus to ecosystems, management will get into even deeper trouble than already experienced —trouble stemming, in part, from a focus that is too narrow, as experienced by focusing on individual species, or on individuals (e.g., individual humans). Especially problematic is management that assumes that humans can control other species or ecosystems and simultaneously avoid the side effects or unintended consequences of management action (ROHMAN, 1999). Systemic management (management that embodies the principles and tenets of management as developed in the literature on management, to represent the best thinking available, and as shown in appendix 1; see also: FOWLER, 1999a, 1999b; F OWLER & PEREZ, 1999; FOWLER et al., 1999; FOWLER, 2002) avoids these problems by considering and accounting for all levels of biological organization as part of an application of the tenets of management in general. It extends beyond the management of human use

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of natural resources; it also applies in other realms (e.g., CO 2 production or energy consumption: FOWLER & PEREZ, 1999; or social and psychological issues: JOHNSON, 1992; CONN, 1995).

Management, regardless of its form, is based on tenets and principles that are seen as important. Systemic management is no different in this regard, and is based, in part, on the principle requiring that elements of various natural systems be maintained within their normal range of natural variation (RAPPORT et al., 1981, 1985; CHRISTENSEN et al., 1996; HOLLING & MEFFE, 1996; MANGEL et al., 1996; FOWLER, 1999a, 1999b; FOWLER et al., 1999; MCCORMICK, 1999 and references for appendix 2) —a theme treated more thoroughly below as a primary point in this paper. In developing this point, there is documentation of the recognition of this principle, the full history of which deserves more extensive treatment than is possible here.

Part of this history involves the conclusion that adhering to this principle requires the use of empirical information about variation and its limits (FOWLER, 1999a, 1999b; FOWLER & PEREZ, 1999; FOWLER et al., 1999).

The existence of a normal range of natural variation implies that there are limits to such variability, but does not rule out the possibility that natural variation will change over time, space and environmental circumstances (e.g., weather and climate). Thus, variation is itself one of the things that varies; but even it has limits. It is often pointed out that everything has its limits (PIMENTEL, 1966; HYAMS, 1976; RAPPORT et al., 1981; PIMM, 1982; RAPPORT et al., 1985; SALTHE, 1985; O’N EILL et al., 1986; S LOBODKIN , 1986; K OESTLER , 1987; C LARK , 1989; G RIME , 1989; ROUGHGARDEN, 1989; ORIANS, 1990; ANDERSON, 1991; MEADOWS et al., 1992; PICKETT et al., 1992; MCNEILL, 1993; MOOTE et al., 1994; WILBER, 1995; AHL & ALLEN, 1996; CHRISTENSEN et al., 1996; HOLLING, & MEFFE, 1996; MANGEL et al., 1996; NATIONAL MARINE FISHERIES SERVICE ECOSYSTEM PRINCIPLES ADVISORY PANEL, 1998; MULLER et al., 2000; UHL et al., 2000).

Limits are one of the more recognized elements of nature, as frequently seen in the study of ecology. Limits define natural patterns. Most general ecology texts address this concept and many contain words such as limits, or limiting factors in their indices (e.g., ALLEE et al., 1949; BROWN, 1995; DIAMOND & CASE, 1986; EMLEN, 1973; KREBS, 1972; ODUM, 1959; PLATT & REID, 1967; RICKLEFS, 1973). Any automated search of the available ecological or biological literature by using the term “limits” reveals the extent of its importance, especially in the titles and key words of many papers published in the biological sciences. Limiting factors are often treated in terms of the constraints posed by available nutrients, or other resources, but also include the effects of predation and disease on population numbers, biomass, productivity, or species

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numbers. While the concept is generally well developed in a variety of ecological settings, it is most commonly used to describe constraints on population size (and the variation of population numbers or biomass in space and time).

Some aspects of limits are straightforward (usually hard limits, see below). A population cannot use more resources than are available, either in total biomass or numbers of species.

Similarly, consuming nothing is not an option for any species because zero consumption guarantees extinction. An ecosystem cannot constitute more than 100% of the biomass in the biosphere. Other limits are more complicated as exemplified by the population dynamics of any species. The limits set on populations result in central tendencies (commonly called carrying capacity, K) such that any species’ numbers ordinarily tend away from zero and cannot be infinite —they find a dynamic balance. These are systemic limits set by combinations of both intrinsic and extrinsic factors (INGRAM & MOLNAR, 1990), or the soft limits of processes, competing or opposing forces, and related rates. For a population, these factors include disease, resource limitations, metabolic needs, density dependence, social dynamics, life history, body size, temperature, habitat, behavior, reproductive strategy, environmental variation, and predation —the list is virtually endless (PIMENTEL, 1966).

This paper includes a partial review of the literature that addresses limits inherent to natural variation to help bring the concept of limits to its proper place in management. The following material presents a much broader perspective, however, than any focus on populations would allow. There is a bias, nevertheless, in consideration of biological and ecological systems at the expense of attention to physical systems (e.g., variation in tidal cycles, climate change, or river flow). This bias tends to place emphasis on factors exemplified by consumption of energy (by biotic systems), consumption of biomass from the biosphere, production of CO2, and predation rates. It is a primary goal of this paper to stimulate recognition of the concept of limits as a way to guide human action in regard to influence on living systems, as well as finding an appropriate place for humans within such systems. A major question is faced in management: “Can scientifically meaningful 'limits' or 'boundaries’ be defined that would provide effective warning of conditions beyond which the nature–society systems incur a significantly increased risk of serious degradation?” (KATES et al., 2001).

The sections below begin with a consideration of the terminology used to discuss and characterize limits and limitations along with terms used to describe the results of such factors.

Following this, there is a section on the factors that contribute to limitations —those things that do the limiting. It contains a sample of what

collectively comprises the full complexity of nature —or what many call reality. Next is a section containing examples of the kinds of things that are limited. Again complexity or reality is involved because virtually everything finite is limited. The fact that there are risks involved in exceeding the normal range of natural variation is emphasized. These risks are among the factors that contribute to establishing limits (e.g., there are risks to each individual human, exemplified by the risk of death associated with body temperature outside the normal range of natural variation). The paper ends with consideration of the application of information about limits, the role of such information in management, and the definition of management based on such information —systemic management.

Terminology It is helpful to recognize two categories of limits introduced above, each of which will be involved in the remainder of this paper: soft limits and hard limits. Soft limits arise from a balance of forces or competing rates in natural processes.

They are usually invoked long before hard limits are approached and can be exceeded for various periods of time, but not indefinitely. Hard limits include physical limits such as space, or the energy content of a resource. Thus, true sustainability exists only within the combination of limits that govern natural systems, each with its own time scale. Temporal scales for soft limits involve the length of time such limits can be exceeded before systemic restorative (homeostatic) forces prevail.

Appendix 2 presents various quotations from the literature where it is seen that a wide variety of terms are used to deal with the concept of limits to natural variation. Equivalent terms are used in both the scientific and management literature, but in different ways. In scientific publications, various words are used to represent limits that are identified, observed, described and measured. Descriptions often include the ways in which limitation is brought about by the factors involved —the processes of limitation or the elements that contribute to limitation. The terms used in scientific work also describe and identify the things that are limited. In contrast, the literature on management uses the same terminology to stress the point that it is important to do what is possible to maintain systems (such as ecosystems, and their component species or populations) within the normal range of natural variation (tenet 3, appendix 1). The literature also makes it clear that managers are increasingly aware that limiting humans becomes both paramount and the only viable option. It is important to limit action so as to avoid risks, including those of doing things that make other systems fall outside the normal range of their natural variation (appendix 1, MCCORMICK, 1999).

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Constrain Variations on this term are often used to characterize nature and natural processes (appendix 2; FARNWORTH & GOLLEY, 1974; ALLEN & STARR, 1982; PIMM, 1982, 1984; SALTHE, 1985; FISHER, 1986; O’NEILL et al., 1986; STEARNS, 1986; BROWN & MAURER, 1987; GLAZIER, 1987; KOESTLER, 1987; AGEE & JOHNSON, 1988a; GRIME, 1989; GRUBB, 1989; TILMAN, 1989; BURNS et al., 1991; PONTING, 1991; HANNON, 1992; NARINS, 1992; BROWN, 1995; AHL & ALLEN, 1996; HOLLING & MEFFE, 1996; MANGEL et al., 1996; MULLER et al., 2000). As will be seen below, systems place limits on their components and the term constrain is used along with others to convey this concept (e.g., BURNS et al., 1991).

Constraining effects are involved in species interacting with each other (e.g., KNOLL, 1989).

The term constrain is also used in the literature on management but it is applied in two ways.

First, it is used in terms of action (constraining human options, and as a matter of exhibiting constraint). Second, it is used interpretively. That is, empirical information observed in scientific studies is seen as guidance for action —what to achieve in carrying out constraining action. The guidance to be used in management is provided by information about natural limits (AGEE & JOHNSON, 1988a; PICKETT et al., 1992; PONTING, 1991; CHRISTENSEN et al., 1996; FOWLER et al., 1999).

Limit, limitations, limiting These words, and other derivatives of the word limit are used often, again both with respect to characterizing nature (DARWIN, 1953; PIMENTEL, 1966; BATESON, 1972; HYMANS, 1976; LEVINTON, 1979; STANLEY et al., 1983; YODZIS, 1984; O’NEILL et al., 1986; AGEE & JOHNSON, 1988a; BUSS, 1988; CLARK, 1989; ROUGHGARDEN, 1989; ORIANS, 1990; WOODWELL, 1990; ANDERSON, 1991; PONTING, 1991; PICKETT et al., 1992; MCNEILL, 1993; SWIMME & BERRY, 1994; WOOD, 1994; ROSENZWEIG, 1995; AHL & ALLEN, 1996; CHRISTENSEN et al., 1996; NATIONAL M ARINE F ISHERIES S ERVICE ECOSYSTEM P RINCIPLES A DVISORY P ANEL , 1998) and as important to management (HYMANS, 1976; AGEE & JOHNSON, 1988a; ANDERSON, 1991; PONTING, 1991; PICKETT et al., 1992; MCNEILL, 1993; MOOTE et al., 1994; WOOD , 1994; H ARDIN, 1995). The concept of management as a process of limiting human influence is interwoven with the observation and characterization of natural limits.

Threshold, boundary, border The concept of limits is also embodied in words that refer to transition points (see the use of these words or their derivatives in references such as BROWN, 1995; BROWN & MAURER, 1989; CLARK, 1989; ELDREDGE, 1991; HASSELL & MAY, 1989; HENGEVELD, 1990; FUENTES, 1993; MANGEL et al.,

1996; NATIONAL MARINE FISHERIES SERVICE ECOSYSTEM PRINCIPLES ADVISORY PANEL, 1998; SALTHE, 1985). In predator/prey interactions, for example, there are various component processes that result in cyclic or chaotic population dynamics when they exceed certain levels, often referred to as thresholds or boundaries, also reflected in certain forms of single–species population dynamics (e.g., HASSELL et al., 1976). However, bounds and borders also refer to the combination of upper and lower limits that confine sets of viable options (BOTKIN & SOBEL, 1975; CHRISTENSEN et al., 1996). As with other terms, these are also used both in defining and guiding the process of management (e.g., see SCHAEFFER & COX, 1992; FUENTES, 1993) as well as in scientific characterization of nature.

Control This word is also used in reference to the concept of limits, especially in regard to the constraining effects of a system’s influence on its components (e.g., KOESTLER, 1987; O’NEILL et al., 1986; SALTHE, 1985; WILBER, 1995). The collective effects of all parts of a system on any one part are greater than the effects of the one on any other (single part). Following this observation, it is recognized that management cannot ignore the fact that human influence on one component of any complex system results in indirect effects on other parts of the system as well as those systems in within which it occurs (secondary effects: PIMM & GILPIN, 1989; second order effects, ripple effects: D IAMOND , 1989; non–linear effects, domino effects: STANLEY, 1984; “down stream” effects, delayed effects, side effects: PONTING, 1991 —all parts of the unintended consequences of human influence: ROHMAN, 1999) and control is seen as a concept restricted primarily to human endeavor (HOLLING & MEFFE, 1996; MANGEL et al., 1996). Humans have no control over other systems in the sense that no one can change the fact that there will always be secondary (or higher order) effects of human influence, even when control is attempted. This includes the feedback of such effects on humans. There are always unintended consequences (ROHMAN, 1999) to management action and one of the limits experienced in management is the inability to change this fact.

Other terms used in regard to limits and limiting processes include regulated (LEVIN, 1989), governed , restricted , restrained , confined , proscribed , suppressed, curtailed, channeled, circumscribed, curbed, contained, barriers (CLARK, 1989), and resistance.

Still more terms are involved in characterizing the results of limitations seen in the empirically observed limits to variation. Such characteristics are the qualities of the limits seen in variation (e.g., range spanned), and the kinds of variation observed (e.g., bimodal or unimodal) within the normal ranges of variation between upper and

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lower limits. Natural variation is constrained by both upper and lower limits. Limits, constraints and risks do not always increase or decrease monotonically. The combined effects of the numerous limitations, as they act in concert, are even more complicated. An example that is easy to relate to as individual human beings is the risk of mortality from various factors —risks that increase for body weight, blood pressure, and body temperature both above and below the midpoints of the ranges that they span (e.g., see C ALLE et al., 1999, and references therein, regarding weight). Therefore, upper and lower limits preclude many options; they function to allow as the only viable alternatives those seen between upper and lower limits. The remaining options are usually realized with their greatest frequency at some midpoint between the limits.

Thus, there is always an emergence of central tendencies between upper and lower limits.

Limits often operate as opposing forces (often soft limits), and the collective balance found in such opposition contribute to the formation of patterns in nature (e.g., see the stochastic analog of equilibrium; BOTKIN & SOBEL, 1975; CHRISTENSEN et al., 1996). There is terminology associated with these patterns, or central tendencies, just as there is for the consideration of any single component among the factors that contribute to limiting natural variation.

Mean, mode and median Statistical names for the measure of central tendencies include terms such as these (SNEDECOR, 1956) to refer to the magnitude of the central tendency (i.e., its position) within the infinite range of options among real numbers.

Kurtosis and skewness These terms refer to the position and concentration of central tendencies with respect to the upper and lower bounds of variation (SNEDECOR, 1956).

Kurtosis refers to the distance between the central tendency and its limits, the concentration of observed measures near the central tendency, or the flatness and spread of the distribution.

Skewness relates more to the degree to which there is a lack of symmetry in the variation. Thus, both terms are used in regard to the shape of the frequency distribution (or probability distribution) of empirically observed variation. Various mathematical models (e.g., log normal, binomial, Poisson, and others, SNEDECOR, 1956) are available to represent the probability distribution of variation in its different forms. Transformations are often used to convert measures showing non–symmetric distributions to more symmetric or normal distributions (especially log transformations, LIMPERT et al., 2001).

Terminology is not confined to the concept of limits, measures of limits, or the characterization

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of variation within limits as treated above.

Various terms are also used in reference to the processes that contribute to the production or origin of central tendencies, especially their positions. Naturally, these include the limiting processes that affect constraint above and below the central tendencies. However,, such processes also include other factors, such as processes involving replication or positive feedback that contribute to the position of central tendencies through the accumulation of more numerous examples in the regions of central tendencies.

Homeostasis, balance and feedback These terms are examples of words regarding the processes that contribute to the origins of central tendencies (as opposed to simple constraint). Specific examples of the elements involved in these processes will be considered below. These processes operate in conjunction with all other processes in nature as none can operate in isolation from the others. The results of the synergistic combination of all the processes are the patterns observed to characterize nature (ALLEN & STARR, 1982) —often seen as emergent patterns (KAUFFMAN, 1993; EL–HANI & EMMECHE, 2000) that include the stochastic analog of equilibrium (BOTKIN & SOBEL, 1975; CHRISTENSEN et al., 1996). These processes are part of what the various species (including humans, tenet 9, appendix 1) are exposed to by being part of systems such as ecosystems.

Integrity, balance and normal (or natural) These are terms related to such patterns as those that make up, or characterize, natural systems (e.g., GRUMBINE, 1994a) often found in the titles of papers describing nature (e.g., WILLIAMS, 1964).

Many of these patterns are correlative, meaning that the magnitude of the mean of a variable is related to that of another variable (measure) as exemplified by the relationship between the central tendency of population density and body size for animals (fig. 1, see also DAMUTH, 1987; P ETERS , 1983). Others relate to the physical environment as found in relationships between geographic range size and latitude (e.g., STEVENS, 1992) or predation rates and temperature. The word integrity is sometimes used with regard to management objectives in the sense of achieving normal states of nature (e.g., KARR, 1990). Balance is often seen as a property of nature in view of the limits to variation (e.g., PIPER, 1993) and something that occurs in spite of variation (i.e., equilibria are rarely static properties of nature, especially biological systems; BOTKIN & SOBEL, 1975; CHRISTENSEN et al., 1996).

There is yet another set of terms used to characterize statistical outliers, extremes, or things beyond the normal range of natural variation (e.g., beyond the limits, MEADOWS et

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log10(density (density,, n/km2)

5 4 3 2 1 0

–1 –2 –3

–2

–1 –0 1 log10(body mass, kg)

2

3

4

Fig. 1. Population density of 368 terrestrial mammalian herbivore species in relation to adult body mass (DAMUTH, 1987; FOWLER & PEREZ, 1999) as an example of variation in one measure of a species in relationship to variation in another.

Fig. 1. Densidad de población de 368 especies de mamíferos herbívoros terrestres en relación con la masa corporal de los adultos (DAMUTH, 1987; FOWLER & PEREZ, 1999) como ejemplo de variación de una medida en una especie respecto a la variación en otra especie.

al., 1992), especially as cases subject to the risks of limiting factors and include words such as abnormal , pathological , deviant , aberrant , atypical, and anomalous. The word unnatural is also used but must be treated with care.

Everything happens naturally and extremes beyond the normal ranges of natural variation are subject to the natural limits and risks that make such extremes rare. Thus, it is not so much unnatural, as it is abnormal, to observe a characteristic or condition (such as a fever) as an extreme. Extreme fluctuation is abnormal (CHRISTENSEN et al., 1996) as is often observed for populations. Thus the term pathological , or carcinogenic is used in reference to human overpopulation (CALHOUN, 1962; BATESON, 1972; HERN, 1993). At the ecosystem level pathology is also used to describe problems when atypical conditions arise (e.g., RAPPORT, 1989a). These are words that help clarify the distinction between the natural occurrence of extremes and things that fall in the normal range of natural variation.

Factors contributing to limits: complexity I Limiting factors combine in nature to make up an interconnected set of forces, risks, and constraints.

A major part of scientific endeavor is dedicated to documenting these factors and the lists that are available now, while long, only scratch the

surface of the complexity of reality —even in their combination. The entire complexity within and among natural systems contributes to both the collective constraints on variation and to the formation of the central tendencies within such variation (e.g., see PIMENTEL, 1966 regarding limits to population size) as introduced above. Research on the limits to variation in biological systems has resulted in the recognition of a great many contributing factors and an exhaustive list is beyond the scope of this paper. However, there are examples worth mention, some of which are found in appendix 2.

A great deal of literature has accumulated from studies of the factors that limit population size. There is a long list, and various categories of such factors are considered to be of importance.

Among such categories are parasites, predators, disease, behavior (COHEN et al., 1980), energy, resources (food, prey), space, competition, and nutrition (including needs for individual elements and their compounds such as amino acids) —all subjects of a long history of research on population ecology and represented by a sample of references in appendix 2 (e.g., PIMENTEL, 1966; FARNWORTH & GOLLEY, 1974; O’NEILL et al., 1986; TILMAN, 1989; MCNEILL, 1993). Other factors include limits on the options for life history strategy especially as related to body size (DAMUTH, 1987), or the options for population growth and kinds of mortality as related to life history strategy (FOWLER, 1988).

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The limitation of populations by microorganisms (diseases or pathogens) or other pests has been of special focus in many studies and are factors recognized by PIMENTEL (1966), FARNWORTH & GOLLEY (1974), STANLEY et al. (1983), and TILMAN (1989). A review of such limitations has been conducted by M C C ALLUM & D OBSON (1995).

However, it is clear that microscopic or small bodied consumers are not the only category of species known to contribute to the limitations on the population size of their hosts. Consumer species that are of larger body size than their consumed prey/resources are also involved (e.g., predators and herbivores; STANLEY et al., 1983; O’NEILL et al., 1986; MCNEILL, 1993). Whether microscopic or not, the degree to which one species acts to limit the population of another varies from case to case. Removing predators experimentally to rid their resources of such influence often results in population increases, but not always. Limiting influence is thus only a tendency and rarely predictable owing to the complicated nature of the interactions and factors that influence them (PIMM, 1991). In the final analysis, mortality caused by consumers or disease count among the many factors that contribute to limiting population size but are not the only factors involved.

Sunlight provides the energy that is passed through the food webs of communities and ecosystems. This energy is involved in metabolism, growth, reproduction and survival. It is not limitless in its flow through biological systems, however, and is among the factors that have been studied for a variety of such systems from cells to the biosphere. As such, energetic constraints are not confined to setting limits on population size and the various limits involving energy are represented by a voluminous literature. Energy has been noted as a limiting factor in a variety of biological systems by BROWN (1981), PIMM (1982, 1984), YODZIS (1984), BROWN & MAURER (1987), GLAZIER (1987), GASTON (1988), TILMAN (1989), and HANNON (1992). Energy is clearly not the only limiting factor for biological systems. The more general issue of resources (including nutrients of various kinds) as constraining factors is often noted (STANLEY et al., 1983; O’NEILL et al., 1986; MCNEILL, 1993), occasionally as expressed through competition (PIMENTEL, 1966; STANLEY et al., 1983).

Another important resource is space (or habitat size). Thus, space is also frequently identified as a limiting factor, including its limitations on species numbers in addition to its constraints on population size (e.g., STANLEY et al., 1983; O’NEILL et al., 1986; ROSENZWEIG, 1995; BROWN, 1995).

Extinction is also a limiting factor (BROWN & MAURER, 1987), perhaps an ultimate limiting factor (at times a soft limit with a long time scale), and one that has its effects on species numbers, diversity, communities (ARNOLD & FRISTRUP, 1982; F OWLER & M AC M AHON , 1982; G OULD , 1982;

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ELDREDGE, 1985; KITCHELL, 1985; LEVINTON, 1988; BROWN, 1995; ROSENZWEIG, 1995), and body size (i.e., as a contributing factor in limiting the maximum size observed among species, e.g., see VAN VALEN, 1973; BARANOSKY, 1989; FOWLER & MACMAHON, 1982; BROWN, 1995). Thus, extinction at the species–level, like death at the individual– level, is one of the risks associated with the extremes characterized as pathological or abnormal. Extinction is a limiting factor that also exemplifies a process rather than a physical entity in its limiting action (soft limit in involving long time scales).

Other limitations involve morphological factors (PIMM, 1982, 1984; FISHER, 1986; BROWN, 1995), functional, historical, and evolutionary elements (PICKETT et al., 1992), physiology, and behavior (BROWN, 1995), various population dynamical forces (as well as other dynamics; P IMENTEL , 1966; LEVINTON, 1979; PIMM, 1982, 1984; ROSENZWEIG, 1995), environmental predictability (LEVINTON, 1979), environmental heterogeneity (PIMENTEL, 1966), evolutionary forces (including genetic feedback mechanisms, PIMENTEL, 1966; FOWLER & MACMAHON, 1982; PIMM, 1984), and the availability of genetic (raw) material (GRUBB, 1989). Nutrition, space, toxic materials, competition, predation, cannibalism, and stress are all limiting factors (ROSENZWEIG, 1974). There is little, if anything, that can be ignored in the complexity of factors that limit variability (PIMENTEL, 1966).

It must be recognized that there are two more closely interrelated categories of limiting factors (each involving both hard and soft limits) depending on whether they are extrinsic or intrinsic to the system showing variation (INGRAM & MOLNAR, 1990). Variation limited by extrinsic factors in biological systems includes the effects of disease, predation, competition, habitat size, and resource availability on population size.

Intrinsic factors limiting population size include, body size, behavior, and the birth and death rates involved in life history strategies. At the same time such factors are observed to contribute to limitations, they also have their influence on the position of central tendencies. Intrinsic and extrinsic factors are involved in the limitation of any system and its interactions with other systems.

As amplified in the next section, there are a variety of levels of biological organization to which limiting factors apply. These span the range from sub–cellular structures, to cells, organs, individual organisms, populations, species, communities and ecosystems, through to biomes and the biosphere. It is easy to find examples of limiting factors for each level of biological organization. At the individual level, body size is limited by extrinsic factors such as food availability, and intrinsic factors such as metabolic dynamics. This list goes on to include mortality at the individual level, and extinction at the species level. At the community or ecosystem level, species numbers are limited

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extrinsically through factors exemplified by energy and space, and intrinsically by evolutionary factors and population dynamics. Collectively, all species in an ecosystem interact with each other such that each one is subject to the constraints emergent from the combined effects of the others.

This happens in all systems such that the extrinsic factors that impose limits include those through which a system poses limits to its parts or its components (e.g., AHL & ALLEN, 1996; MULLER et al., 2000). These include the processes of natural selection involving death and extinction.

Both intrinsic and extrinsic factors operate simultaneously and collectively in natural systems (INGRAM & MOLNAR, 1990) —sometimes reinforcing, sometimes nullifying each other. The degree to which such things happen varies from case to case. Furthermore, synergistic effects and interactions among such factors are common. The combined action of such factors result in observed patterns (e.g., as observed in the results of various forms of natural selection; ARNOLD & FRISTRUP, 1982; FOWLER & MACMAHON, 1982; GOULD, 1982; LEVINTON, 1988). Thus, patterns are the results of systemic effects, or the effects of the entire suite of limiting factors and all of their interactions.

Some of these patterns in nature are partially explained by the balances that result from limiting factors that function to reinforce or oppose one another. Balances resulting from the latter are especially important in observed patterns.

Extinction acting to limit the options for natural selection at the individual level provides a good example (ALEXANDER & BORGIA, 1978; FOWLER & MACMAHON, 1982; GOULD, 1982; LEVINTON, 1988).

Other patterns result from parallel, or reinforcing, effects. Examples of factors that may work in concert are seen in the interplay of body size, population size and geographic range (BROWN & MAURER, 1987; GASTON & BLACKBURN, 2000) on extinction rates. Species of large body size and species with small geographical ranges appear to have higher extinction rates. This may contribute to there being fewer species that are large bodied with small geographic ranges compared to species with small bodies and large ranges.

The things with constrained variation: complexity II Limitations are imposed on all components and processes at each level of biological organization.

Whether it be a cell, physiological process, population, predation rate, total population biomass, speciation, or number of species, it is something with variation that is subject to limits.

This section turns from the things that exert limiting influences reviewed in the previous section to examples of the things that are subject to limitations. These include such things as body size, blood pressure, and heart rates for individual animals. The components of ecosystems and

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ecosystems themselves are also subject to limitations (NATIONAL MARINE FISHERIES SERVICE ECOSYSTEM PRINCIPLES ADVISORY PANEL, 1998; HAGEN, 1992).

Population size and population variation are limited. There is a voluminous literature treating limits to population size (e.g., HOLLING, 1966; PIMENTEL, 1966; FARNWORTH & GOLLEY, 1974; O’NEILL et al., 1986; GLAZIER, 1987; SINCLAIR, 1989; TILMAN, 1989) that cannot be ignored. Many things that limit population size per se are also factors that limit population variation which is limited within species as well as among species (SPENCER & COLLIE, 1997; FOWLER & PEREZ, 1999). Variation in general is limited and population variation is an example (BUSS, 1988; HOLLING, 1966; O’NEILL et al., 1986).

The results of work on populations serve as an example of insight that would be expected for other aspects of biological systems had they been the subject of equivalent study.

Other factors are far from ignored, however. In addition to population size and variation, the limits in variation have been shown for a variety of biological processes and dynamics. The evolutionary process is not free of limitations (e.g., GRUBB, 1989).

For example, the extent of evolutionary change is limited (F ISHER , 1986) because evolution is “channeled” by various constraints (GRIME, 1989).

The general concept is exemplified by the lack of evolutionary options as limited by cell structure.

There are no single celled organisms that weigh a metric ton. Other processes are also limited. The behavior of organisms and its evolution is limited (NARINS, 1992). The variety of dynamics of (and within) communities and ecosystems are limited (LEVIN, 1989; PIMM, 1982). These include the flow of energy among species (owing to the limitations established by the inefficiency of metabolic, photosynthetic, and digestive processes). As will be seen, processes such as predation, CO 2 production, reproduction and mortality all fit within limits.

The size of cells and the qualities of individual organisms are limited just as the qualities of populations and ecosystems are (again by both intrinsic and extrinsic factors, INGRAM & MOLNAR, 1990; HAGEN, 1992; TILMAN, 1989). The characteristics and qualities of species are limited by, among other things, a variety of evolutionary processes as well as intrinsic factors. Among species groups, attributes are limited by selective extinction which often involves intrinsic and extrinsic factors operating in concert (ARNOLD & FRISTRUP, 1982; FOWLER & MACMAHON, 1982; GOULD, 1982; STANLEY et al., 1983; LEVINTON, 1988). There are limits to diversity (HUTCHINSON, 1972; INGRAM & MOLNAR, 1990).

Other factors that are subject to limits include range size (PAGEL et al., 1991; STANLEY, 1989; GASTON & BLACKBURN, 2000), the total number of species (VALENTINE, 1990) and length of food chains (PIMM & LAWTON, 1977; LEVINTON, 1979; PIMM, 1984; YODZIS, 1984). Variation within and among ecosystems and that of ecological

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communities are constrained by the influence of factors such as selective extinction (ALEXANDER & BORGIA, 1978; FOWLER & MACMAHON, 1982; ARNOLD & FRISTRUP, 1982; GOULD, 1982; ELDREDGE, 1985; KITCHELL, 1985; LEVINTON, 1988; HERRERA, 1992; GASTON & BLACKBURN, 2000), including limitations on the numbers of species (e.g., the size of the membership of a community as the count of species, ROUGHGARDEN, 1989; GLAZIER, 1987) or species richness (LEVINTON, 1979). The numbers of species consumed by a consumer and the number of consumers that consume a particular prey species are constrained (MARTINEZ, 1994). The qualities of species involved in communities and ecosystems are limited as exemplified by the small number of species with large body size compared to small–bodied species (FOWLER & MACMAHON, 1982; BROWN & MAURER, 1987). Within communities and ecosystems the number of trophic levels are limited (ROSENZWEIG, 1995).

Constraints influence most of the patterns and dynamics of (and within) communities and ecosystems (LEVIN, 1989; PIMM, 1982).

The components of systems are limited, among other things, by the systems of which they are a part. There is a substantial body of literature that presents a helpful interpretation of the collective effects of limiting factors —that is, the limitations resulting from the suite of all factors acting together, regardless of what is being limited. In such work, it is pointed out that the collective effects of complex systems control, constrain or otherwise limit their components (e.g., DYLE, 1988; KOESTLER, 1987; O’NEILL et al., 1986; SALTHE, 1985; WILBER, 1995; MULLER et al., 2000). An example would be the limiting influence of an ecosystem on its component species and their populations (O’NEILL et al., 1986).

Such work adds to the importance of the observation that everything is subject to limits.

Everything (everything finite) is part of a more inclusive system which includes all of the factors that contribute to setting limits. Thus, within biological systems, each thing chosen for scientific study will be limited by the more inclusive or collective level of biological organization of which it is a part, along with the non–biological elements and processes of its environment (sometimes referred to as context, appendix 1). This is a matter of scale as noted by AHL & ALLEN (1996) who point out that small–scale entities are limited by the larger scale entities. Much of the literature makes the point more generally: all components of more inclusive systems are limited by the collective influence of the factors to which they are exposed (e.g., BATESON, 1972; ALLEN & STARR, 1982; MAYR, 1982; SALTHE, 1985; O’NEILL et al., 1986; KOESTLER, 1987; BUSS, 1988; ORIANS, 1990; BURNS et al., 1991; MCNEILL, 1993; AHL & ALLEN, 1996; MULLER et al., 2000). And everything finite is a component of some larger system (WILBER, 1995).

It must be concluded that everything is subject to limits in its natural variation.

Personal experience emphasizes this fact.

Perhaps this is recognized most clearly in observing that humans are limited in what can be known (FOWLER et al., 1999) or what can be conceptualized (MCINTYRE, 1997). Thus, not only are there limits to what can be done and what humans can be, but humans are limited in what can be understood.

Knowledge itself is limited. In part, the experience of these limits, along with other limitations, is related to the fact that finite things are, by their very nature, limited. The models used to represent things can not be all inclusive and the results of exercises based on models are thereby subject to error; being limited, models are real but not reality, just as maps are not the territory (BATESON, 1972, 1979; models are never the reality they represent). Thus, science is limited. This is experienced in the inability to recombine information from the things that are studied (what might be called the Humpty–Dumpty effect, or syndrome, NIXON & KREMER, 1977; DUNSTAN & JOPE, 1993; REGAL, 1996; HORGAN, 1999). Even more of the limits of science are experienced in the inability to adequately or accurately assign importance to the influence (limiting or otherwise) of each factor made the focus of research (ALLEN & STARR, 1982; BARTHOLOMEW, 1982; ROSENBERG, 1985; SALTHE, 1985; GROSS, 1989; PETERS, 1991; PICKETT et al., 1994).

There is a continued experience of limitations in progression from science (e.g., PETERS, 1991; S TANLEY , 1995) to management. As already mentioned, the options for management are limited in that humans cannot control the fact that there will always be unintended consequences to management action. There is no control over other systems to avoid such effects. The tenets of management limit what can be done; they are based on principles that exert a form of natural selection among the options. Humans are limited, as in everything else, in management. It is time to manage with limits in mind.

Utility / practical application Patterns arise, in part, from the limits to variation resulting from the vast array of inter-relationships among the various elements of nature operating simultaneously. Variation itself, both within, and as a part of pattern, is also a product of this complexity. Everything is subject to the influence of the elements in its environment (context, BATESON, 1972, and extrinsic factors) along with the influence of its components (WILBER, 1995; intrinsic factors). Are these observations of no more than philosophical interest? Many can be easily documented or experienced personally, but of what use are they?

One tenet of management requires that things (e.g., biological systems and processes) be maintained within the normal range of natural variation (tenet 3, appendix 1). There is an

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especially important element of responsibility for implementing this element of management with respect to biological systems. Such requirements have long been recognized in human and veterinary medicine. This is now being extended to ecosystems and all of their components, including humans (e.g., CHRISTENSEN et al., 1996; MANGEL et al., 1996; MCCORMICK, 1999, appendix 1 and 2). Various panels and groups convened to address the management process (especially at the ecosystem level) have reached the conclusion that this is an essential tenet of management (e.g., NATIONAL MARINE FISHERIES SERVICE ECOSYSTEM PRINCIPLES ADVISORY PANEL, 1998, appendix 2). MOOTE et al. (1994) were clear that ecosystems and natural patterns are the result of limits and that humans have the responsibility to fall within such limits.

Managers are responsible for doing what can be done to ensure that ecosystems fall within the normal range of natural variation. However, this conclusion is not restricted to individuals, species, ecosystems or communities. It applies to nature (e.g., combinations of biological systems) in general (e.g., DARWIN, 1953; PICKETT et al., 1992; SALZMAN, 1994; WOOD, 1994; CHRISTENSEN et al., 1996; NATIONAL MARINE FISHERIES SERVICE ECOSYSTEM PRINCIPLES ADVISORY PANEL, 1998). Management should be carried out by doing everything possible to ensure that biological systems fall within their normal range of natural variation. Doing so is at the core of systemic management.

Part of the concept of normal involves what is natural. Much of the literature on management emphasizes the importance of doing things to maintain or recover natural states regardless of whether it is for individuals, species, communities or ecosystems. Recent literature regarding ecosystems illustrates the progression in the development of this concept from its acceptance at the individual level to its application at higher levels of biological organization (HOLLING & MEFFE, 1996; MANGEL et al., 1996; RAPPORT et al., 1981, 1985; DAVIS & SIMON, 1994; CHRISTENSEN et al., 1996; FOWLER, 1999a, 1999b; FOWLER et al., 1999). The word intact is used to refer to systems that are “healthy” or “undamaged” (ANDERSON, 1991). Such concepts are meaningless without frames of reference. Thus, “natural” patterns are often seen as those that fall within the normal limits of variation, not only for physical structure but also for natural processes. There is need for care here. It is important to be mindful of the fact that it is natural for there to be occasional outliers as examples beyond the normal range of natural variation and when such occasions arise, they are subject to the natural effects of limits (i.e., the natural phenomena that set limits, pose risks, and prevent the occurrence of more such extremes —risks exemplified by death and extinction).

It is also important to account for human influence. There are few if any systems left on the planet that have not been subjected to abnormal human influence and the problem of providing

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reference points is growing (D AYTON , 1998).

However, all species influence their ecosystems and the other species in such systems. The extent of human influence would not be a particularly large problem if anthropogenic effects were not themselves abnormal as will be seen in the sections ahead. As a result of the extensive human influence it is important to define “normal” and “natural” so as to focus more on situations wherein human influence itself is not abnormal; that is, within the range of natural variation of influences that other species exhibit.

Attempts to apply the concepts of “normal” and “natural” include efforts to return ecosystems to normal states. However, restoration (e.g., ecosystem restoration, JORDAN et al., 1987) cannot be a recovery of the past —a clear hard limit is the irreversibility of time. It is possible to learn from history, and seek guiding information from patterns historically observed, but it is impossible to reconstruct what existed in the past. Change is a permanent part of the processes that cannot be avoided, especially change resulting from action taken in management.

When considering management, it is impossible to escape the concept of what should be and hence, the matter of ethics. The material presented here is based on the assumption that the tenets that have been accepted in the literature are, in fact, important. Tenet 3 (appendix 1) emphasizes the importance of acting so as to facilitate any biological system’s falling within its normal range of natural variation (whether such a system be a cell, organ, individual, population, species, ecosystem or the biosphere). It is worth pointing out, however, that there are religious elements to the ethic behind this tenet that are of long standing importance (e.g., CLARK, 1989; PONTING, 1991). An in–depth treatment of ethical issues, or their history, is beyond the scope of this paper.

Another tenet of management is that of having measurable goals and objectives; there need to be norms, standards, reference points, guidelines and criteria to go by (tenet 7, appendix 1). These are provided through systemic management: the central tendencies and statistical confidence limits observed in natural variation provide such guidance.

They represent options that are optimal in minimizing risk —not just any particular set, but all risks working in concert. These risks and constraints are the entire suite of factors experienced by systems such as cells, species, or individuals in the real world. Thus, the empirically observed central tendencies fall between the upper and lower limits observed for variation subject to the all limiting factors of the real world acting synergistically. Therefore, understanding limits, and taking advantage of the results of their action, provides a great deal to go on in this regard and provides hope of implementing sound management (DARWIN, 1953).

This is the concept behind the medical perception of health when action is taken to

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restore body temperature, blood pressure, or body weight that is abnormal. Thus, the normative concept of health can be applied whether to individuals (e.g., in maintaining proper cholesterol or blood sugar levels) or ecosystems (RAPPORT, 1989b; E HRENFELD , 1993; H OLLING & MEFFE , 1996) by implementing the concept of evaluation with regard to normal variation (KING, 1993). Just as processes within individuals (e.g., metabolism, digestion, respiration) are important to management in this regard, so are the processes within the higher levels of biological organization, such as nutrient flow in ecosystems (e.g., HOLLING & MEFFE, 1996). Other ecosystem features that are subject to limited natural variation include numbers of species, trophic structure, energy storage, population variation and total biomass levels.

How are the goals and standards from central tendencies of use? Such information can be used to evaluate both human and non–human systems.

What happens if the characteristics of an ecosystem are outside the normal range of natural variation? Direct management of ecosystems is impossible because of the lack of control over ecosystems (EHRENFELD, 1981; MCNEILL, 1989; HOLLING & MEFFE, 1996; MANGEL et al., 1996; COMMITTEE ON ECOSYSTEM MANAGEMENT FOR SUSTAINABLE MARINE FISHERIES, 1999; FRANCIS et al., 1999). That is, management cannot be carried out to avoid many of the effects of attempted control (whether it be control of other individuals, species ecosystems, or the biosphere); many such consequences are unintentional and unpredicted. However,, humans do influence ecosystems, as do all species. Both past and present human influence has resulted in ecosystems that exhibit abnormal qualities, but influence is something that every species has.

Human influence may be interpreted as a limited form of control over ecosystems, but management can not control the fact that there will be unintended consequences (ROHMAN, 1999) as the side effects of influence. This lack of control is one of the limitations that is experienced in management in general. It is impossible to exert influence and, at the same time, know or control all of the effects. In part, the lack of control stems from being a part of ecosystems —humans are components (and the human species is a component, tenet 9, appendix 1) subject to the collective limits described above (BATESON, 1972; O’NEILL et al., 1986; KOESTLER, 1987; O’NEILL et al., 1986; SALTHE, 1985; WILBER, 1995).

So where do the central tendencies have practical application? How can management use such information in view of the fact that all influences lead to secondary (or other higher order) effects, at least some of which will result in feedback over various scales of time that places (or will place) limits on humans? The 8th tenet of management (appendix 1) is based on the fact that the elements over which there is most control are the human elements, recognizing that even in self control there will be

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ramifications in the rest of the systems of which humans are a part. Some of these effects will be desirable from certain points of view, but others will be negative (that is, many of the effects of management action will result in feedback that will have limiting effects on individual humans and our species). All effects would be positive if managers had full control, but it is humanly impossible to control or predict which will be beneficial and which will not (WOOD, 1994). Even taking mitigating action to avoid influences beyond those intended will always have its unintended consequences. There is one remaining alternative. It is the option of exerting self control (intransitive or passive management in which humans regulate what humans do, MCCORMICK, 1999). To exercise this option humans do everything possible so that humans fall within the normal range of natural variation, guided by central tendencies.

This is a critical point. What it means to management is: humans undertake change to exert influence and exhibit characteristics so as to be a part of biological systems in which humans fall within the normal range of natural variation (DARWIN, 1953; OVINGTON, 1975; PICKETT et al., 1992; FUENTES, 1993; MCNEILL, 1993; GRUMBINE, 1994b; MOOTE et al., 1994; SALZMAN, 1994; WOOD, 1994; MANGEL et al., 1996; CLARK, 1989; UHL et al., 2000).

As suggested by APOLLONIO (1994), humans have the alternative of mimicking other species. Other species serve as empirical examples of sustainability.

Mimicking can be accomplished by ensuring that humans fall within the normal range of natural variation (especially in finding positions near central tendencies as standards of reference, or management guidelines, FOWLER et al., 1999). This amounts to an extension of biomimicry (BENYUS, 1997) to the species level to address not only questions about how to feed ourselves, but also how many humans there should there be to feed.

Alternatively it can be viewed as parallel to the process of benchmarking in business management (SPENDOLINI, 1992; BOGAN & ENGLISH, 1994; BOXWELL, 1994; CAMP, 1995), with hierarchical options. First, managers can find the advisable constraints on what businesses are and do (as in conventional benchmarking), and secondly, managers can address the meta–level question of whether or not any particular business should even exist, and if so at what level they carry out their functions and influence. It is an application of restoration ecology to restore human involvement in nature so as to fall within the normal range of natural variation.

Nature has been carrying out a form of adaptive management (HOLLING, 1978; WALTERS & HILBORN, 1978; WALTERS, 1986) over evolutionary time scales so that it is now possible to take advantage of eons of natural experiments with sample sizes involving millions of trials. In short, it is possible to learn from nature (GRUMBINE, 1994b), or learn to live as humans by observing other species, much in line with the philosophy of Thoreau and Muir

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(who saw “...sensitive observation of nature as the source of wisdom,” NORTON, 1994), or Leopold “who pointed out that wilderness provides a ‘base– datum of normality’” (CHRISTENSEN et al., 1996).

The degree to which current forms of management are transitive varies. Terrestrial systems are often more engineered in agricultural practices than are marine systems (however, aquaculture is quite transitive in this regard).

Most fisheries are managed by controlling the fishing effort; nevertheless fish populations are transitively driven to predetermined levels to elicit desired productivity without serious or exhaustive consideration of the systemic consequences. No such transitive management has withstood the test of evolutionary time scales and such approaches fail to acknowledge the track record of human failure in similar circumstances in terrestrial settings (e.g., PONTING, 1991).

Regardless of context, however, what is being done in most of current management ignores limits as they apply to humans. Management fails to place humans within the normal range of natural variation in conventional approaches —a fact that is often mentioned in the literature on management and especially in literature critical of conventional management practices (e.g., GADGIL & BERKES , 1991). This point is made repeatedly in work that draws empirical information produced in scientific studies to the attention of society, particularly managers.

Shortcomings and failures are most clear with regard to management at the ecosystem level where the need for changes and alternatives are emphasized (e. G ., A GEE & J OHNSON , 1988a).

However, among scientists, the full importance of limits is not always recognized (GRUBB, 1989).

Socially, freedom is often confused with ignoring the laws of nature (JOHNSTON, 1991). PIANKA (1974) sees a generic pattern in human failure to see the wisdom of finding a place (“balance”) between upper and lower limits. Many of the world’s problems today can be attributed to the lack of this mode of management (WOODWELL, 1990).

Continuing to ignore limits is no longer a tenable option (CLARK, 1989; MANGEL et al., 1996; NATIONAL M ARINE F ISHERIES S ERVICE ECOSYSTEM P RINCIPLES A DVISORY P ANEL , 1998). It is of paramount importance to find a place for humans within the normal limits of natural variation. As will be seen later in this paper, there are many cases where humans are so far outside the normal range of natural variation that other elements of biological systems have responded to show abnormal variation themselves (CHRSITENSEN et al., 1996). In the end, there is really no choice but that of finding the human place within the limits of the systems of which humans are a part (MCNEILL, 1993). The effects already caused by the cases of human abnormality, or pathology, continue to unfold through delayed consequences. Hopefully these are not so extreme as to preclude otherwise viable options for management. The risks resulting

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from past actions are risks that are yet to be faced (OVINGTON, 1975) and the remaining hope is that actions taken now will both avoid further risk as well as reduce risk from past mismanagement. One of the challenges will be to conduct research that provides needed information (ORIANS, 1990; K ATES et al., 2001, tenets 5 and 6, appendix 1). This clearly includes demonstration of the central tendencies of natural variation, and displaying them in graphic form (FOWLER & P EREZ, 1999). These central tendencies occur between limits. As maintained by CLARK (1989), one of the main functions of scientific endeavor is the production of information about limits —they bound the central tendencies and present managers with viable options to address one of the main questions of sustainability science (as quoted in the introduction, KATES et al., 2001).

Discussion: systemic management, a move in the right direction What happens if management follows the guidelines established to avoid the problems created by current approaches? The various tenets of management in appendix 1 have been developed over the last several decades in trying to solve management problems (e.g., CHRISTENSEN et al., 1996; MANGEL et al., 1996; NATIONAL MARINE FISHERIES SERVICE ECOSYSTEM PRINCIPLES AAVISORY PANEL, 1998; UNITED STATES INTERAGENCY ECOSYSTEM MANAGEMENT T ASK F ORCE , 1995; C OMMITTEE ON E COSYSTEM MANAGEMENT FOR SUSTAINABLE MARINE FISHERIES, 1999; MCCORMICK, 1999). Can management adhere to them? Is it possible to avoid exacerbating problems inherited from past actions while expanding the scope of management? Is it possible to include ecosystems or the biosphere without giving up on species or individuals as important levels of biological organization to which management applies? The implementation of systemic management will lead toward accomplishing these objectives (even if there is no guarantee that future problems from the failures of past management can be avoided). It is a form of management that emerges from past practices and draws on the lessons learned from experience. As stated at the outset, it embodies the principles that have emerged from concerted effort to deal with problems that have not been avoided in traditional management. The following sections provide more depth to the definition of systemic management.

There is progress toward systemic management seen in some of the conclusions reached in attempts to develop management at the ecosystem level (“ecosystem management”). One conclusion is particularly important. As reviewed above, it is not possible to manage ecosystems, but, at the same time, it is imperative that ecosystems be taken into account —along with the rest of complexity (especially in managing

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human interactions with various biotic systems).

It is important that management proceed in ways that apply, not only at the ecosystem level, but also at the levels of individual, species, and the biosphere. Single–species approaches should not be abandoned to focus on ecosystems, or vise versa. How are such multiple goals accomplished by systemic management? How can management deal with the fact that the forces and process of individuals, populations, species, ecosystems and the biosphere are often in opposition (e.g., WILSON & SOBER, 1989; WILLIAMS, 1992)? Highly trained and experienced specialists are often at odds with each other based on conflicting interpretations in conventional management, in part because of the many opposing forces of nature. How does adopting the principle of confining variation to within its normal limits lead to adhering to the tenets of management, one of which requires that such issues be dealt with consistently (e.g., across disciplines)?

Limits to management options There are limitations on the options for management, consistent with there being limitations on everything. This is seen in the application of the tenets of management. Such limits lead to the elimination of many management options. Applying these limits is a process that helps focus on what is possible and avoids the waste and problems created by trying things that will not work. Within the full, or unlimited, suite of options are those that involve controlling non–human species, ecosystems, or the biosphere, as often attempted in the past. Attempts have been made, and more might be undertaken, to directly control these systems without fully considering the effects, especially those that result in risks —particularly to humans, and particularly in the long run. However, it is increasingly clear that these options can no longer be considered (tenet 8, appendix 1 and 2, and as concluded in the literature referred to above) because, in each and every case, there are always uncontrollable side effects that are systemic in nature —some with negative consequences for ourselves (e.g., through the effects on the human environment that result in problems such as emergent diseases, RAPPORT & WHITFORD, 1999, or loss of resources).

There are unintended consequences (negative or positive, ROHMAN, 1999) to every management action. They may involve humans directly as participants in various systems, or indirectly through effects on other members of such systems (whether individuals, species, ecosystems). It is impossible to control the fact that such things happen. This leaves only options involving the control of human activities and the regulation of human influence (e.g., fish can not be regulated but commercial fishing can). By taking this approach, management involves finding appropriate levels of influence by humans (complete with all of their ramifications,

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positive or negative). Management can, for example, proceed by addressing appropriate levels of biomass consumption, whether from a species or an ecosystem, the numbers of species used as resources, or the extent of habitat to be protected (habitat for which direct influence is prohibited).

Considerable progress has been made in the step outlined in the previous paragraph —progress made by eliminating options, as tempting as they might be, that would be counterproductive, wasteful or impossible. This is an important juncture —that of recognizing what remains as viable management options. Among the remaining possibilities is that of finding sustainable levels of human influence. Human influences on each level of biological organization are things that can be addressed and things that are critically important to be addressed. However, the list of such things is enormous; this again brings managers to a confrontation with the complexity of nature, but all as part of considering complexity in achieving sustainability. Here it appears in regard to the wealth of ways in which humans (and all individuals and species) exert influence or interact with other elements of the human environment. This diversity is only superficially exemplified by measures of such things as how much humans eat, the quantity of fish harvested from a population, volume of CO2 added to the atmosphere, or the portion of the various habitats that humans occupy in any ecosystem.

Using empirically observed limits This section returns to the point of addressing how information on variation, and especially information on the limits to variation, is useful.

At this point, what might appear esoteric regarding the concept of limits becomes practical through empirically observed limits. How can management make the transition from traditional to systemic?

Every species has a wealth of influences on the other elements of related systems —all consistent with, and emergent from, the complexity of reality. The limits that they experience are those observed. Observed limits include both the characteristics of other species as well as their influences. Thus, what is seen are the things that work, the things that can be done to minimize the risk of failure as exemplified by death or extinction. Other species survive the full range of consequences of such influence, whether on other species, ecosystems or individuals. Managers thus have the full benefit of knowing that the influences of other species, along with all related processes and consequences, have normal ranges of natural variation —limits. There are empirical limits to the variation of such influences because the influence species have on each other and other systems also has limits. In this regard, existing species represent empirical examples of sustainability.

However, some alternatives within the normal

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range of natural variation are better than others.

These are the various alternatives between the upper and lower limits of natural variation that are emphasized in being represented by a predominance of examples —by their abundance, or frequency of occurrence. For individual organisms this is exemplified by the abundance of people with body temperatures close to 37ºC compared to the less frequent occurrence of individuals at either the high or low extremes bounding variation in body temperature. For species, it is the same. Better examples are found in the abundance of species representing a particular measure, especially the cluster of species near the central tendencies of natural variation. Species, as empirical examples of sustainability, represent the successes in nature’s multi–level, trial–and–error, game of survival (FOWLER & MACMAHON, 1982; LEVINTON, 1988).

Measures of other species reveal probability distributions as naturally occurring Nash equilibria (NASH, 1950) in which the central tendencies change over time and space according to environmental conditions. Nash equilibria are defined in terms of game theory, and, in this case, the games involve players (such as species) which are parts of systems (such as ecosystems) involved in their own games. Things have to work for both the systems and their parts at multiple levels.

Beyond the limits of variation among species, examples are rare because, by definition, risks and limits prevent the occurrence of such species.

For example, there are no 100 ton mammals that give birth to one offspring at the end of a 400 year lifetime, that consume only one carnivorous species from the 14th trophic level, and that are confined to arid deserts — they don’t exist (FOWLER & MACMAHON, 1982). Likewise, there is so much influence exerted by species that consume all of their resources that their existence is precluded.

By confining human species–level influence to within the normal range of natural variation, it is possible to simultaneously avoid risk and achieve sustainability. Decisions to seek the extremes, tacit or overt, are actions bound to lead to increased and unwanted risks. It is impossible to avoid the side effects of any action, but there is emphasis to be placed on the need to avoid the risks that prevent the accumulation of species beyond the normal range of natural variation. It is possible to achieve sustainability as exemplified by empirical examples that have faced the complexity of risks and constraints over various time scales —time scales that include the evolutionary and geological.

Accounting for complexity How does systemic management account for complexity (tenet 2, appendix 1)? There are three ways in which complexity gets taken into account if humans manage by finding and achieving a

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place within the normal range of natural variation (as amplified in the following paragraphs). Two of these are matters of human activity —where managers and scientists do the accounting/ considering. The third, and most crucial, is an automatic process central to the guiding information used in systemic management.

The three ways complexity is taken into account are: 1. Addressing variety in management issues/ questions, the identification of which is a management responsibility, 2. Making use of correlative relationships, a matter of importance in science for translating information into appropriate guidance, and 3. Using empirical patterns in limited variation as automatic integrations of complexity. All three can involve human interactions with ecosystems (to solve the problem of management at the ecosystem level).

However, it should be noted that it is not “ecosystem management” as transitive management wherein managers would manipulate ecosystems to achieve some desired state, but rather intransitive management wherein humans fit in sustainably. All three also involve human interactions with the biosphere (to include “biosphere management” —but, again, not as a transitive form of management). All involve species–level variation, and all involve interactions with the various levels of biological organization.

The following paragraphs examine how all three are treated in systemic management.

First, complexity is involved in the wide variety of management questions that have to be addressed. It is not just a matter of finding, achieving and maintaining individual sustainability such as appropriate body temperature or blood pressure; it includes sustainability in the species composition of fisheries catches, the amount of CO2 released to the biosphere, the consumption of biomass from ecosystems, the habitat preserved for other species, the age composition of harvested resources, the numbers of species that humans drive to extinction, the number of prey organisms consumed, and the places where humans live or exploit resources. The relevant questions involve the countless ways in which species interact with other species, their ecosystems, and the biosphere.

To account for complexity in this regard, managers are faced with the responsibility of addressing all such issues, at least all that they can think of (and it is impossible to think of them all). It is insufficient to simply find a sustainable rate for consuming biomass from a particular resource species. Managing fisheries systemically is not enough; carbon dioxide production must be included. Complexity is involved in the huge variety of issues to be addressed, issues that do not go away. They are also issues that can only be addressed by what humans do; nobody else, and certainly no other species, is going to do the work that only humans can do.

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Second, complexity is involved in recognizing that the limits to variability are interrelated (e.g., fig. 1) and function jointly. In nature, things are correlated. Thus, the appropriate limits must be chosen carefully (FOWLER, 1999a; FOWLER et al., 1999) to account for relationships among various measures of biological systems. The frequency and kinds of such relationships have yet to be appreciated but can not be ignored. For example, judging the status of a marine mammal population by using comparisons with bacterial populations is not an option (fig. 1), any more than is an attempt to find a sustainable level of net CO2 production for humans with information from species capable of photosynthesis. Managers would need to take the physical environment into account in correlative relationships such as these and the relationship between range size and latitude (STEVENS, 1992; GASTON & BLACKBURN, 2000). For example, climate change would be taken into account through correlative relationships in which climate is known to be related to patterns in limited variation relevant to any specific management question (e.g., rate of biomass consumption from a resource species).

Third, as described in earlier sections, complexity is automatically involved in the patterns of variation that provide empirically observed guidance for systemic management. Such patterns are of systemic origin. Complexity is behind the measurable limits and central tendencies involved in the variation inherent to such patterns. These patterns represent an integration of all of the factors important to their origin. Importantly, this integration involves an accounting of these factors in proportion to their relative importance.

This third point deserves further consideration even though it is something that happens automatically when empirical information is used in systemic management.

The empirical examples of sustainability embodied by other species are informative because these species have survived an evolutionary history of exposure to all the risks and factors that are to be taken into account. They have survived the multitude of risks that constrain variation, including the risks of extinction. These species, and the patterns of variation they exhibit, are products of complexity. In other words, what is seen in empirical information about natural variation and its limits is the result of the collective influence of all limiting factors, the aggregate of forces that come into play in producing the distributions. Forces or factors that are relatively unimportant are taken into account in proportion to their effects and the weight of their influence in the origin of observed patterns (including the variation of such patterns). If the rotation of the Earth influences biomass consumption (e.g., by determining the amount of daylight), then this factor is included in the empirical variation, with its limits, seen in observed rates of biomass consumption. Perhaps of equal importance, such

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factors are included in proportion to the strength of their influence; each factor is considered completely objectively relative to the influence of all other factors (i.e., without direct human involvement in the consideration —thus avoiding the risk of misleading human choices based on human values). The same holds true for other factors as well, whether they be the forces of evolution through natural selection, the nature of the carbon/oxygen chemical bond, extinction, the spectral composition of ambient light, the relative abundance of elements in the universe, or the structure and composition of cells.

Thus, this third point is that complexity gets taken into account automatically in systemic management. This happens by virtue of the fact that empirical examples of sustainability show natural variation that is both produced and limited in ways that integrate contributing factors amongst all aspects of complexity. They do so through their exposure to the collective set of factors that make up the context within which they occur and have occurred over geological time scales. This happens in a natural Bayesian–like integration process (FOWLER, 1999a, 1999b; FOWLER et al., 1999). This integration happens in reality, as opposed to through manmade models that cannot capture the full extent of reality (BATESON, 1972). Perhaps of greatest value is the fact that this integration happens in a way that gives proper emphasis or weight to each of the factors involved. This relieves managers of the need to decide whether embryological factors are more or less important than evolutionary factors, or long time scales are more important than short time scales. There is a synthesis of such information that scientists are incapable of achieving, thus overcoming reductionism as one of the limitations of science (A LLEN & S TARR , 1982; B ARTHOLOMEW , 1982; ROSENBERG, 1985; SALTHE, 1985; GROSS, 1989; PETERS, 1991; PICKETT et al., 1994; STANLEY, 1995) while taking advantage of the strength of this facet of science to find the empirical information about variation that is so critically important to management regarding each specific management question.

It is important here to emphasize the limitations inherent to science because in human culture it is often thought that science is capable of providing answers to all questions. First, it is important to remember that science is merely a methodology —a formula for inquiry that seeks truth, understanding and explanation of the universe in which humans find themselves.

Science, by definition, seeks knowledge. The pursuit of knowledge, however, explores components of systems and will, by definition, have limited success in knowing the system itself, especially the full system of reality. Part of this stems from the fact that the whole is always more than the sum of its parts. Part of the limitation stems from each system being part of more inclusive

Animal Biodiversity and Conservation 25.2 (2002)

systems. Bateson (e.g., BATESON, 1972, 1979) spoke of a knowledge and understanding of the greater system as wisdom. It is wisdom that is sought in management rather than merely more knowledge of system components and it is wisdom which science does not, and is not designed to, address. It is the deeper understanding or wisdom that is used in systemic management —where science is a tool for seeing useful information exemplified in the probability distributions that characterize patterns of limited variation.

Thus, it should be emphasized that the automatic aspect of the integration described above works two ways. Empirical information is informative as guidance and it accounts for the consequences of management action. The impacts of human actions are part of what is considered.

The complexity of these impacts is automatically taken into account because all components of complex systems (e.g., species) have the kinds of effects that humans have, and of the magnitude that humans will have if it is possible to manage to fit within the normal range of natural variation.

These impacts include those that generate risk through feedback in proportion to their relative importance. Thus empirical information accounts for complexity both in its informative role (based on the products of complexity) and in its accounting for the effects of human actions (nature in its complexity has experienced such effects over evolutionary time frames).

An overview of systemic management and the nine tenets Systemic management was introduced above as a form of management that adheres to basic tenets and principles of management that have been established in trying to deal with the inadequacies of conventional approaches. It is important to have a more detailed understanding of what systemic management is, in order for it to be implemented. It is important to understand how it should be carried out to meet the requirements embodied in the tenets of management found in appendix 1. How does it comply with basic principles? The following paragraphs consider the answer to this question in a way that simultaneously emphasizes the interrelated nature of the tenets and principles of management.

Natural systems are internally consistent and fully interconnected; no laws involving the conservation of mass and energy are broken in nature. Thus, empirical examples of sustainability embodied in species and their interactions with their environments are role–models of consistency.

In addition to this, humans, as participants in ecosystems and the biosphere, are required to apply information about natural variation in sustainability to all management questions (thus involving both tenets 1 and 2, appendix 1).

Therefore, consistency is accomplished in applying

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these principles of management by achieving a position for humans within the normal ranges of natural variation, not by choosing a few easy or simple cases, but by doing so broadly. This automatically involves consistency in application, but does so while simultaneously accounting for complexity. This, of course, would be a direct adherence to tenet 3 while also complying with tenet 8 (appendix 1) because managers would be choosing to act only on those issues where there is most control. This form of management would directly place humans into a sustainable role in the systems of which our species is a part (but not just as parts of ecosystems, tenet 9, appendix 1). It would do so by taking action to fall within the normal range of natural variation so as to avoid the risks and constraints reviewed above (tenet 4, appendix 1). Science would be crucial to the production of information on the limits to natural variation (CLARK, 1989, tenets 5 and 6).

There remains the need to meet the requirements of the tenet 7. How is it possible to establish goals, standards of reference, and guidelines? The answer to this question was introduced above in the discussion of central tendencies between upper and lower limits. Figures 2–6 (with relevant information and sources identified in appendix 3) show empirical data regarding variation and its limits (see also FOWLER & PEREZ, 1999; FOWLER et al., 1999; FOWLER, 1999a, 1999b; FOWLER, 2002), and the deviation of humans from the normal ranges of natural variation (with quantitative measures shown in table 2, appendix 3). The goals and objectives for systemic management are found near the central tendencies of frequency distributions (FOWLER & PEREZ, 1999) such as shown in these figures (recognizing that there are imperfections in current data and that systems change; e.g., FOWLER, 1999a; FOWLER et al., 1999). By virtue of their relative numerical abundance, the species in the region of the central tendencies emphasize the forms of sustainability they represent. These figures also emphasize the breadth of application of management that can be used to fit within the normal range of natural variation (FOWLER & PEREZ, 1999).

It should be clear that systemic management is, strictly speaking, neither restricted to being a conventional systems approach to management, nor merely a holistic approach. One distinction between traditional systems approaches and the systemic approach is particularly important.

Systems approaches usually focus on a single complex system like a population, ecosystem, family, community or individual that give it, and its components, a form of significance or relevance different from the significance it actually has in nature in relation to other systems, especially those of which it is a part. Thus, systems approaches that exist as precedents lack sufficient consideration of complexity, especially context, which is necessary for a fully developed systems approach to adequately account for hierarchical structure of reality (GRUMBINE, 1994a). Part of

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Fig. 2. Six frequency distributions showing a comparison between the rates at which humans consume biomass from individual resource species compared to the rates other species consume the same resource, all measured in units of log 10 metric tons per year: A. Eleven species of marine mammals as consumers of hake; B. Twelve species of bird, mammals and fish as consumers of herring; C. Sixteen species of birds, mammals and fish as consumers of mackerel; D. Six species of mammals as consumers of walleye pollock; E. Twelve species of birds as consumers of anchovy; F. Twenty species of birds, mammals and fish as consumers of walleye pollock. Further details are provided in appendix 3 (tables 1 and 2).

Fig. 2. Seis distribuciones de frecuencia en las que se comparan los índices de consumo de biomasa procedente de una especie utilizada como recurso por el hombre y los de otras especies que consumen el mismo recurso, todos medidos en log 10 toneladas métricas por año: A. Once especies de mamíferos marinos como consumidores de merluza; B. Doce especies de aves, mamíferos y peces como consumidores de arenques; C. Dieciséis especies de aves, mamíferos y peces como consumidores de caballa; D. Seis especies de mamíferos como consumidores de colín de Alaska; E. Doce especies de aves como consumidores de anchoas; F. Veinte especies de aves, mamíferos y peces como consumidores de colin de Alaska. Para más detalles ver apéndice 3 (tablas 1 y 2).

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Animal Biodiversity and Conservation 25.2 (2002)

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Fig. 3. Four frequency distributions showing a comparison between the rates at which humans consume biomass from various groups of resource species compared to that of other consumer species, all measured in units of log10 metric tons per year: A. Twenty species of marine mammals as consumers of finfish; B. Sixteen species of birds, mammals, and fish as consumers of hake, herring and mackerel (with humans in the same bar as dog fish); C. Thirteen species of birds and mammals as consumers of hake, herring and mackerel; D. Eighteen species of birds as consumers of anchovy, lanternfish, lightfish, and hake. Further details are provided in appendix 3 (tables 1 and 2).

Fig. 3. Cuatro distribuciones de frecuencia en las que se comparan los índices de consumo de biomasa de varios grupos de especies utilizadas como recurso por el hombre y por otras especies consumidoras, medidos en log10 toneladas métricas por año: A. Veinte especies de mamíferos marinos consumidores de peces óseos; B. Dieciséis especies de aves, mamíferos y peces, consumidores de merluza, arenques y caballa (con el hombre en la misma franja que la lija); C. Trece especies de aves y mamíferos, consumidores de merluza, arenques y caballa; D. Dieciocho especies de aves, consumidores de anchoas, pez linterna, luciérnaga perlada y merluza. Para más detalles ver apéndice 3 (tablas 1 y 2).

what has to be embraced in management are the more inclusive systems within which the focal systems occur (e.g., the biosphere that contains ecosystems). As such, existing attempts at systems approaches find it difficult to address questions regarding desirable emergent or aggregate qualities of a focal system, or even more difficult questions such as whether or not the system should exist at all. Insufficient importance is attached to the interactions of any particular system with other systems or the physical environment. For biological systems the other systems would include those at the same

level of biological organization, such as individuals interacting with individuals, species interacting with species, or ecosystems interacting with other ecosystems. Of possible greater relevance is the lack of attention given to the interactions between a system and the more inclusive systems of which they are a part. The interactions between a species and its ecosystem would be an example, as would the effects of an individual on its species, or a species on the biosphere. Perhaps of greatest importance is the fact that previous attempts at a systems approach have not accounted for the relative importance

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Fig. 4. Six frequency distributions showing a comparison between the rates at which humans consume biomass from various ecosystems compared to that of other species, all measured in units of log10 metric tons per year: A. Twenty–one species of mammals in Eastern Bering Sea (two species, including humans, in the bar representing the highest consumption rates); B. Forty–six species of fish, birds, and mammals from the Georges Bank; C. Thirty–three species of birds off the southwest coast of Africa (with humans sharing one bar with two species of birds); D. Twenty–three species of birds and mammals from the Georges Bank. E. Sixteen species of birds, mammals and fish from the Northwest Atlantic. F. Twelve species of marine mammals from the Georges Bank. Further details are provided in appendix 3 (tables 1 and 2).

Fig. 4. Seis distribuciones de frecuencia en las que se comparan los índices de consumo de biomasa procedente de varios ecosistemas por el hombre y por otras especies, todas las medidas en log10 toneladas métricas por año. A. Veintiuna especies de mamíferos del este del mar de Bering (dos especies, incluido el hombre, en la franja correspondiente a la mayor tasa de consumo); B. Cuarenta y seis especies de peces, aves y mamíferos del banco Georges; C. Treinta y tres especies de aves en el litoral de la costa suroeste de África (con el hombre compartiendo una franja con dos especies de aves); D. Veintitrés especies de aves y mamíferos del banco Georges; E. Dieciséis especies de aves, mamíferos y peces del noroeste Atlántico; F. Doce especies de mamíferos marinos del banco Georges. Para más detalles ver apéndice 3 (tablas 1 y 2).

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Animal Biodiversity and Conservation 25.2 (2002)

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Fig. 5. Six frequency distributions showing a comparison of humans with other species: four in regard to the rate of consumption of biomass (A–D), CO2 production (E), and energy ingestion (F), with biomass consumption and CO2 production measured in units of log10 metric tons per year, and energy consumption measured in log10 billion joules per year: A. Fifty–four species of marine mammals as consumers of biomass; B. Forty–two species of terrestrial mammals as consumers of biomass; C. Sixty– three species of mammals of body size similar to humans and as consumers of biomass; D. Ninety–six species of mammals as consumers of biomass; E. Sixty–three species of mammals of human body size as producers of CO2. F. Sixty–three species of marine mammals of human body size as consumers of energy. Further details are provided in appendix 3 (tables 1 and 2).

Fig. 5. Seis distribuciones de frecuencia en las que se compara el hombre con otras especies: cuatro referidas a la tasa de consumo de biomasa (A–D), producción de CO2 (E) e ingestión de energía (F), con el consumo de biomasa y la producción de CO2 medidos en log10 toneladas métricas por año, y el consumo de energía medido en log10 1.000 millones de julios por año: A. Cincuenta y cuatro especies de mamíferos marinos, consumidores de biomasa; B. Cuarenta y dos especies de mamíferos terrestres, consumidores de biomasa; C. Sesenta y tres especies de mamíferos de tamaño corporal similar al del hombre, consumidores de biomasa; D. Noventa y seis especies de mamíferos, consumidores de biomasa; E. Sesenta y tres especies de mamíferos de tamaño corporal equivalente al del hombre, productores de CO2; F. Sesenta y tres especies de mamíferos marinos de tamaño corporal equivalente al del hombre, consumidores de energía. Para más detalles ver apéndice 3 (tablas 1 y 2).

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Fig. 6. Six frequency distributions showing a comparison of humans with other species in regard to geographic range size (A, log10 1,000 k2), population size (B, D, F, log10 numbers), energy consumption per unit area (C, log 10 million joules per k2 per day), and percent of North America unoccupied (E, arcsine scale): A. Five hundred and twenty–three species of terrestrial mammals and their geographic range, in comparison to humans assumed to use either 20% or 70% of the non–Antarctic land surface area of the Earth; B. Twenty–one species of marine mammals of human body size and their total population size; C. Three hundred sixty–eight species of mammals in their consumption of energy per unit area in comparison to humans assumed to use either 20% or 70% of the non–Antarctic land surface area of the Earth; D. Forty–two species of terrestrial mammals of human body size and their total population size; E. Five hundred twenty–three species of terrestrial mammals with the portion of North America that they leave un–occupied. F. Sixty–three species of mammals of human body size and their total population size —a combination of B, and C. Further details are provided in appendix 3 (tables 1 and 2).

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of these categories of interactions. Conventional systems approaches can not assign importance in proportion to the importance realized in nature.

Systemic management builds on the components provided by analogous approaches exemplified by biomimicry (BENYUS, 1997) or benchmarking (SPENDOLINI, 1992; BOGAN & ENGLISH, 1994; BOXWELL, 1994; CAMP, 1995). In addition to asking how to feed ourselves there has to be a way to address the question of how many of humans there should be to feed. In addition to asking how to run a business enterprise, it is necessary to be able to address the matter of whether or not there should be such a business.

In the use of tools, it should be possible to ask whether their manufacture, use and disposal have effects that are within the normal range of natural variation. In order to use technology to solve problems, it must be possible to address the effects of such technology (e.g., manufacture, disposal, side effects). Management must apply at various levels of complexity and systemic management accomplishes this task.

Systemic management is an outgrowth of the systems approach and it accounts for the nature of systems, including the limits of human systems.

However, the systemic approach (as used here) is based, in part, on the fact that each system is part of a more inclusive system, such that an individual is part of a species, an ecosystem is part of a biosphere and a cell is part of an organism. In addition, systems (e.g., ecosystems, individuals, cells, species) interact with each other. Thus, systemic management is based on the recognition that the limits discussed in the earlier sections of this paper (i.e., the limits of nature or reality on its components) are limits that include those stemming from each system being parts of systems on larger scales. This means that a sustainable population is one that is sustainable by its supporting ecosystems and that the ecosystems providing the support to the population are in a state that can sustainably provide the support —balance (dynamic) within limits.

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There is another difference between systems approaches and systemic management. The latter is not merely holistic. It is not restricted to considering whole systems (i.e., an ecosystem, or a species) because it is also based on recognition of intrinsic limits, and that every system has components. The intrinsic limits are the limits imposed by virtue of systems being made up of components that themselves contribute to limits.

That is, systemic management recognizes there are both intrinsic and extrinsic factors that come to bear in all cases, and their influences are considered in proportion to their relative effects in nature. Thus, part of sustainability at the population level involves the effects of a population or species on the ecosystems of which it is a part in combination with the effects that individuals have from within the population.

Perhaps most importantly, systemic management requires that action and decisions be based on observed limits to natural variation. These include the ways that humans interact with other systems (e.g., consuming resource species, release of CO2 to the biosphere, or sharing habitat with other species). This is done, while avoiding being confined to focus on any one level or system, while clearly acknowledging the importance of the limits that systems place on their components (e.g., species and the limits that are placed on them by the ecosystems and all of the species of which they are comprised; KOESTLER, 1987; O’NEILL et al., 1986; SALTHE, 1985; WILBER, 1995). Finding what can effectively be controlled and acquiring information to guide control may be challenging, but gathering such information is a crucial scientific exercise in management (CLARK, 1989).

Scientists cannot control things to make management happen at the species level (and higher levels) but can, and must, be part of the process, especially by discovering, observing and measuring limits, then contributing the resulting information for use in guiding management (e.g., FOWLER & PEREZ, 1999). Many forms of conven-

Fig. 6. Seis distribuciones de frecuencia en las que se compara el hombre con otras especies en relación con el tamaño de área de distribución geográfica (A, log10 1.000 k2), tamaño de población (B, D, F, números en log10), consumo de energía por unidad de superficie (C, log10 millón de julios por k2 y día) y porcentaje de América del Norte no ocupado (E, escala en arcoseno): A. Quinientas veintitrés especies de mamíferos terrestres y su distribución geográfica comparadas con el hombre suponiendo el uso del 20% o el 70% de la superficie no Antártica de la Tierra; B. Veintiuna especies de mamíferos marinos de tamaño corporal equivalente al del hombre y el tamaño total de su población; C. Trescientas sesenta y ocho especies de mamíferos y su consumo de energía por unidad de superficie en comparación con el hombre suponiendo el uso del 20% o el 70% de la superficie terrestre no Antártica; D. Cuarenta y dos especies de mamíferos terrestres de tamaño corporal equivalente al del hombre y el tamaño total de su población; E. Quinientas veintitrés especies de mamíferos terrestres con la porción de América del Norte no ocupada por ellos; F. Sesenta y tres especies de mamíferos de tamaño corporal equivalente al humano y el tamaño total de su población —es una combinación de B y C. Para más detalles ver apéndice 3 (tablas 1 y 2).

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tional management can no longer be used owing to their failure to adhere to one or more of the principles of management and the resulting failures observed as the consequences of such management. The question before managers is: Is it possible to manage to achieve sustainability?

It is our species (and the individuals who are members of our species) that must do what is necessary to undertake the needed change. In navigation, knowing where one is and where one wants to be are both crucial pieces of information necessary to getting there. The path is then specified by other information. Likewise, the path for change is not specified in systemic management by information confined to establishing the endpoints or objectives. The details of actually undertaking change involve separate questions also to be addressed systemically as further steps in accounting for complexity.

It is now possible to see how the tenets of management laid out in appendix 1 actually define systemic management. These tenets owe some of their origins to efforts to move forward by amplifying upon and solving the problems of conventional practices. However, even though the tenets have been well developed in the literature, they have made little difference in what is actually done in management. Nevertheless, these tenets, provide a basis for doing things differently to achieve a realistic management process. Many of the roots of these tenets can be found in consideration of the inadequacies of past practices.

In this regard, systemic management holds promise in that it is different enough to be the change called for by those seeing a need for a completely new approach (ClARK, 1989; SANTOS, 1990; NORTON, 1991; GRUMBINE, 1992; KNIGHT & GEORGE, 1995; C OMMITTEE ON E COSYSTEM M ANAGEMENT FOR S USTAINABLE M ARINE F ISHERIES, 1999). Systemic management is management through human action to find a sustainable role in the systems of which the human species is a part. It is systemic in that it accounts for complexity, applies broadly, and involves all levels of biological organization.

However, to fully account for complexity it must be applied broadly in practice, not just in concept.

It is also systemic in that it requires dealing with the complexity of human systems by achieving change in human behavior, human influence, and human qualities through management. It should be noted that the complexity of this process involves social, economic, political, religious, scientific, and psychological issues —anything but a simple process and one that includes each and every person (CLARK, 1989). Thus, changes required of the human species do not free individuals from their part in the process. Individuals are also parts of natural systems and individual humans are components comprising our species. Individuals, regardless of species, contribute to what such systems (e.g., species) are and, as parts of such systems, are subject to the natural laws involved

in limits and constraints. The daunting nature of this task lends to the personal experience of the challenge of systemic management.

Systemic management has to be applied with regard to every system, emphasizing action where there is most control, especially in making decisions. There are “systems” components of systemic management in a variety of realms (CONN , 1995; O’CONNER, 1995; O’NEILL, 1999).

However, to be truly systemic, it is imperative to go beyond dealing with the internal workings of the respective systems to address questions regarding the interactions of such systems with others —their context. Systemic management emphasizes the responsibility shouldered by individuals, society, and the human species for the consequences experienced from failing to undertake such management all levels (PIANKA, 1974; CLARK, 1989; MOOTE et al., 1994; WILBER, 1995). To consider humans part of ecosystems or the biosphere (tenet 9, appendix 1) it is also necessary to consider humans subject to limits and risks (ROSENZWEIG, 1974).

Acknowledgments The authors wish to thank Robyn Angliss, Mary Clark, Jean Fowler, Carolyn Kurle, Alec MacCall, Shannon McCluskey, Susan Picquelle and at least one anonymous reviewer for very helpful reviews of earlier drafts of this paper. Shannon McCluskey, Laura Murray and Gyda May were very helpful in library work regarding examples of limitations, and references for both the “law of unintended consequences” and publications recognizing the importance of limits. Thanks are extended to them all for their efforts.

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Appendix 1. A list of tenets (criteria and principles) that must be met, or adhered to, in management. These tenets define systemic management (e.g., see FOWLER et al. 1999), however, they are extracted from a large body of literature dealing with management, especially in regard to management at the ecosystem level, most published in the last several decades of the 20th century (with references found throughout the text of this paper).

Apéndice 1. Relación de dogmas (criterios y principios) que deben conocerse u observarse en el manejo. Dichos dogmas definen el manejo sistémico (ver FOWLER et al., 1999), aunque se han extraído de una amplia literatura relacionada con el manejo, en especial con el manejo a nivel de ecosistemas, la mayoría publicada en las últimas décadas del siglo XX (las referencias aparecen a lo largo del texto de este trabajo).

1. Any application of management must be consistent with other applications and any form of management must apply simultaneously at the various levels of biological organization. For example, the harvest of biomass from individual resource species can not be in conflict with management of the harvest of biomass from the ecosystems in which the harvested species occur.

Similarly, biomass consumption by humans from the biosphere must be guided by principles that are not in conflict with those guiding the harvest of biomass from either an individual resource species or any particular ecosystem.

2. Management action must be based on an approach that accounts for reality in its complexity over the various scales of time, space, and biological organization. The context of environmental factors (e.g., ecological complexity) must be accounted for along with the elements of stochasticity and the diversity of processes, mechanics, and dynamics. The complexes of chemical and physical substances and processes as well as energetic dynamics must be taken into account, along with evolutionary processes at all levels. These factors must be given weight in decision-making that is in proportion to their relative importance and all must be dealt with simultaneously.

Furthermore, managers must be able to deal with uncertainty, including what cannot be known.

3. A core principle of management is that of undertaking actions that ensure that processes, relationships, individuals, species and ecosystems are within (or will return to) their respective normal ranges of natural variation as components of the more aggregated levels of biological organization. Included are evolutionary processes, and all those involved in ecosystem dynamics, as well as physiological and embryological processes. Any form of management must apply this principle (appendix 2, and the central theme of this paper).

4. Management must be risk averse and exercise precaution in achieving sustainability.

Sustainability is, by definition, not achieved by any form of management that generates risk rather than minimizing it.

5. Management must be information based. Guidance must be available to management in the form of useful information that enables managers to develop meaningful, measurable and reasonable goals and objectives (tenet 7). This information must be based on interdisciplinary approaches involving science (tenet 6) to adhere to the principle behind tenet number 2 above.

6. Management must include science (scientific methods and principles) in research, monitoring and assessment, not only to produce the information that is used for guidance (tenet 5), but also for evaluation of progress in achieving established goals and objectives (tenet 7).

7. There must be clearly defined goals and objectives that are measurable to provide quantitative evaluation of problems to be solved and gauge progress in solving them. There must be guidelines, criteria, and standards of reference.

8. It must be recognized that control over other species and ecosystems is impossible. The only option for control is the control of human action (CHRISTENSEN et al., 1996; MANGEL et al., 1996; HOLLING & MEFFE, 1996). For example, it is possible to control fishing effort but not the fish nor the fact that fishing will have its consequences, many of which will be both unintended and undesirable. It is not possible to control resource populations or ecosystems. It is possible to influence any resource population and its ecosystem, but not to control them to avoid indirect changes, side effects, or secondary reactions brought about by our influence. The guidance (tenet 7) needed for management is guidance regarding the level of influence (e.g., harvest rate) that meets the other criteria of this list.

9. Humans must be considered as parts of complex biological systems. Humans must have the option of being components of at least some ecosystems to avoid the unrealistic option of precluding human existence. Humans are not separate from, unaffected by, or free of the limits of the systems of which any species is a part.

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Appendix 2. Limits to Natural Variation (including biophysical limits): quotations from the literature.

Apéndice 2. Límites de la variación natural (incluye límites biofísicos): citas de la literatura.

AGEE & JOHNSON (1988a): “...limits and constraints.. [are not a] ...commonly understood concept of ecosystem management...”

AHL & ALLEN (1996): “By being unresponsive, higher levels constrain and thereby impose general limits on the behavior of small–scale entities.”

ALEXANDER & BORGIA (1978): “One implication is that while ecological communities may often be significantly affected by differential extinction of species, species are not necessarily likely to have been greatly influenced by differential extinction of populations or demes...”

ALLEN & STARR (1982): “It is sometimes advantageous, however, to view organization not positively as a series of connections, but rather negatively, as a series of constraints.

Ordered systems are so, not because of what the components do, but rather because of what they are not allowed to do.”

“Thus the large reductionistic ecosystem models may tell something of the how of ecosystems but lose much of the why. They focus on system dynamics rather than rate independent system constraints...”

ANDERSON (1991): “Intact suggests that all of the critical ecosystem components are present and structured in such a way that processes function within normal limits...over the long term.”

ANGERMEIER & KARR (1994): “[Integrity is] the capability of supporting and maintaining a balanced, integrated, adaptive community of organisims having a species composition, diversity, and functional organization comparable to that of natural habitat of the region.”

APOLLONIO (1994): “[Fisheries] ...must have characteristics comparable to apex predators if the systems are to be manageable, that is, the vessels must emulate the essential characteristics of K–selected species.”

ARNOLD & FRISTRUP (1982): “Selection at a given level can be opposed, reinforced, or unaffected by processes operating at other levels.”

BATESON (1972): "...the steady state and continued existence of complex interactive systems depend upon preventing the maximization of any variable, and that any continued increase in any variable will inevitably result in, and be limited by, irreversible changes in the system.” “In principle, the homeostatic controls of biological systems must be activated by variables which are not in themselves harmful.”

BROWN (1995): “...morphology, physiology, and behavior of individual organisms play major roles in causing, or at least constraining, large-scale patterns of distribution and abundance, both within and among species.” [others have] “...recently developed a statistical method to fit lines to the boundaries of ... two–dimensional scatter plots of data to represent estimates of constraints.”

BROWN & MAURER (1987): “Since species of large body size are constrained to have low population densities, such species with small geographical ranges should have high probability of extinction because the total species population is small.” “A more interesting example of an apparently absolute constraint is an energetic trade–off between maximum population density and body size.”

BURNS et al. (1991): “Existing theories of evolution as a general process of ordered change have come not from biology, but from physics and general systems theory... In addition, a great deal of corroborating evidence is accumulating in the study of chemical reaction systems..., life’s origin..., epigenetic systems..., cell evolution... and the biosphere... that there is a common and fundamental description of self–organizing change in far– from–equilibrium systems. What these theories share is a recognition that entities are systems evolving within still larger interactive systems, entities with environments both modified by and constraining their evolution.”

BUSS (1988): “Traits expressed in the higher unit now act as selective agents on the variation arising in the lower unit. The organization of the higher unit is, however, a function of prior variation in the lower unit. Thus, the lower unit can influence the replication of the higher unit by modification of its organization to suit the lower unit, but only to the extent that replication of the lower unit does not disadvantage the higher unit in its interaction with

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the external environment.” “The external environment will act solely on the higher unit only if the lower unit is physically contained within the higher unit, as in the case of genes within cells or cells within multi–cellular organisms. When the lower unit is not physically enclosed within the higher unit, e.g., organisms within species, the external environment may actively select both units.” “A second factor, however, is equally important. Variance will also arise which disrupt the higher unit, that is, they will favor the lower unit at the expense of the higher unit. The rate and magnitude of such conflicts must be limited, or the higher unit will perish. If variants arise in the lower unit whose affect is to limit the occurrence or magnitude of subsequent variation, then the higher unit will eventually become resistant to further perturbation.”

CHRISTENSEN et al. (1996): “Extreme fluctuation is abnormal in most ecosystems and, when caused by human activity, is what often threatens ecosystem functioning.”

CLARK (1989): “Science, by illuminating for us at least some of the complexities of Nature, can provide us with an ultimate boundary for our actions. If we perceive how Nature works we can tell when we are threatening its ability to function in a healthy fashion.” “Science can only tell us, if we decide we want to survive, what the boundary conditions are, what the ‘rules of the survival game are’, so to speak.” “Science is for discovering the limits of the natural world and the laws by which it proceeds and within which we are free to act. This aspect of science can add greatly to the maps and signposts we need to guide us into the future.”

DARWIN (1953): “...we certainly can do something to control the world around us, and if we can appreciate the limits of what is possible, we may have some hope...”

EHRENFELD (1993): “So it is with communities in the organismic view. They have recognizable identity, and in the final stage of community embryology, or succession, that identity becomes fixed and normative: a prairie, a beech–sugar maple forest, a desert. Because communities have fixed identifies, because they are normative likes organisms, we can easily apply the normative idea of health to them: if they are functionally and structurally similar to their abstract ideal, they are healthy; if they deviate significantly, they are sick.”

FARNWORTH & GOLLEY (1974): “Both plant and animal pests challenged the progenitors of domesticated species long before the invention of agriculture, but counter selection pressures constrained their populations within the long term carrying capacity of their environments and regulated the virulence of pathogens at moderate levels that would preserve the hosts.”

FISHER (1986): “Thus, on average, the most conspicuous, sustained trends will be in the direction of least morphological constraints.”

FRANCIS et al. (1999): [Ecosystem Management should:] “Strive to retain critical types and ranges of natural variation in ecosystem. That is, management should facilitate existing processes and variabilities rather than changing and controlling them.”

FUENTES (1993): “...we should concentrate on defining the borders of a sustainability space...”

GOODLAND (1995): “Humanity must learn to live within the limitations of the biophysical environment.”

GLAZIER (1987): “The present hypothesis represents a modified version of a model used to explain correlations between species diversity and productivity among ecological communities...

According to this modified model, an increase in energy availability and/or a decrease in energy demand permits more congeneric species to subdivide the energy supply of a given generic niche such that each species still obtains a sufficient portion to maintain a population size having a low probability of extinction. This model assumes that evolution tends to produce increasingly specialized species (i.e., those having a narrower range of resources), because they are more efficient at using resources than generalized species.”

GRIME (1989): “These appear to reflect fundamental constraints of habitat and organism which channel evolution into predictable paths. A current challenge is to assess the extent to which recognition of these patterns provides the essential clues to community and ecosystem structure.”

GRUBB (1989): “It seems that increasingly practitioners write explicitly that optimization is constrained by the available genetic material. However, I seriously doubt whether that point is sufficiently emphasized to beginning students.”

GRUMBINE (1994b): “...our purpose in protecting wildness is not to preserve nature or to improve it, but rather to learn a sense of limits from it and to model culture after it.”

HAGEN (1992): “[Odum] stressed the homeostatic nature of ecosystems such that they should be expected to have properties... [and] the much stronger claim that all living systems —cells, organisms, populations and ecosystems— share this common self–regulatory property.”

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HANNON (1992): “We will be required to reduce our GNP per capita and probably our population to comply with this solar constraint. Such a change is unprecedented in recorded world history, except perhaps for Ireland.”

HOLLING (1966): “Those organisms, those communities that lacked the mechanisms necessary to permit adaption to major changes cannot survive the many short– and long–term dislocations of the environment that occurred long before man appeared. These mechanisms are homeostatic or feedback processes that tend to resist change and promoted stability.

Any departure from a norm tends to be opposed, and opposed with increasing vigor as the departure becomes greater and greater. One example is found in the not necessarily controversial idea of density dependence, so familiar to students of population dynamics.”

HOLLING & MEFFE (1996): “Natural resource management should strive to retain critical types and ranges of natural variation in ecosystems.” “...when the range of natural variation in a system is reduced, the system loses resilience.” “That is, management should facilitate existing processes and variabilities rather than changing or controlling them.” “...effective natural resource management that promotes long–term system viability must be be based on an understanding of the key processes that structure and drive ecosystems, and on acceptance of both the natural ranges of ecosystem variation and the constraints of that variation for long-term success and sustainability.”

HYAMS (1976): “It is possible to rearrange the parts within the whole without permanently impairing the balance; but only within certain limits.”

INGRAM & MOLNAR (1990): “Overall, nature is not very diverse.” “When one looks at the living world, what impresses is the lack of diversity. While there may be a multitude of entities, what is noticeable is their sameness.”

JOHNSTON (1991): “...fallacy of equating freedom with "soft" containers.”

KING (1993): “Maintenance of an ecosystem integrity implies maintenance of some normal state or norm of operation (e.g., homeostasis or homeorhesis). Measuring or observing ecosystem integrity, or its loss, thus requires observations over sufficient temporal extent to identify and characterize this normalcy. We are prisoners of perspective, and our concept of normal is empirically bound to the scales with which we observe a system. ...concepts of normalcy, constancy, variability, and thus, ecosystem integrity, are only meaningful within bounds set by the scale of observation.”

KOESTLER (1987): “...while the canon imposes constraints and controls on the holons activities, it does not exhaust its degrees of freedom... guided by the contingencies of the environment.”

LEVIN (1989): “What are the natural patterns and dynamics of ecosystems, how are they regulated, and how robust are they to perturbation?”“We must develop a theory for the response pattern of different ecosystems to stresses. We must develop standards of comparisons among ecosystems, based on the identification of common, functionally important processes and properties. Such understanding can emerge only from theoretical syntheses based on a comprehensive program of microcosm research and experimental manipulation coupled with the retrospective studies.”

LEVINTON (1979): “Therefore, the equilibrium species richness is less in unpredictable environments.” “...length of food chains may also be limited by population dynamical forces...”

MANGEL et al. (1996): “The goal of conservation should be to secure present and future options by maintaining biological diversity at genetic, species, population and ecosystem levels; as a general rule neither the resource nor other components of the ecosystem should be perturbed beyond natural boundaries of variation” “The best possible relationship between humans and nature safeguards the viability of all biota and the ecosystems of which they are a part and on which they depend, while allowing human benefit (for present and future generations) through various uses. Conservation thus includes the consumptive and non–consumptive use of resources (management) and the preservation of critical resources so that future options can be kept open and so that normal ecological structure and function may continue. The challenge is to determine the appropriate balance between the health of resources and ecosystems and the health and quality of human life.” “...economic interests are given priority over biological reality and constraints. ...The disparity between economic and ecological time scales presents a great challenge because the economic system responds to change much faster than the ecological system; that is, biological systems are constrained by much slower time scales than economic systems.”

“Treating wild living resources as has been done in the past is untenable for the long term. The fundamental relationship between people and the rest of nature needs to be rethought, and policies developed that fully recognize the realities of the biophysical constraints under which humans must function.”

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MCCORMICK (1999): “When limits of acceptable change are exceeded, the corrective action most often required is regulation and restoration of human intervention.”

MCNEILL (1993): “We will never escape the ecosystem and the limits of the ecosystem. Whether we like it or not, we are caught in the food chain, eating and being eaten. It is one of the conditions of life.”

MOOTE et al. (1994): “Ecosystem management focuses on the maintenance of an ecosystem’s natural flows, structures, and cycles, displacing the traditional emphasis on the protection of such individual elements as popular species or natural features” “Ultimately, we shoulder the responsibility to live within the limits of our environment or to decide not to...”

NATIONAL MARINE FISHERIES SERVICE ECOSYSTEMS PRINCIPLES ADVISORY PANEL (1998): “Ecosystems have real thresholds and limits which must not be exceeded.”

O’NEILL et al. (1986): “Each level in the hierarchy can be over ridden by the next higher level, and is thereby under the constraint or control of the next higher level. The higher–level control in a sense is pursuing a more general strategy to which the more local strategy of the lower-level controls are subordinated.” “The higher level appears as an immovable barrier to the behavior of the lower level. This constraint is a natural consequence of the asymmetry in rate constants.” “In the natural world, population growth rate cannot approach its maximum because of limited food, space, predators, and so forth.”

ORIANS (1990): “Ecological theory is currently insufficient to predict when such limits may be reached.” “Simple solutions are not possible and should not be sought. However, determining system specific limits is nonetheless vital.”

OVINGTON (1975): “...it is possible that the impact of man can be accommodated within the foreseeable future until the disturbing influence of man can be brought into a more stable and intimate balance with the global environment realities.”

PIANKA (1974): “[Balances] are obvious and incontestable, yet modern man has largely failed to appreciate their relevance to his own existence.”

PICKETT et al. (1992): “If nature is a shifting mosaic or in essentially continuous flux, then some people may be wrong to conclude that whatever societies choose to do in or to the natural world is fine. The question can be stated as, ‘If the state of nature is flux, then is any human–generated change okay?’ The answer to this question is a resounding ‘No!’ ... Human–generated changes must be constrained because nature has functional, historical, and evolutionary limits. Nature has a range of ways to be, but there is a limit to those ways, and therefore, human changes must be within those limits.”

PIMENTEL (1966): “To date no one has described all the factors which limit the numbers in any population of a natural community. One factor is clear: no population can increase indefinitely and convert all the food of its environment into itself and its seed. The number of all populations is limited. The mechanisms which regulate and limit populations are numerous and varied, but basically all are density–dependent. The various limiting mechanisms can be classified into four general categories and are listed according to their relative speed of action: (1) interspecific competition, (2) natural enemies (parasites and predators), (3) environmental heterogeneity, (4) genetic feedback mechanisms.”

“The action of the genetic feedback mechanism leads to regulation of numbers of parasites, predators, herbivores and competitors into the gradual evolution of species toward ecological homeostasis with the community associates...”

PIMM (1982): “...Constraints on population dynamics, energy flow, and the structural designs of animals explain... [observed patterns].”

PIMM (1984): “The causes of the short food chains, so frequently observed in the real world, are far from certain. There are four hypotheses: energetic constraints, size or design restrictions, a balance between evolutionary tendencies to lengthen and shorten chains, and dynamical constraints.”

PIPER (1993): “A major theme running through the book is the conceptual problem between such ecosystem–level phenomena as the apparent balance and homeostasis of nature and such population–level phenomena as competition, randomness, and chaos.”

PONTING (1991): “Other religious traditions in the world did not place humans in such a special and dominant position. Chinese Taoist thought emphasized the idea of a balance of forces within both the individual and society. Both ought to try to live in a balanced and harmonious way with the natural world.” “Human history is, at one level, the story of how these limitations have been circumvented and of the consequences for the environment of doing so. Overwhelming the most important departure from basic ecological constraints has been the increase in human numbers far beyond the level that could be supported by natural ecosystems. ...this depended on a number of special attributes stemming from their greatly increased brain size–speech, social cooperation and the development of various technologies...”

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RAPPORT et al. (1981): “Distress would be reflected in abnormal values for vital signs and/or preclinical indicators.” “Diagnosis involves pattern recognition, or correlating the abnormal values of signs with ecosystems breakdown syndromes.”

REICHLE et al. (1975): “Ecosystems... all appear to exhibit common properties of persistence and growth.” “...all ecosystems have also developed mechanisms for energy storage as an operational basis for maintaining homoeostasis.”

ROSENZWEIG (1995): “Perhaps some combination of the thermodynamic hypothesis, the area hypothesis, and the dynamics hypothesis limits the number of trophic levels in all systems.”

ROUGHGARDEN (1989): “The first generation of models traces to Hutchinson’s ...conceptualization of the ideas of limited membership.”

SALTHE (1985): “Everything controls its parts and, as a part is controlled by the whole it is a part of.” “In it the dynamics of upper and lower levels produce output that can influence the dynamics of the focal level. Lower level constraints, dubbed initiating conditions, will be seen to give rise autonomously to focal level dynamics which exemplify some law(s) of nature, while higher–level constraints, which I propose should be referred to as boundary conditions, regulate the results of focal level dynamics.”

SALZMAN (1994): [We need to] “ ...agree to abide by the same ecological and evolutionary rules of behavior governing nonhuman species and ecosystems.”

STANLEY et al. (1983): “Species selection may be driven by internal factors, such as traits that endow a particular kind of species with a propensity to speciate, or it may be driven by external agents. The external agents of species selection are ecological limiting factors, the biotic varieties of which are predation (including parasitism), competition, and provision of food or substratum.”

SWIMME & BERRY (1994): “It was a moment when the human was able to establish its species identity with new clarity, an achievement that had it admirable but also its dangerous aspects since this clarity of species identity tended toward isolating the human within itself over against the nonhuman components of the larger Earth community. Once again we can observe that every perfection imposes limitations.”

TILMAN (1989): “As has long been recognized, the most general constraint comes from the universal requirement of all living organisms for energy and matter. ...Each individual organism exists within a web of consumer-resource relations. Its reproductive rate is constrained by the availabilities of the items it consumes–it resources. Its survivorship is constrained by the organisms that attempt to consume it. The universality of consumer–resource interactions has motivated both theory and experiments..., but has not yet become as central a concept in ecology as its universality demands. ...Conversely, if population ecologists had started in 1916, to seek the causes of the broad, general patterns Clements described, that subdiscipline could have advanced much more quickly. There is much about the evolution of the organismal traits that can be best understood in terms of ecosystem-level constraints, just as there are many ecosystem-level patterns that are best explained in terms of constraints on the evolution of individual organisms. ...In this paper, I have suggested that we should study broad, general patterns. In studying such patterns, we should pursue ecological abstraction by using the simplest possible approach that explicitly includes the most universal constraints of the environment and the unavoidable trade–offs that organisms face in dealing with these constraints. The most universal constraints may come from consumer–resource interactions because all species are, of necessity, parts of food webs.”

UHL et al. (2000): “Live within limits.” “Recognize that our natural resources are finite endowments to be used with care and prudence at a rate consonant with their capacity for regeneration.” “There are limits to growth and consumption...”

WOOD (1994): “Respecting limits to land use and acknowledging that we often lack the ability to predict the land’s response to management activities are critical points of departure for the ecosystem management concept.” “...ecosystem management entails setting limits on the use of the land.”

WOODWELL (1990): “The cause of the disruption is a single species, Homo sapiens, which has escaped the normal limitations that keep the numbers of individuals of each species in check and has swarmed over the earth as no species has ever done previously.”

YODZIS (1984): “If there is any property of whole ecosystems that almost every ecologist would regard as universal, it is the limitation of food chains to two or three links for the most part, with food chains having more than five links being rare.” “The data are consistent with the hypothesis that food chain lengths are limited by the available energy.”

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Animal Biodiversity and Conservation 25.2 (2002)

Appendix 3. Empirical data on observed limits to natural variation and the degree to which humans exceed such limits.

Apéndice 3. Datos empíricos sobre límites observados en la variación natural y el grado en que los humanos exceden estos límites.

Table 1. A list of descriptions for the data shown graphically in figures 2–6 with sample sizes for the nonhuman species (units for the measure are indicated in corresponding graphs): F. Figure; N. Number of species; C. Category of species (B. Birds; F. Fish; M. Mammals; MHbs. Mammals of human body size; MM. Marine mammals; MMHbs. Marine mammals of human body size; TM. Terrestrial mammals; TMHbs. Terrestrial mammals of human body size); S. Source (1. FOWLER et al., 1999, 2. OVERHOLTZ et al., 1991; 3. LIVINGSTON, 1993; 4. FOWLER & PEREZ, 1999; 5. CRAWFORD et al., 1991; 6. BACKUS & BOURNE, 1986).

Tabla 1. Lista de descripciones para los datos que se muestran en las figuras 2–6, con indicación del tamaño de las muestras para las especies no humanas (las unidades de medida se indican en los gráficos correspondientes): F. Figura; N. Número de especies; C. Categoria de especies (B. Aves; F. Peces; M. Mamíferos; MHbs. Mamíferos de tamaño corporal similar al humano; MM. Mamíferos marinos; MMHbs. mamíferos marinos de tamaño corporal similar al humano; TM. Mamíferos terrestres; TMHbs. mamíferos terrestres de tamaño corporal similar al humano); S. Fuente (1. FOWLER et al., 1999, 2. OVERHOLTZ et al., 1991; 3. LIVINGSTON, 1993; 4. FOWLER & PEREZ, 1999; 5. CRAWFORD et al., 1991; 6. BACKUS & BOURNE, 1986).

F 2A

N 11

C B, M & F

2B

12

B, M & F

2C

16

B, M & F

2D

6

2E

12

B

2F

20

B, M & F

3A

20

MM

3B

16

B, M & F

3C

13

B&M

3D

18

B

4A 4B 4C

21 46 33

MM F, B & M B

Topic Measure Biomass consumption of hake (Merluccius bilinearis) Biomass consumption of of herring (Clupea harengus) Biomass consumption of mackerel (Scomber scombrus) Biomass consumption of walleye pollock (Theragra chalcogramma) Biomass consumption of anchovy (Engraulis capensis) Biomass consumption of walleye pollock Biomass consumption of finfish Biomass consumption of hake, herring, and mackerel Biomass consumption from hake, herring, and mackerel Biomass consumption of anchovy, lanternfish, lightfish, and hake (E. capensis, Lampanyctodes hectoris, Maurolicus mulleri, and Merluccius spp.)

Total biomass consumption Total biomass consumption Total biomass consumption

4D 4E

23 16

B&M B, M & F

Total biomass consumption Total biomass consumption

4F 5A

12 54

MM MM

Total biomass consumption Total biomass consumption

MM

Region / Location S Marine ecosystem off 1,2 NE coast of North America Marine ecosystem off 1,2 NE coast of North America Marine ecosystem off 1,2 NE coast of North America Bering Sea and 1,3,4 North Pacific ecosystem Marine ecosystems off SW coast of Africa Eastern Bering Sea and North Pacific Eastern Bering Sea Marine ecosystem off NE coast of North America Marine ecosystem off NE coast of North America Marine ecosystems off SW coast of Africa

Eastern Bering Sea George Bank ecosystem Marine ecosystems off SW coast of Africa Georges Bank ecosystem Marine ecosystem off NE coast of North America Georges Bank ecosystem Marine environment

4,5 1,3,4 4 2,4 2,4 4,5

4 6 5 6 2 6 4

Fowler & Hobbs

44

Tabla 1. (Cont.)

F 5B 5C 5D 5E 5F 6Aa

N 42 63 96 63 63 523

C TM MHbs M MHbs MHbs TM

6Ab

523

M

6B 6Ca

21 368

MMHbs M

6Cb

368

M

6D 6E 6F

42 523 63

TMHbs TM MHbs

Topic Measure Total biomass consumption Total biomass consumption Total biomass consumption CO2 production Energy ingestion Geographic range (humans at 20% of Earth’s non–Antarctic land surface) Geographic range (humans at 70% of Earth’s non–Antarctic land surface) Total Population size Consumption of energy per unit area (human value based on consumption spread over 20% of the Earth’s terrestrial surface) Consumption of energy per unit area (human value based on consumption spread over 70% of the terrestrial Earth’s surface) Total population size Portion of North America unoccupied Total population size

Region / Location Entire Earth Entire Earth Entire Earth Entire Earth Entire Earth Entire Earth

S 4 4 4 4 4 4

Entire Earth

4

Entire Earth Entire Earth

4 4

Entire Earth

4

Terrestrial environment North America Entire Earth

4 4 4

45

Animal Biodiversity and Conservation 25.2 (2002)

Table 2. Results of statistical tests of the hypothesis that humans are within the normal range of natural variation among other species for a variety of measures (listed for the corresponding graph numbers in table 1, with units shown in the corresponding graphs) and measures of humans expressed as multiples of measures of non–human species (expresed as the antilog of differences between columns): F. Figure; Mean. Geometric mean among non–human species; V. Value for humans; P. Probability of human value, or more extreme; * The measure of humans expressed as a multiple of non–human species is based on the raw values corresponding to the arcsin measures rather than log values.

Tabla 2. Resultados de las pruebas estadísticas referentes a la hipótesis de que los humanos se encuentran dentro del espectro normal de variación natural entre otras especies para una variedad de medidas (consignadas para los gráficos correspondientes en la tabla 1 y con las unidades indicadas asimismo en los gráficos correspondientes) y medidas de humanos expresadas como múltiplos de las medidas de especies no humanas (expresadas como el antilogaritmo de las diferencias entre columnas): F. Figura; Mean. Media geométrica entre especies no humanas; V. Valor para los humanos; P. Probabilidad del valor humano, o más extremo; * La medida de los humanos expresada como múltiplo de especies no humanas está basada en mayor medida en los valores brutos correspondientes al arcoseno de las medidas que en los valores logarítmicos

Confidence limit V

Human value as multiple of

F

Mean

P

0.95

0.99

2A

3.068

4.255

0.043

4.209

4.681

Mean 15.4

0.95 limit 0.99 limit 1.1

0.4

2B

3.122

4.929

0.000

3.986

4.344

64.2

8.8

3.8

2C

3.127

4.792

0.055

4.840

5.549

46.2

0.9

0.2

2D

4.360

6.072

0.001

5.278

5.659

51.5

6.2

2.6

2E

2.829

5.681

0.000

4.202

4.770

712.3

30.2

8.1

2F

3.866

6.072

0.028

5.760

6.546

160.7

2.0

0.3

3A

4.170

6.301

0.024

5.949

6.686

135.2

2.2

0.4

3B

3.870

5.218

0.038

5.118

5.635

22.3

1.3

0.4

3C

3.344

5.218

0.006

4.567

5.074

74.8

4.5

1.4

3D

3.209

5.681

0.002

4.575

5.141

296.4

12.8

3.5

4A

1.865

3.301

0.035

3.170

3.711

27.3

1.4

0.4

4B

0.613

2.049

0.137

2.770

3.664

27.3

0.2

0.02

4C

2.294

5.681

0.000

3.964

4.655

2,436.8

52.2

10.6

4D

0.389

2.049

0.005

1.460

1.903

45.7

3.9

1.4

4E

3.870

5.218

0.038

5.118

5.635

22.3

1.3

0.4

4F

0.294

2.049

0.000

1.149

1.502

56.9

8.0

3.5

5A

5.572

9.478

0.001

7.556

8.378

8,066.1

83.6

12.6

5B

5.158

9.478

0.001

7.396

8.323

20,900.6

120.9

14.3

5C

5.222

9.727

0.001

7.538

8.497

31,979.3

154.6

17.0

5D

5.391

9.478

0.001

7.506

8.382

12,234.0

93.9

12.5

5E

4.650

10.301

0.000

6.969

7.930

447,951.9

2,148.8

235.2

5F

6.067

10.572

0.001

8.383

9.342

31,979.3

154.6

17.0

6Aa

2.355

4.318

0.035

4.135

4.873

91.9

1.5

0.3

6Ab

2.355

5.030

0.007

4.135

4.873

473.0

7.8

1.4

6B

5.235

9.761

0.002

7.789

8.848

33,627.9

93.7

8.2 19.0

6Ca

1.912

4.719

0.000

2.992

3.440

640.5

53.3

6Cb

1.912

4.020

0.001

2.992

3.440

128.1

10.7

3.8

6D

5.265

9.761

0.000

7.250

8.072

1,370.3

324.9

48.9

6E*

1.295

0.030

0.000

0.801

0.597

0.0010

0.0017

0.0029

6F

5.196

9.761

0.001

7.483

8.430

36,762.0

190.0

21.4

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 25.2 (2002)

47

Is growing tourist activity affecting the distribution or number of breeding pairs in a small colony of the Eleonora’s Falcon?

A. Martínez–Abrain1,2,*, D. Oro2, V. Ferrís3 & R. Belenguer3

Martínez–Abrain, A., Oro, D., Ferrís, V. & Belenguer, R., 2002. Is growing tourist activity affecting the distribution or number of breeding pairs in a small colony of the Eleonora’s Falcon. Animal Biodiversity and Conservation, 25.2: 47–51.

Abstract Is growing tourist activity affecting the distribution or number of breeding pairs in a small colony of the Eleonora’s Falcon?— Human disturbance is a common threat for species of conservation concern such as the Eleonora’s Falcon. This paper shows that the rise in tourist presence from 1992 to 2000 has not affected the overall number of breeding pairs or their productivity in a small archipelago of the western Mediterranean (Columbretes Islands). However, the increasing tourist activity has coincided with a shift in the degree of occupancy on two islands within the archipelago, favouring that with a lower human presence close to colonies. Several conservation actions are reported and suggested, aimed at both testing and preventing the role of human presence as a factor influencing long–term colony persistence and growth.

Key words: Eleonora’s Falcon, Human disturbance, Navigation tourism, Columbretes, Conservation, western Mediterranean.

Resumen ¿Está afectando la actividad turística creciente a la distribución o al número de parejas reproductoras de una pequeña colonia de halcón de Eleonora?— Las perturbaciones de origen antrópico son un factor de amenaza común para especies vulnerables como el halcón de Eleonora. El presente artículo muestra que el incremento de la presencia humana en un archipiélago del Mediterráneo occidental (islas Columbretes), durante el periodo 1992–2000, no ha afectado ni al número de parejas nidificantes ni a su productividad. Sin embargo, dicho incremento de la actividad turística ha coincidido con un cambio en el nivel de ocupación de dos islas del archipiélago, favoreciendo a la isla menos frecuentada por embarcaciones turísticas. Se sugieren algunas medidas de gestión que pueden servir para comprobar si las visitas turísticas pueden influir en el mantenimiento y crecimiento de la colonia a largo plazo, así como para prevenir estos posibles efectos.

Palabras clave: Halcón de Eleonora, Perturbaciones de origen antrópico, Embarcaciones turísticas, Columbretes, Conservación, Mediterráneo occidental.

(Received: 11 II 02; Conditional acceptance: 7 V 02; Final acceptance: 6 VI 02) 1

Alejandro Martínez–Abrain,CPEMN Conselleria de Medi Ambient, Avda. de los Pinares 106, 46012–El Saler, Valencia, Spain.

A. Martínez–Abrain & D. Oro, Instituto Mediterráneo de Estudios Avanzados IMEDEA (CSIC–UIB), Miquel Marqués 21, 07190–Esporles, Mallorca, Spain.

3 V. Ferrís & R. Belenguer, Reserva Natural de las Islas Columbretes, Conselleria de Medio Ambiente, Avda.

Hermanos Bou 47, 12003 Castellón, Spain.

2

* Corresponding author: A. Martínez–Abrain, CPEMN Conselleria de Medi Ambient, Avda. de los Pinares 106, 46012–El Saler, Valencia, Spain.

E–mail: a.abrain@uib.es ISSN: 1578–665X

© 2002 Museu de Ciències Naturals

Martínez–Abrain et al.

48

Introduction

Material and methods

The Eleonora’s Falcon (Falco eleonorae) is a highly migratory species which breeds on Mediterranean islands and winters in the Indian Ocean (WALTER, 1979). It is presently considered to have an unfavourable conservation status in Europe (TUCKER & HEATH, 1994). This species has evolved a late breeding calendar as an adaptation to feeding chicks, taking advantage of the pulse of migrant birds moving southwards late in the summer over the Mediterranean basin (WALTER, 1979). Human disturbance is presently considered one of the major threats to birds and other vertebrates (TUCKER & HEATH, 1994; HILL et al., 1997; RISTOW, 1999). Hence, Eleonora’s Falcons are prone to suffer from human presence since tourist visits to colonies commonly peak during the breeding period.

This paper presents the effects of the increasing number of tourist boats on Eleonora’s Falcons breeding on a small archipelago of the western Mediterranean, following a long period of monitoring their breeding performance.

The study took place on the Columbretes Islands (39º51’N 0º40’E), a 19 ha volcanic outcrop (comprising four major islet groups: Carallot, Ferrera, Foradada–Lobo and Grossa) located close to the edge of the wide continental shelf of Castellón, E Spain (fig. 1).

The Columbretes archipelago has been a nature reserve since 1988 and a marine reserve since 1990. The total area of the marine reserve is 4,400 ha. Two of the islands (the largest and the smallest, Grossa and Carallot) have a special protection regime (integral reserve).

Our main prediction was that changes in distribution or number of breeding pairs on these two islands would be small whereas changes in both parameters on Ferrera and Foradada–Lobo would be larger.

Data regarding public use of the islands and breeding performance of Eleonora’s Falcons were obtained from unpublished reports (Reserva Natural Islas Columbretes, 1988–2001) supplied by the regional government from 1988 to 2001.

Grossa N

Ferrera Iberian peninsula

1

Mancolibre

Western Mediterranean

350

Foradada

700 km

Lobo

N

0 20 m

Carallot

Fig. 1. Map of the study area showing the location of Eleonora’s Falcons nests in 2001 and the approximate location of buoys for tourist boats in Grossa Island (dotted circle).

Fig. 1. Mapa de las islas Columbretes. Se muestra la localización de los nidos de halcón de Eleonora en la Isla Grossa en 2001 y la localización aproximada de las boyas de amarre para embarcaciones turísticas (círculo con puntos).

49

Animal Biodiversity and Conservation 25.2 (2002)

Results

Human presence was measured as the number of boat licence plates recorded daily (boats–day hereafter).

Boats were tied up to the buoys located around the islands and the team of three wardens living on the main island counted them daily by means of a terrestrial telescope.

The monitoring of boats was constant throughout the study period. The number of breeding pairs was also determined by knowledgeable wardens of the reserve by inspecting the islands from a boat early in the breeding season to locate and count breeding pairs and later by double–checking the existence of nests from the mainland.

Productivity (i.e. number of fledglings per nest) was estimated from the content of nests when visited for chick ringing in mid September, using field procedures developed by two members of the study team (AM, DO).

Monitoring and ringing of falcons was approximately constant throughout the study period. In 1999, the overall number of breeding pairs was not estimated due to lack of an appropriate boat to visit all the islands, but productivity was estimated from nests located on Grossa Island and Mancolibre (fig. 1).

Inter–annual variation in the number of boats– day is shown in table 1. The overall trend was a progressive increase in human presence on the islands (r s = 0.97, n = 13, p < 0.001). Monthly variations in the number of boats–day are shown in figure 2. Boats–day clearly peaked in July and August precisely the time when falcons were laying and incubating their eggs (DOLZ & DIES, 1987). However, the number of breeding pairs remained approximately constant through the years (26 ± 2.16 pairs, mean ± SD, n = 13) as did their productivity (1.64 ± 0.33, mean ± SD, n = 13) (table 1). In fact, correlations between years and number of pairs (rs = 0.18, n = 13, p > 0.05) and productivity (rs = 0.50, n = 13, p > 0.05) were not significant.

No significant correlation was found either between overall numbers of boats–day during the breeding period (July–September) and numbers of breeding pairs (rs = –0.14, n = 12, p = 0.66,) or between overall number of boats– day during the breeding period and productivity (rs = 0.23, n = 12, p = 0.46). Inter–annual variation in the use of the various islands by breeding falcons and tourist boats is shown in table 1.

Table 1. Number of nests and productivity of Eleonora’s Falcons (Falco eleonorae) detected on each island of the Columbretes archipelago during the period 1988–2000 (source: Reserva Natural Islas Columbretes, 1988–2001): ND. No data available; In brackets number of boats–day.

Tabla 1. Número de nidos y productividad de halcones de Eleonora (Falco eleonorae) detectados en cada una de las islas del archipiélago de las Columbretes durante el periodo 1988–2000 (datos extraídos de: Reserva Natural Islas Columbretes, 1988–2001): ND. Información no disponible; entre paréntesis se indica el número de barcos–día durante el periodo reproductor.

Year

Carallot

Foradada–Lobo

Ferrera

Grossa

Productivity

Total

1988

1

6

5

11

–

23 (184)

1989

–

–

–

–

1.37

22 (242)

1990

–

–

–

–

1.73

28 (374)

1991

–

–

–

–

1.41

27 (509)

1992

0 (2)

8 (31)

4 (11)

15 (592)

1.53

27 (636)

1993

1 (12)

3 (65)

7 (31)

15 (537)

1.66

26 (645)

1994

1 (19)

4 (131)

5 (36)

14 (606)

1.0

24 (792)

1995

0 (33)

5 (86)

8 (40)

13 (493)

1.61

26 (652)

1996

1 (106)

3 (107)

6 (38)

13 (481)

1.89

23 (732)

1997

1 (0)

3 (94)

6 (66)

13 (695)

1.35

23 (855)

1998

1 (0)

3 (93)

8 (45)

15 (715)

2.0

27 (853)

1999

1 (0)

– (75)

– (66)

12 (804)

2.0

– (945)

2000

1 (0)

1 (86)

9 (51)

14 (758)

1.6

25 (895)

2001

1

4

10

15

2.17

30

Martínez–Abrain et al.

50

1997 1998

700

Boats/day

600

1999 2000

500 400 300 200 100 0 E

F

M

A

Ma

J Months

Jl

Ag

S

O

N

D

Fig. 2. Monthly variation in the number of boats–day at the Columbretes Islands during the period 1997–2000: E. January; F. February; M. March; A. April; Ma. May; J. June; Jl. July; Ag. August; S. September; O. October; N. November; D. December.

Fig. 2. Variación mensual en el número de barcos–día en las islas Columbretes durante el periodo 1997–2000: E. Enero; F. Febrero; M. Marzo; A. Abril; Ma. Mayo; J. Junio; Jl. Julio; Ag. Agosto; S. Septiembre; O. Octubre; N. Noviembre; D. Diciembre.

The percentage of falcons breeding on Ferrera (in relation to the total breeding pairs of Ferrera + Foradada–Lobo) increased over time (table 1).

Indeed, a non–parametric correlation run to check whether this percentage had changed over with time showed a significant strong correlation (r s = 0.78, p = 0.014), although correlations between annual numbers of breeding pairs and annual numbers of boats– day at Ferrera and Foradada (considering both the number of boats–day at years t and t–1, to test for any influence of tourist presence the year before) were all not significant.

Discussion Shifts in island use by Eleonora’s falcons seem to have affected only the colonies on Ferrera and Foradada, the two islands with no special protection regime. Anchoring of boats around Carallot is not permitted as the distance from Grossa makes it difficult to keep activities carried out within the restricted area under control.

Nevertheless, tourist activities such as scuba– diving are allowed on Grossa, where the island wardens, who have a permanent base on this island, can more easily monitor the activities of visitors; boats must be tied up to buoys in the bay, thereby remaining far from falcon nests which are mostly located in the outer cliffs of the island (see fig. 1).

We are not aware of any factor (e.g. food, nest– site availability, competing species, ectoparasites)

other than human presence that may have influenced the change in the distribution of breeding pairs, albeit the exact way in which human presence may have affected falcons remains unknown. However, the fact that scuba–divers prefer Foradada as compared to Ferrera, because of the existence of submerged archs (S. Sales, pers. com.) may have played some role.

Our data indicate that high tourist presence coincideds with a loss of pairs at Foradada–Lobo and that low tourist presence coincided with an increase in the number of pairs at Ferrera, and that there were no changes in the overall number of breeding pairs (i.e. the colony remains stable and hence increases and decreases in the number of falcon pairs in each island are only rearrangements within the archipelago). However, only experimental manipulation of the number of boats–day could unequivocally demonstrate a cause–effect relationship. We predict that any marked decreased in the number of boats around Foradada–Lobo would be paralleled by an increase in the number of falcon breeding pairs.

These spatial changes may not be dangerous for short–term colony persistence. The clumping of breeding pairs in social species, such as the Eleonora’s Falcon, can have positive consequences for breeding performance; one possible short– term conservation option would be to increase protection of Ferrera (where the level of human presence is quickly approaching that of Foradada– Lobo), allowing only Foradada–Lobo as a tourist destination. However, given the reduced size of the archipelago, high protection on Foradada–

51

Animal Biodiversity and Conservation 25.2 (2002)

Lobo should also be attained in the future so as not to threaten long–term colony persistence and growth (e.g. banning the presence of boats within a buffer zone around the island).

Tourism affecting Eleonora’s Falcons in the Columbretes Islands was previously reported in 1997, when a marked decrease in breeding pairs occurred in a small rocky islet located beside the main island (Mancolibre, see fig. 1). This reduction was probably caused by excessive presence of scuba divers according to SÁNCHEZ (1997). The environmental authorities experimentally removed a buoy placed close to the isle, and banned the transit of boats around the islet. This sub–colony quickly recovered its usual number of breeding pairs in 1998. Hence, conservation measures addressed to reduce human presence around the colonies of Eleonora’s Falcons can give positive results and should be further employed to determine the role of human presence on the patterns of island use by falcons.

Acknowledgements This study is contribution no. 7 to the LIFE–NATURE program BA–3200/98/447 “Conservation of island SPAs in the Valencian region”, financed by the Generalitat Valenciana and the EU. This investigation would not have been possible without the work of all the wardens on the Columbretes reserve. We specially thank Roque

Belenguer and Vicente Ferrís for their valuable assistance during field work. Eduardo Mínguez and a second anonymous referee provided valuable comments. Covadonga Viedma and Mario Giménez, critically read drafts of the manuscript.

References DOLZ, J. C. & DIES, I., 1987. El halcón de Eleonor (Falco eleonorae, Gené) en las Islas Columbretes.

In: Islas Columbretes: Contribución al estudio de su medio natural: 241–263 (L. A. Matilla, J. L. Carretero & A. M. García–Carrascosa, Eds.).

Generalitat Valenciana, Valencia.

HILL, D., HOCKIN, D., PRICE, D., TUCKER, G., MORRIS, R. & TREWEEK, J., 1997. Bird disturbance: Improving the quality and utility of disturbance research.

Journal of Applied Ecology, 34: 275–288.

RISTOW, D., 1999. International species action plan for Eleonora’s Falcon Falco eleonorae. BirdLife International. Unpublished report.

S ÁNCHEZ, A., 1997. Preliminary report on the impact of scuba–diving on the breeding population of Eleonora’s Falcon of the Columbretes Islands. Generalitat Valenciana, unpublished report.

TUCKER, G. M. & HEATH, M. F., 1994. Birds in Europe: their conservation status. BirdLife Conservation Series No. 3. BirdLife International, Cambridge.

WALTER, H., 1979. Eleonora’s Falcon: adaptations to prey and habitat in a social raptor. Chicago University Press, Chicago.

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 25.2 (2002)

53

Effects of fire management on the richness and abundance of central North American grassland land snail faunas J. C. Nekola

Nekola, J. C., 2002. Effects of fire management on the richness and abundance of central North American grassland land snail faunas. Animal Biodiversity and Conservation , 25.2: 53–66.

Abstract Effects of fire management on the richness and abundance of central North American grassland land snail faunas.— The land snail faunas from 72 upland and lowland grassland sites from central North America were analyzed. Sixteen of these had been exposed to fire management within the last 15 years, while the remainder had not. A total of 91,074 individuals in 72 different species were observed. Richness was reduced by approximately 30% on burned sites, while abundance was reduced by 50–90%.

One–way ANOVA of all sites (using management type as the independent variable), a full 2–way ANOVA (using management and grassland type) of all sites, and a 2–way ANOVA limited to 26 sites paired according to their habitat type and geographic location, demonstrated in all cases a highly significant (up to p < 0.0005) reduction in richness and abundance on fire managed sites.

Contingency table analysis of individual species demonstrated that 44% experienced a significant reduction in abundance on firemanaged sites. Only six species positively responded to fire. Comparisons of fire response to the general ecological preferences of these species demonstrated that fully 72% of turf–specialists were negatively impacted by fire, while 67% of duff–specialists demonstrated no significant response. These differences were highly significant (p = 0.0006). Thus, frequent use of fire management represents a significant threat to the health and diversity of North American grassland land snail communities.

Protecting this fauna will require the preservation of site organic litter layers, which will require the increase of fire return intervals to 15+ years in conjunction with use of more diversified methods to remove woody and invasive plants.

Key words: Land snail, Biodiversity, Conservation, Fire management, Grassland, North America.

Resumen Efectos de la gestión con fuego sobre la riqueza y abundancia de la fauna de caracoles terrestres de las praderas de América del Norte.— Se analiza la fauna de caracoles terrestres de 72 praderas en mesetas y llanuras de la región central de América del Norte. En 16 de ellas se habían efectuado intervenciones de incendio controlado durante los últimos 15 años, mientras en el resto no. Se observaron un total de 91.074 individuos de 72 especies diferentes. La riqueza en especies estaba reducida en un 30% en las áreas quemadas, mientras que la abundancia de individuos estaba reducida en un 50–90%. Un ANOVA unidireccional de todas las áreas (usando como variable independiente el tipo de intervención), un ANOVA bidireccional completo (usando el tipo de intervención y el tipo de pradera) en todas las áreas y un ANOVA bidireccional limitado a 26 áreas agrupadas según su tipo de hábitat y localización geográfica, demostró en todos los casos una reducción altamente significativa de la riqueza y de la abundancia (hasta p < 0,0005) en áreas sometidas a incendio. Un análisis individual de las especies mediante tablas de contingencia demostró que el 44% experimentaron una reducción significativa de su abundancia en las áreas quemadas. Sólo seis especies respondieron positivamente al fuego. Comparando la respuesta al fuego con las preferencias ecológicas generales de estas especies se demostró que al menos el 72% de las especialistas que viven en sustrato herbáceo fueron afectadas negativamente por el fuego mientras que el 67% de las que viven en sustrato húmico no demostraron ninguna respuesta significativa. Estas diferencias fueron altamente significativas (p = 0,0006). Así pues, el uso frecuente del fuego representa una amenaza significativa para la salud y diversidad de las comunidades de caracoles terrestres de las praderas de América del Norte. La protección de esta fauna requerirá la preservación de las capas de materia orgánica y la ampliación de los intervalos entre las actuaciones de quema a periodos superiores a 15 años, así como el uso de métodos más diversos para eliminar las plantas leñosas e invasivas.

Palabras clave: Caracol terrestre, Biodiversidad, Conservación, Gestión con fuego, Praderas, América del Norte.

(Received: 9 IV 02; Final acceptance: 18 VI 02) Jeffrey C. Nekola, Dept. of Natural and Applied Sciences, Univ. of Wisconsin–Green Bay, Green Bay, Wisconsin 54311 USA. E–mail: nekolaj@uwgb.edu

ISSN: 1578–665X

© 2002 Museu de Ciències Naturals

Nekola

54

Introduction Fire has long been implicated in the maintenance of central North American grassland communities (WEAVER, 1954; CURTIS, 1959). Numerous native plant species respond to fire by increasing their growth and reproductive rates (EHRENREICH & AIKMAN, 1963; KUCERA & KOELLING, 1964; TOWNE & OWENSBY, 1984). One of the most direct effects of prairie fire is the removal of the soil mulch layer, which has been implicated in the ‘stagnation’ of prairie plant communities through the delay of initial spring growth, thinning of grass stem density, and prevention of herbaceous understory development (WEAVER & ROWLAND, 1952; KUCERA & KOELLING, 1964). Fire is also thought to limit invasion of woody and exotic plants into native prairie habitats (e.g., PAULY, 1985; ROOSA, 1984). For these reasons, prescribed fire has become the management tool of choice by prairie conservation groups throughout the midwestern USA (COLLINS & WALLACE, 1990).

However, an increasing body of research suggests that fire is not universally beneficial all prairie biota. Fire depresses growth and reproductive rates of native C3 prairie plants (DIX, 1960; HADLEY, 1970; HILL & PLATT, 1975), which make up at least 50% of the native flora north of 44o N (STOWE & TEERI, 1978; SIMS, 1988). Fire has also been implicated in the loss and/or reduction of numerous native prairie invertebrate species including Lepidoptera, Homoptera, Hymenoptera, and Araneae (SWENGEL, 1996, 1998; HARPER et al., 2000). The effects of such practices on prairie soil biodiversity are largely undocumented. Combustion of mulch through repeated fire episodes will remove the detritusphere, one of the most important reservoirs for soil biodiversity (COLEMAN & CROSSLEY, 1996). HARPER et al. (2000) documented significant reductions in Collembola following Illinois prairie fires. As the soil fauna represents one of the largest species pools in terrestrial ecosystems (BEHAN–PELLETIER & NEWTON, 1999), the potential impacts of such processes on total site biodiversity may be large.

Although not as hyper–diverse as bacteria, fungi, nematodes, and arthropods, molluscs still represent one of the more important components of soil biodiversity (RUSSELL–HUNTER, 1983). Almost 600 species are known from eastern North America (HUBRICHT, 1985), with up to 21 taxa cooccurring within 400 cm2 microhabitats (NEKOLA & SMITH, 1999). Most of these taxa represent generalist detritivores that live in and on dead organic material (BURCH & PEARCE, 1990) As almost 90% of snails occur within 5 cm of the soil surface (HAWKINS et al., 1998), protection of this fauna will likely be tied to the fate of mulch layers. Disturbances such as logging, recreational or urban development, or bedrock and soil removal cause dramatic changes in woodland snail communities with duff soil surfaces (NEKOLA, in press a). The impact of fire, and associated detritusphere removal, on snail

communities is unclear. Fire has been suggested to negatively influence the faunas of Aegean islands (W ELTER –S CHULTES & W ILLIAMS , 1999), Queensland fens (STANISIC 1996), and Tasmanian woodlands (REGAN et al., 2001). However, FREST & JOHANNES (1995) state that molluscs are able to survive natural fires in northwestern North America, and THELER (1997) argued that xeric prairie faunas in Wisconsin owe their existence to frequent fires that keep grassland areas treeless. Unfortunately, no data was presented by these various authors to validate such conflicting statements.

To evaluate this issue, the richness and abundance of land snails was quantitatively compared between unburned and recently (< 15 year) burned sites in the midwestern USA, including 13 pairs of sites which possess similar habitats and are spatiall proximate. From these, the following questions will be considered: 1. Is there a significant difference in land snail community richness between burned and unburned grasslands? 2. Is there a significant difference in land snail abundance between burned and unburned grasslands? 3. What species show positive, negative, or no response to fire?

What ecological factors (if any) may help explain these responses?

Materials and methods Study Sites Seventy two grassland sites were surveyed between May 1996–November 2001 for terrestrial molluscs across a 850 km extent of central North America (fig. 1, table 1). Sites are generally centered on northwestern Minnesota and northeastern Iowa. Forty–two occur in Minnesota, 25 in Iowa, and 5 in Wisconsin. Thirty–two sites represent upland habitats (including tallgrass prairie, sand prairie, and bedrock glades), while the remaining 40 are lowland sites (including wet prairie, sedge meadow, and fens). Previous use of fire management on sites was assessed by either observing carbonized woody plant stems or other debris on the ground surface, or through interviews with site managers or other knowledgeable individuals. No use of fire management was noted from 56 sites (88% of total), while 16 (22%) had been subjected to some amount of prescribed burning. Eleven of these burned sites occur in Minnesota, while the remaining five occur in Iowa. The latitude– longitude location of each site was determined using either USGS 7.5 minute topographic maps or a hand–held GPS. Field Methods Documentation of terrestrial gastropod faunas from each site was accomplished by hand

55

Animal Biodiversity and Conservation 25.2 (2002)

collection of larger shells and litter sampling for smaller taxa within 100–1,000 m2 areas that contained examples of all major microhabitats and were thus representative of the larger site.

The actual grain size employed was determined by the minimum size necessary to emcompass all microhabitats. Soil litter sampling was primary used as it provides the most complete assessment of grassland faunas (OGGIER et al., 1998). A single site sample consisted of a composite of individual soil litter subsamples of approximately 200 ml collected from appropriate microhabitats. As suggested by E MBERTON et al. (1996), litter collections were made at places of high micromollusc density, with a constant volume (approximately 4 liters) being gathered from each site. Sampling was generally comprised of: 1. Small blocks (ca. 125 cm3) of turf; 2. Loose soil and leaf litter accumulations under or adjacent to shrubs, cobbles, boulders, and/or hummocks; and 3. Other microsites supporting relatively thick mulch layers.

L aboratory procedures Samples were slowly and completely dried in either a low–temperature soil oven (ca. 80–95oC) or in full sun in a greenhouse. Dried samples were then soaked in water for 3–24 hours, and subjected to careful but vigorous water disaggregation through a standard sieve series (ASTME 3/8" (9.5 mm), #10 (2.0 mm), #20 (0.85), and #40 (0.425 mm) mesh screens). Sieved sample fractions were then dried and passed again through the same sieve series. These dry, resorted fractions were hand picked against a neutralbrown background. All shells and shell fragments were removed.

All identifiable shells from each site were assigned to species (or subspecies) using the author’s reference collection and the Hubricht Collection at the Field Museum of Natural History (FMNH), with the total number of shells per species per site being recorded. The total number of unassignable, immature individuals was also counted from each site. All specimens have been catalogued and are housed in the author’s collection at the University of Wisconsin–Green Bay. Nomenclature generally follows that of HUBRICHT (1985), with updates and corrections by FREST (1990, 1991) and NEKOLA (in press b). The general ecological preferences (turf specialist, duff–specialist or generalist) of each species is based upon analyses presented in NEKOLA (in press a).

Statistical procedures Differences in species richness and total shell abundance between burned and unburned grassland sites were analyzed via ANOVA. Initially, 1–way ANOVAs were preformed on the entire dataset. However, the effect of fire may be

Fig. 1. Map of study region, showing location of surveyed grassland sites: F Unburned upland; M Burned upland; H Unburned lowland; F Burned lowland.

Fig. 1. Mapa del área de estudio que muestra la localización de las praderas estudiadas: F Meseta no quemada; M Meseta quemada; H Llanura no quemada; F Llanura quemada.

obscured in this analysis due to confounding effects of habitat type and geographic location.

To help control for this, two additional sets of ANOVAs were conducted. First, full 2–way ANOVAs were calculated for all sites using grassland type (upland vs. lowland) and management history (burned vs. unburned) as the independent variables. Second, 13 pairs of sites representing closely similar habitats within the same geographic region, but differing in their fire management history, were selected. These site pairs are (first site is burned, second is unburned): Malmberg Prairie vs. Sandpiper Prairie; Pankratz Mesic Prairie vs. Radium NE; Pankratz Low Prairie vs. Bjornson WMA; Pankratz Fen vs. Faith South; Marcoux WMA vs. Cyr Creek; East Park WMA vs. Goose Lake; Felton Fen 1 vs. Ogema West; Waubun SE vs. Eastlund Lake; Chicog vs. Tansen; Beemis Creek vs. Hampton East; Fayette vs. Decorah Glade; Baty Glade vs. Canton Glade; Brayton–Horsley vs.

Stapleton Church. A 2–way ANOVA without interaction was then calculated for these sites, with site pair identity and management type representing independent variables.

Nekola

56

Table 1. Location, grassland type, management, species richness and total number of collected individuals from sample sites: GT. Grassland type; M. Management; R. Richness; I. Individuals.

Tabla 1. Localización, tipo de pradera, gestión, riqueza de especies y número total de individuos recogidos en cada área de estudio: GT. Tipo de pradera; M. Gestión; R. Riqueza; I. Individuos.

State / County / Site Name

Location

GT

91°17'12" W – 43°27'13" N

Upland

91°29'1" W – 43°8'1" N

M

R

I

Unburned

21

632

Upland

Unburned

23

2,708

92°6'29" W – 42°48'36" N

Lowland

Burned

16

627

91°51'7" W – 42°22'27" N

Lowland

Unburned

16

3,217

Rowley North Fen

91°51'3" W – 42°22'35" N

Lowland

Unburned

17

3,231

Rowley West Fen

91°54'40" W – 42°22'15" N

Lowland

Unburned

22

2,250

93°11'11" W – 43°10'36" N

Lowland

Unburned

19

4,770

92°6'14" W – 43°1'35" N

Lowland

Unburned

18

1,065

Postville Fen

91°33'59" W – 43°2'3" N

Lowland

Unburned

12

252

Turkey River Mounds

91°2'11" W – 42°42'46" N

Upland

Unburned

22

870

90°39'5" W – 42°1'12" N

Upland

Unburned

12

310

90°44'30" W – 42°32'55" N

Upland

Unburned

18

375

Iowa Allamakee County Fish Farm Mounds Williams Creek 3 Bremer County Brayton–Horsley Fen Buchanan County Rowley Fen

Cerro Gordo County Buffalo Slough Chickasaw County Stapelton Church Fen Clayton County

Clinton County Maquoketa South Dubuque County Roosevelt Road Fayette County Fayette

91°47'28" W – 42°50'11" N

Upland

Burned

13

254

Turner Creek 1 Fen

91°52'11" W – 42°58'15" N

Lowland

Unburned

16

1,071

Beemis Creek

93°1'18" W – 42°59'39" N

Upland

Burned

8

192

Juniper Hill

92°59'2" W – 43°3'10" N

Upland

Unburned

12

206

93°8'13" W – 42°43'42" N

Upland

Unburned

15

381

Hayden Prairie

92°23'4" W – 43°26'30" N

Upland

Burned

12

132

Staff Creek Fen

92°30'34" W – 43°26'41" N

Lowland

Unburned

15

1,599

90°34'9" W – 42°4'23" N

Upland

Unburned

15

340

90°59'52" W – 42°10'46" N

Upland

Unburned

19

446

Baty Glade

91°39'14" W – 42°11'44" N

Upland

Burned

16

345

Paris Fen

91°35'42" W – 42°13'40" N

Lowland

Unburned

12

1,254

Floyd County

Franklin County Hampton East Howard County

Jackson County Hamilton Glade Jones County Canton Glade Linn County

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Animal Biodiversity and Conservation 25.2 (2002)

Table 1. (Cont.)

State / County / Site Name

Location

GT

92°38'11" W – 43°22'49" N

Lowland

91°46'11" W – 43°18'55" N

Upland

Audubon South Fen

95°58'47" W – 46°49'58" N

Lowland

Callaway North

95°55'22" W – 47°3'57" N

Upland

Greenwater Lake Fen

95°29'59" W – 46°59'20" N

Lowland

Ogema West Fen

95°55'59" W – 47°6'32" N

Lowland

Straight Lake

95°18'40" W – 46°58'40" N

Upland

95°18'21" W – 48°15'56" N

Lowland

M

R

I

Unburned

18

2,926

Unburned

18

605

Unburned

15

1,816

Unburned

19

362

Unburned

20

2,132

Unburned

16

5,001

Unburned

13

281

Unburned

14

1,403

Mitchell County Stone School Fen Winneshiek County Decorah Glade Minnesota Becker County

Beltrami County Fourtown Fen Clay County Barnesville WMA

96°17'34" W –46°43'5" N

Upland

Unburned

11

469

Barnesville WMA Fen

96°17'38" W – 46°43'9" N

Lowland

Unburned

13

436

Bjornson WMA

96°21'24" W – 46°45'44" N

Lowland

Unburned

14

436

Bluestem Prairie

96°28'45" W – 46°51'18" N

Upland

Burned

15

371

Felton Prairie 1 Fen

96°26'21" W – 47°3'51" N

Lowland

Burned

15

2,370

Felton Prairie 2 Fen

96°26'20" W – 47°4'0" N

Lowland

Unburned

14

3,131

Felton Prairie

96°26'1" W – 47°3'34" N

Upland

Unburned

5

63

96°11'17" W – 46°42'14" N

Upland

Unburned

10

146

95°14'35" W – 47°45'41" N

Lowland

Unburned

9

126

91°45'0" W – 43°40'5" N

Upland

Unburned

21

1,151

Twin Pines Farm

91°22'45" W – 43°44'48" N

Upland

Unburned

24

591

Yucatan Twp.

91°38'28" W – 43°43'23" N

Upland

Unburned

20

765

Eastlund Lake

95°47'5" W – 47°26'41" N

Upland

Unburned

13

490

Mahnomen North

95°58'8" W – 47°21'27" N

Upland

Unburned

18

806

Waubun SE

95°54'55" W – 47°9'57" N

Lowland

Unburned

18

2,915

Waubun SE

95°55'4" W – 47°10'5" N

Upland

Burned

8

220

96°16'44" W – 48°31'57" N

Lowland

Burned

14

735

Florian WMA

96°33'21" W – 48°26'33" N

Lowland

Unburned

17

3,923

Radium NE

96°32'38" W – 48°16'49" N

Upland

Unburned

12

493

Faith South

96°5'12" W – 47°15'42" N

Lowland

Unburned

16

3,047

Prairie Smoke Dunes

96°18'22" W – 47°27'44" N

Upland

Unburned

3

19

Sandpiper Prairie

96°24'22" W – 47°14'43" N

Lowland

Unburned

12

1,261

Tansen Clearwater County Bagley Lake Fen Filmore County Vesta Creek Houston County

Mahnomen County

Marshall County East Park WMA

Norman County

Nekola

58

Table 1. (Cont.)

State / County / Site Name

Location

GT

M

R

I

Goose Lake

96°27'44" W – 48°5'37" N

Lowland

Unburned

17

996

Higenbotham WMA

96°17'41" W – 48° 0'22" N

Lowland

Unburned

22

1,114

96°21'9" W – 48°3'52" N

Lowland

Unburned

15

2,218

Pennington County

Sanders Fen Polk County Chicog Prairie

96°23'14" W – 47°35'53" N

Upland

Burned

2

153

Erskine North

96°0'3" W – 47°44'17" N

Lowland

Unburned

19

741

Gulley Fen

95°37'22" W – 47°48'13" N

Lowland

Unburned

19

2,032

Malmberg Prairie

96°49'25" W – 47°43'52" N

Lowland

Burned

7

563

Pankratz Prairie

96°26'37" W – 47°43'23" N

Lowland

Burned

12

314

Pankratz Prairie

96°26'31" W – 47°43'23" N

Upland

Burned

11

159

Pankratz Prairie

96°26'48" W – 47°43'9" N

Lowland

Burned

7

190

Crane WMA

95°42'49" W – 47°53'27" N

Lowland

Unburned

15

425

Cyr Creek

96°16'12" W – 47°48'10" N

Lowland

Unburned

22

1,845

Marcoux WMA

96°13'27" W – 47°47'55" N

Lowland

Burned

12

688

91°23'28" W – 43°56'53" N

Upland

Burned

19

788

88°54'20" W – 43°57'47" N

Lowland

Unburned

20

3,454

87°30'40" W – 44°11'52" N

Upland

Unburned

4

6

88°40'54" W – 42°48'2" N

Lowland

Unburned

20

1,106

88°18'25" W – 43°22'42" N

Lowland

Unburned

20

2,858

89°16'59" W – 44°0'16" N

Lowland

Unburned

19

1,466

Red Lake County

Winona County Great River Bluffs Wisconsin Green Lake County Berlin Fen Manitowoc County Point Beach St. Forest Walworth County Bluff Creek Fen Washington County Allenton Fen Waushara County Bass Lake Fen

The central tendencies in these various relationships were graphically represented via box plots. In box plots, the central line represents the median of the sample, the margins of the box represent the interquartile distances, and the fences represent 1.5 times the interquartile distances. For data having a Gaussian distribution, approximately 99.3% of the data will fall inside of the fences (VELLEMAN & HOAGLIN, 1981). Outliers falling outside of the fences are shown with asterisks.

The average number of individuals per species per site was determined for burned uplands, unburned uplands, burned lowlands, and

unburned lowlands. The average proportion of each species in the total community for each site was calculated for each management/habitat type.

These proportions were placed in rank order, and plotted vs. log–transformed frequency to create dominance–diversity curves (WHITTAKER, 1975).

The response of individual species to fire was analyzed through log–linear modelling, as predicted values in the associated contingency table were sparse (< 5) in more than one–fifth of cells (ZAR, 1984). The total number of individuals within all burned or unburned sites was compared to a null expectation of equal occurrence

59

Animal Biodiversity and Conservation 25.2 (2002)

Table 2. List of encountered species, with their average abundances from burned and unburned sites. P–values are based on log-likelihood ratio tests, with the two–tailed significance threshold being lowered to p = 0.000347 to account for the 72 tested species. General ecological preferences are based on NEKOLA (in press a). Turf–specialists represent those species demonstrating at least a p < 0.05 preference to sites with a friable upper A soil horizon supporting few living plant roots.

Turf specialists represent those species demonstrating at least a p < 0.05 preference to sites with an upper A soil horizon that is bound together with living plant roots. Species without preferences were too infrequently encountered by NEKOLA (in press a) to be statistically assigned: AvU. Average unburned; Abb. Abundance burned; Ecp. Ecological preference (T. Turf; D. Duff; G. Generalist.)

Tabla 2. Lista de especies detectadas, con sus abundancias medias en áreas quemadas y no quemadas. Los valores de P se basan en tests de cociente de probabilidad logarítmica, con el umbral de significación de doble cola reducido hasta p = 0,000247 para las 72 especies estudiadas. Las preferencias ecológicas generales se basan en NEKOLA (in press a). Las especies que viven en sustrato herbáceo presentan una preferencia de al menos p < 0,05 por las zonas con horizonte de tierra friable superior A provisto de escasas raíces de plantas vivas. Las especies que viven en sustrato herbáceo presentan una preferencia de al menos p < 0,05 por las zonas cuyo horizonte se mantiene unido por raíces de plantas vivas. Las especies sin preferencias resultaron excesivamente infrecuentes según NEKOLA (in press a) para consignarlas estadísticamente: AvU. Medias en áreas no quemadas; Abb. Abundancia en áreas quemadas; Ecp. Preferencia ecológica (T. Sustrato herbáceo; D. Sustrato húmico; G. Generalista.)

Species Negative responses

Carychium exiguum (Say, 1822) Carychium exile H. C. Lea, 1842 Catinella exile (Leonard, 1972) Catinella "vermeta" Deroceras laeve (Müller, 1774) Discus cronkhitei (Newcomb, 1865) Euconulus alderi (Gray, 1840) Gastrocopta contracta (Say, 1822) Gastrocopta holzingeri (Sterki, 1889) Gastrocopta pentodon (Say, 1821) Gastrocopta procera Gould, 1840 Gastrocopta rogersensis Nekola & Coles, 2001 Gastrocopta similis (Sterki, 1909) Gastrocopta tappaniana (C. B. Adams, 1842) Hawaiia minuscula (A. Binney, 1840) Helicodiscus n. sp.

Nesovitrea binneyana (Morse, 1864) Nesovitrea electrina (Gould, 1841) Oxyloma retusa (I. Lea, 1834) Pomatiopsis lapidaria (Say, 1817) Punctum minutissimum (I. Lea, 1841) Punctum n. sp.

Punctum vitreum H. B. Baker, 1930 Stenotrema leai leai (A. Binney) Striatura milium (Morse, 1859) Strobilops affinis Pilsbry, 1893 Triodopsis multilineata (Say, 1821) Vallonia pulchella (Müller, 1774)

AvU

Abb

P–value

273.607 5.196

90.250 0.000

0.0000000 0.0000000

T D

58.446 1.482

1.625 0.000

0.0000000 0.0000001

T T

4.036 16.143

1.188 5.000

0.0000050 0.0000000

G G

43.054 21.232

8.375 5.875

0.0000000 0.0000000

T G

36.196 9.661

17.938 4.875

0.0000000 0.0000072

D D

2.304 5.518

0.000 0.062

0.0000000 0.0000000

T T

21.518 112.929

4.125 33.375

0.0000000 0.0000000

T T

36.286 1.071

23.062 0.062

0.0000000 0.0001509

G T

1.500 80.179

0.000 22.688

0.0000001 0.0000000

D T

21.268 1.196

8.750 0.000

0.0000000 0.0000021

T –

26.286 41.982

10.500 12.625

0.0000000 0.0000000

D T

16.536 2.696

2.812 0.375

0.0000000 0.0000004

D T

0.714 74.911

0.000 4.312

0.0002470 0.0000000

G T

1.571 23.321

0.062 11.688

0.0000016 0.0000000

G T

Ecp

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60

Tabla 2. (Cont.)

Species Vertigo elatior Sterki, 1894 Vertigo milium (Gould, 1840) Vertigo morsei Sterki, 1894 Vitrina limpida Gould, 1850 No response Anguispira alternata (Say, 1817) Catinella avara (Say, 1824) Cochlicopa lubrica (Müller, 1774) Cochlicopa lubricella (Porro, 1838) Columella simplex (Gould, 1841) Discus catskillensis (Pilsbry, 1898) Euconulus fulvus (Müller, 1774) Euconulus polygyratus (Pilsbry, 1899) Gastrocopta abbreviata (Sterki, 1909) Gastrocopta armifera (Say, 1821) Glyphyalinia indentata (Say, 1823) Haplotrema concavum (Say, 1821) Hawaiia n. sp.

Helicodiscus inermis H. B. Baker, 1929 Helicodiscus parallelus (Say, 1817) Helicodiscus shimeki Hubricht, 1962 Helicodiscus singleyanus (Pilsbry, 1890) Hendersonia occulta (Say, 1831) Mesodon clausus clausus (Say, 1821) Oxyloma peoriensis (Wolf in Walker, 1892) Pupoides albilabris (C. B. Adams, 1821) Stenotrema barbatum (Clapp, 1904) Stenotrema fraternum fraternum (Say, 1824) Succinea indiana Pilsbry, 1905 Succinea ovalis Say, 1817 Triodopsis alleni (Wetherby in Sampson, 1883) Vallonia gracilicosta Reinhardt, 1883 Vertigo arthuri (von Martens, 1884) Vertigo gouldi (A. Binney, 1843) Vertigo nylanderi Sterki, 1909 Vertigo ovata Say, 1822 Vertigo tridentata Wolf, 1870 Zonitoides arboreus (Say, 1816) Zonitoides nitidus (Müller, 1774) Positive response Gastrocopta corticaria (Say, 1816) Strobilops labyrinthica (Say, 1817) Vallonia costata (Müller, 1774) Vallonia parvula Sterki, 1892 Vallonia perspectiva Sterki, 1892 Vertigo pygmaea (Draparnaud, 1801)

AvU 41.875 59.357 3.589 1.143

Abb 5.875 36.375 0.375 0.000

P–value 0.0000000 0.0000000 0.0000000 0.0000035

Ecp T T T G

0.018 7.286 0.464 1.714 0.071 0.357 3.429 0.018 0.000 1.232 2.732 0.411 2.571 0.679 5.393 0.286 0.375 0.036 0.054 0.125 8.393 0.107 0.054 0.000 0.143 0.071 11.500 0.643 0.018 0.036 5.750 0.375 4.143 0.464

0.000 8.000 0.000 1.938 0.188 0.000 1.625 0.000 0.062 1.188 3.250 0.000 1.750 1.812 6.438 0.000 1.125 0.062 0.000 0.000 7.062 0.000 0.062 0.188 0.188 0.000 11.062 0.000 0.000 0.000 4.000 0.062 4.625 0.000

0.5622176 0.5185276 0.0031253 0.6798546 0.4068651 0.0095467 0.0040433 0.5622176 0.2039785 0.9197258 0.4543545 0.0054455 0.1616094 0.0089186 0.2831711 0.0204383 0.0247064 0.7606162 0.3154693 0.1251903 0.2324971 0.1557229 0.9262276 0.0277912 0.7834904 0.2464148 0.7459095 0.0005065 0.5622176 0.4124393 0.0472312 0.0738709 0.5650976 0.0031253

D T D G D D D D – G D G T – G D G D D – T D D – D D D – D T T D D T

0.732 9.661 1.804 8.250 2.143 0.000

3.500 22.375 6.438 13.250 5.625 0.562

0.0000003 0.0000000 0.0000000 0.0001267 0.0000055 0.0001385

D D G T D G

61

Animal Biodiversity and Conservation 25.2 (2002)

p = 0.001

p = 0.008 6,000 Total # of individuals

Species richness

30

20

10

5,000 4,000 3,000 2,000 1,000

0

0 Unburned Burned Management type

Unburned Burned Management type

Fig. 2. Box–plot diagram of the response of species richness and abundance to management type on all sampled sites.

Fig. 2. Diagrama de la respuesta en riqueza y abundancia de especies al tipo de actuación desarrollado en todas las áreas estudiadas.

frequency. This null expectation was calculated by assigning 88% of all encountered individuals to unburned sites, with the remaining 22% to burned sites. This procedure was necessary as the number of unburned vs. burned sites was not balanced (88% vs. 22%). A two–tailed significance threshold was employed so that species with positive and negative responses to fire could both be identified. As these analyses were repeated for each species, a Bonferroni correction was used to adjust the significance threshold. Differences between fire responses across the three general ecological preference types were documented via a contingency table, with significance being estimated using both log–linear modelling and Fisher’s Exact test.

Results These grassland habitats were generally found to support a diverse and abundant land snail fauna. A total of 91,074 individuals in 72 different species were recovered from the 72 surveyed sites (tables 1, 2). The number of species per each 4 l litter sample ranged from two (Chicog gravel prairie) to 24 (Twin Pines Farm sandstone glade). Average richness ranged from roughly 15 in upland sites, to 17 in lowland. Snail abundance per site ranged from 6 (Point Beach State Forest dunes) to 5,001 (Ogema West fen). Average abundance ranged from roughly 500 in upland sites to 2,000 in lowlands.

One–way ANOVA, using all sites, demonstrated that both species richness (p = 0.001) and abundance (p = 0.008) were significantly lower on sites that had experienced fire management (fig. 2). Median species richness was approximately 18 on unburned vs. 12 on burned sites. Likewise, median shell abundance was 1,000 on unburned vs. 300 on burned sites.

Full 2–way ANOVA, using all sites and considering both management type and habitat type (upland vs. lowland) as independent variables, demonstrated a highly significant (p = 0.002) reduction (approximately 30%) in species richness in both upland and lowland sites (fig. 3). Habitat type and the interaction between habitat and fire history were not significant predictors (p = 0.209 and p = 0.628, respectively).

Likewise, a significant (p = 0.010) reduction in shell abundance (50–70%) was noted on burned sites (fig. 3). In this case, however, habitat type was a more significant (p < 0.0005) predictor, with lowlands having 4–10 times the number of shells as uplands. Additionally, a marginally significant (p = 0.088) interaction between management and habitat was observed, with the reduction appearing to be roughly 50% greater in lowlands.

Two–way ANOVA restricted to the 26 paired sites (fig. 4) demonstrated that even after blocking of variation due to site pair identity, a significant reduction in richness (p < 0.0005) and abundance (p = 0.015) still occurred on fire– managed sites.

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62

Lowland sites

Upland sites

Species richness

30

20

10

0 ANOV ANOVA A results:

fire p = 0.002 habitat p = 0.209 interaction p = 0.628

Total # of individuals

6,000 5,000 4,000 3,000 2,000 1,000 0

Unburned Burned Management type ANOV A results: ANOVA

Unburned Burned Management type fire p = 0.010 habitat p < 0.0006 interaction p = 0.088

Fig. 3. Box–plot diagram of the response of species richness and abundance to management and habitat type on all sampled sites.

Fig. 3. Diagrama de la respuesta en riqueza y abundancia de especies al tipo de actuación desarrollado y el hábitat en todas las áreas estudiadas.

Comparison of dominance–diversity diagrams for these sites (fig. 5) demonstrates that both burned upland and lowland sites have truncated curves, with the rarest 40–50% of species being much less common as compared to unburned sites. However, the more common species appear to have largely similar dominance–diversity diagrams.

Contingency table analysis of individual species responses to fire (table 2) indicate that 32 (44%) experience a significant reduction in abundance on fire–managed sites, even following use of a Bonferroni–corrected two–tailed significance threshold (p = 0.000347). Only six species (8%) demonstrated positive responses to fire, while the remaining 34 (47%) demonstrated no

63

Animal Biodiversity and Conservation 25.2 (2002)

6,000

Total # of individuals

Species richness

30

20

10

0

5,000 4,000 2,000 3,000 1,000 0

Unburned Burned Management type

Unburned Burned Management type

ANOV A results: ANOVA Pairs p = 0.001 Fire p < 0.0005

ANOV A results: ANOVA Pairs p = 0.009 Fire p = 0.015

Fig. 4. Box–plot diagram of the response of species richness and abundance to management on 26 sites paired by habitat type and geographic location.

Fig. 4. Diagrama de la respuesta en riqueza y abundancia de especies a la actuación desarrollada en 26 áreas emparejadas según el tipo de hábitat y localización geográfica.

Lowland sites

Upland sites

ln (% frecuency)

–1

–4

–7

–10

0

10

20 30 40 Rank order

50

60

0

10

20 30 40 Rank order

50

60

Burned Unburned

Fig. 5. Dominance–diversity curve for upland/lowland sites which have been burned/unburned.

Fig. 5. Curva de la dominancia–diversidad para las mesetas/llanuras que hayan sido quemadas/ no quemadas.

Nekola

64

significant changes in population size. Contingency table analysis of ecological preference vs. fire response indicated that fully 72% of turf– specialists were negatively impacted by fire (table 3). However, only 22% of duff–specialists exhibited negative responses. While 67% of duff– specialists demonstrated no significant response to fire only 24% of turf–specialists were unaffected. Generalist species demonstrated little discernable trend to fire, with seven decreasing, two increasing, and five with no response. Log– likelihood ratio and Fisher’s Exact tests both indicated these differences as being highly significant (p = 0.0006 and p = 0.004, respectively).

Table 3. Contingency table analysis of fire response vs. general ecological preferences.

Log–likelihood ratio p = 0.000634; Fisher’s Exact Test p = 0.004 (Ecological preferences: T. Turf; D. Duff; G. Generalist.)

Tabla 3. Análisis de la tabla de contingencia de la respuesta al fuego frente a las preferencias ecológicas generales. Logaritmo de la razón de verosimilitudes p = 0,000634; Test exacto de Fisher p = 0,004 (Preferencias ecológicas: T. Sustrato herbáceo; D. Sustrato húmico; G. Generalista.)

Discussion These data clearly indicate that fire management causes significant reductions in land snail community richness and abundance in both upland and lowland grasslands throughout a significant section of the tallgrass prairie biome in central North America. At a species–level, fire most strongly impacts the rarest species, and causes significant population reductions in 44% of the 72 encountered taxa. These negative impacts were most strongly felt in turf–specialists, where almost 75% experienced significant reductions. Thus, statements regarding the benign nature of fire on snail populations (FREST & JOHANNES, 1995), and the beneficial impact of fire on North American grassland faunas (THELER, 1997) can be proven false. Rather, frequent use of fire management appears to represent a significant threat to the health and diversity of North American grassland land snails.

It is not possible through these analyses to definitively identify the factors that directly lead to these impacts. However, at least part of the answer must lay in grassland detritusphere removal. This will lead to direct mortality, as the great majority of land snails are limited to this layer (H AWKINS et al., 1998). As land snail abundance (BERRY, 1973), diversity (CAIN, 1983; L OCASCIULLI & BOAG , 1987), and composition (CAMERON & MORGAN–HUWS, 1975; BAUER et al., 1996; BARKER & MAYHILL, 1999) is often positively correlated with litter depth, detritusphere removal would be expected to have a strong negative impact on land snail community structure.

Redevelopment of an equilibrium thickness of organic detritus takes at least five years in southern Plains grasslands (KUCERA & KOELLING, 1964), with even longer intervals being required in more northern locations (HILL & PLATT, 1975).

The optimal interval between fires for land snails might be even longer, depending upon the time required for more refractory plant debris (such as lignified grass stems) to break down, allowing a complete suite of decompositional microhabitats to develop. Litter architecture is known to effect snail community composition in forests of Virginia

Ecological preferences Fire response

T

D

G

18

6

7

None

6

18

5

Positive

1

3

2

Negative

(BURCH, 1956), British Columbia (CAMERON, 1986), and Puerto Rico (ÁLVAREZ & WILLIG, 1993) and grasslands of England (YOUNG & EVANS, 1991). It should thus not be surprising that in the current data set, sites burned up to 15 years ago have maintained lowered land snail richness and abundance as compared to unburned sites.

As grassland land snails presumably evolved in conjunction with natural fire regimes, it is also intriguing to note that turf–specialists experienced the most severe negative impacts to fire. If fire was a common process structuring central North American grasslands, evolution should have selected for individuals that were more tolerant of, or favored by, this disturbance. Like other native grassland invertebrate groups (SWENGEL, 1996; HARPER et al., 2000), land snails in the presettlement landscape may have been able to tolerate fires by being able to easily recolonize from source pools in adjacent unburned areas. Even when such adjacent source pools are present, recolonization may take over a dozen years (MÄND et al., 2001). In modern landscapes, where grasslands are highly fragmented and surrounded by agricultural, urban, or forest habitats, such recolonization has become much more difficult. Thus, turf–specialist taxa may continue to decrease in burned grasslands due to a lack of recolonization sources, while generalist and duff-specialist woodland taxa, which are more common in the surrounding landscape, may be able to maintain their populations through mass effect (SHMIDA & ELLNER, 1984).

The depression of land snail richness and abundance following fire episodes, the length of time required to redevelop a mature detritusphere, and the greater sensitivity of turf– specialist taxa to fire casts doubt on the wide–

Animal Biodiversity and Conservation 25.2 (2002)

held belief (e.g., PAULY, 1985) that North American grasslands should be burned at 2–6 year intervals.

Rather, these data support the contention that presettlement return intervals ranged between 20–30 years (SIMS, 1988). These data also strongly suggest that other factors, such as large herbivore grazing (COLLINS et al., 1998) and periodic drought (BORCHERT, 1950), may have also played essential roles in keeping prairies treeless, as these processes do not lead to the wholesale detritusphere removal.

Protecting the health of North American grassland land snail populations will require the preservation of mulch layers on sites. Such efforts will also help protect a large percentage of the entire grassland soil biota. The detritusphere can only be protected if more realistic fire return intervals (20–30 years) are adopted by conservation agencies, and used in conjunction with more diversified approaches towards woody and invasive plant removal. Activities like grazing, haying, and hand cutting/pulling will not cause widespread removal of the detritusphere, and should thus be more compatible with land snail (and soil biodiversity) conservation.

Acknowledgements Alyssa Barnes, Tracy Kuklinski, J. J. Schiefelbein and Angela Sette helped processed many soil litter samples, and assisted in shell counting.

Additional assistance in litter processing was also provided by students of the Land Snail Ecology Practicum at the University of Wisconsin – Green Bay. Funding was provided by the Minnesota Nongame Wildlife Tax Checkoff and Minnesota State Park Nature Store Sales through the Minnesota Department of Natural Resources Natural Heritage and Nongame Research Program.

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Genetic structure of two pseudoscorpion species living in tree hollows in Sweden T. Ranius* & P. Douwes

Ranius, T. & Douwes, P., 2002. Genetic structure of two pseudoscorpion species living in tree hollows in Sweden. Animal Biodiversity and Conservation, 25.2: 67–74.

Abstract Genetic structure of two pseudoscorpion species living in tree hollows in Sweden.— Two saproxylic pseudoscorpions, Larca lata and Allochernes wideri, were compared in an analysis of genetic structure in southern Sweden. Allochernes wideri is a relatively widely distributed species that occurs in single–standing trees and in small tree hollows, while L. lata is on the Swedish red list and confined to larger assemblages of very old trees with hollows containing large amounts of wood mould. In A. wideri, the polymorphism of PGM was used, whereas in L. lata the variation for PGI was studied.

The genetic differentiation between trees within a site was low for both species, indicating that the migration between nearby trees is considerable despite the fact that phoretic dispersal has only been occasionally observed in these species.

Between sites, situated four to 900 km from each other, the genetic differentiation was small both in A. wideri and L. lata with no difference between the species, when considered on the mainland only. The small differentiation suggests the habitat was fragmented recently (100–170 years ago). The relation between the rate of migration and long–term population survival and the risk of mis–interpretation due to selection for alleles is discussed.

Key words: Allochernes wideri, Allozymes, Dispersal, Habitat fragmentation, Larca lata, Phoresy.

Resumen Estructura genética de dos especies de pseudoescorpión que viven en los huecos de árboles en Suecia.— Se comparan dos pseudoescorpiones saproxílicos, Larca lata y Allochernes wideri, del sur de Suecia mediante un análisis de su estructura genética. Allochernes wideri es una especie de distribución relativamente amplia que se encuentra en árboles aislados y en pequeños huecos de árboles, mientras que L. lata aparece en la lista roja sueca y se encuentra confinado en grandes agrupaciones de árboles muy viejos cuyos huecos contienen gran cantidad de moho. En A. wideri se empleó el polimorfismo de PGM mientras que en L. lata se estudió la variación por PGI. La diferenciación genética entre árboles de un mismo lugar fue baja para ambas especies, indicando que la migración entre árboles cercanos es considerable aun cuando sólo se observó dispersión forética ocasionalmente en ambas especies. Entre zonas situadas a una distancia de 4 a 900 km, la diferenciación genética fue escasa en ambas especies, A. wideri y L. Lata, sin ninguna diferencia entre las mismas cuando se consideró únicamente la zona principal. Esta pequeña diferenciación sugiere que el hábitat se fragmentó recientemente (100–700 años antes). Se discute la relación entre la tasa de migración y la supervivencia de la población a largo plazo y el riesgo de una mala interpretación debida a la selección de los alelos.

Palabras clave: Allochernes wideri, Aloenzimas, Dispersión, Fragmentación del hábitat, Larca lata, Foresis.

(Received: 4 IV 02; Conditional acceptance: 6 VI 02; Final acceptance: 26 VII 02) Thomas Ranius & Per Douwes, Lund Univ., Dept. of Zoology, Helgonav. 3, SE–223 62 Lund, Sweden. * New address for corresponding author: Thomas Ranius, Swedish Univ. of Agricultural Sciences, Dept. of Entomology, P. O. Box 7044, SE–750 07 Uppsala, Sweden.

E–mail: thomas.ranius@entom.slu.se

ISSN: 1578–665X

© 2002 Museu de Ciències Naturals

Ranius & Douwes

68

Introduction Most species are associated with a habitat that is more or less patchy, resulting in a population structure with areas of high abundances separated by areas in which the species is rare or absent. In the last few centuries, human activities have caused many habitats to become subdivided into patches which are much smaller and more isolated than in the primaeval landscape (e.g. ANGELSTAM, 1992; HARRISON & FAHRIG, 1995). Especially for those species that have evolved in a spatially more continuous habitat, fragmentation into smaller, isolated populations may increase susceptibility to extinction both for genetic and demographic reasons (NILSSON & ERICSON, 1997).

Genetic differentiation measurements might provide an understanding of the population structure and migration, which are important in conservation work (STACEY et al., 1997). The impact of decreased habitat patch size and increased isolation on population genetics have, among invertebrates, mainly been studies on butterflies and moths (e.g. VAN DONGEN et al., 1998; HOOLE et al., 1999; MEGLÉCZ et al., 1999; CLARKE & O’DWYER, 2000; FIGURNY–PUCHALSKA et al., 2000), while other taxa have been less studied (see however VOGLER et al., 1993; KNUTSEN et al., 2000; JONSSON, 2002 on beetles).

The present study considers the genetic differentiation in two pseudoscorpion species that are associated with tree hollows. One of the species, Larca lata H. J. Hansen (Pseudoscorpionida, Larcidae), is only found in larger assemblages of ancient, hollow oaks, whereas the other, Allochernes wideri C. L. Koch (Pseudoscorpionida, Chernetidae), has a broader habitat and occurs at more localities (RANIUS & WILANDER, 2000). Old oaks occur mainly in old–growth deciduous forests and pasture woodlands, and in Europe both these habitats have decreased severely in the last few centuries (HANNAH et al., 1995; KIRBY & WATKINS, 1998). In Sweden, the major decrease of old oaks occurred 100–170 years ago (ELIASSON & NILSSON, 1999). A rare and endangered saproxylic fauna, mainly consisting of beetles, flies and pseudoscorpions, is associated with tree hollows (SPEIGHT, 1989). It seems that only one genetic study on a rare saproxylic invertebrate has been performed (JONSSON, 2002) and that was not on a species associated with tree hollows. Tree hollows are expected to be a stable habitat, with narrow fluctuations in microclimate and nutrient supply.

In a living hollow tree, partly decomposed wood inside the trunk is surrounded by growing sound wood, resulting in a continuous nutrient supply for the saproxylic fauna. The daily microclimate fluctuation is much smaller in a trunk hollow than at the surface of the trunk (KELNER–PILLAULT, 1974; PARK & AUERBACH, 1954). This might cause inhabiting species to have narrow population fluctuations, which decrease their extinction rate in comparison with other invertebrate populations

of the same size (RANIUS, 2001). Therefore it is possible that these species have relictual distributions, with small, isolated populations surviving in small remnants over long periods after the habitat density has become too low to allow long–term metapopulation persistence (RANIUS, 2000).

Many pseudoscorpion species disperse phoretically, which means that they hitch–hike with other animals, usually insects. There is circumstantial evidence that both L. lata and A. wideri perform phoretic dispersal, but it is not known how frequent this behaviour is (RANIUS & WILANDER, 2000). As L. lata is confined to larger assemblages of hollow trees, whereas A. wideri occurs also in single trees far from other hollow trees, it has been suggested that L. lata has a more restricted colonization ability (RANIUS & WILANDER, 2000).

In this study, the degree of genetic differentiation was examined in order to estimate the extent of genetic drift and migration. Being the less abundant species and inhabiting a narrow ecological range L. lata was expected to have lower population sizes within a given area and lower frequency of migration, which would give rise to higher levels of genetic differentiation than for A. wideri.

Material and methods Sampling Sampling was designed to determine the degree of genetic differentiation at two geographic levels: 1.

Samples were taken from trees situated 100–700 m from each other in Bjärka–Säby (fig. 1). About 30 individuals of A. wideri were then sampled from each of three trees and individulas of L. lata from four trees. 2. Samples were taken from sites situated four to 900 km apart, all within southern Sweden (fig. 1). Allochernes wideri was sampled from ten, and L. lata from six sites (table 1 and 2). A total sample of about 30 individuals of each species was taken from one to five hollow trees at each site, except at Bjärka–Säby where larger samples were taken as all those at the tree level were pooled when used as a sample at the site level.

The sampling was carried out from 1995 to 1999. It was performed by sieving wood mould, and in the field the fine fraction was spread out on a white sheet where the pseudoscorpions were searched for. The pseudoscorpions were stored alive before transfer to a freezer.

Electrophoresis was performed within two years of sample collecting.

Electrophoresis Horizontal starch–gel electrophoresis was used to investigate allozyme variation. The electrophoresis technique used has been described by SELANDER et

69

Animal Biodiversity and Conservation 25.2 (2002)

1

2

3 4 5 6 7

8 9

Northern Europe 10 11 12

13

Fig. 1. Sampling sites in Sweden: M Sites where A. wideri samples have been taken; F Sites where L. lata samples have been taken; M Sites where both A. wideri and L. lata samples have been taken. Localities: 1. Strömsholm; 2. Kinnekulle; 3. Långvassudde; 4. Bjärka–Säby; 5. Grebo; 6. Tjärstad; 7. Kättilstad; 8. Djursö; 9. Sankt Anna; 10. Strömserum; 11. Halltorp; 12. Hallands Väderö; 13. Yddingen.

Fig. 1. Áreas de estudio de Suecia: M Áreas donde se tomaron muestras de A. wideri; F Áreas donde se tomaron muestras de L. lata; M Áreas donde se recogieron muestras de ambas A. wideri y L. lata. Localidades: 1. Strömsholm; 2. Kinnekulle; 3. Långvassudde; 4. Bjärka–Säby; 5. Grebo; 6. Tjärstad; 7. Kättilstad; 8. Djursö; 9. Sankt Anna; 10. Strömserum; 11. Halltorp; 12. Hallands Väderö; 13. Yddingen.

al. (1971). The loci of six enzymes were screened: (ME (malic enzyme), =–GPD (=–glucosephosphate dehydrogenase), MDH (malate dehydrogenase), PGI (phosphoglucose isomerase), PGM (phosphoglucomutase) and IDH (isocitrate dehydrogenase) in specimens from Bjärka–Säby of both species. ME, =–GPD and MDH had scorable activity in none or only a few individuals, and no variation was observed among scorable individuals. Therefore, these loci were not further used in this study. PGI, PGM and IDH had scorable activity in all individuals and were thus assessed in all samples. Sufficient material was normally obtained from each individual to load two starch gels, but some small nymphs did not give any visible bands. To control for possible between–gel artefacts, specimens from at least two sites were run in each gel.

Statistical analyses The statistical package POPGEN vers. 1.31 (by F. Yeh, R. Yang & T. Boyle) was used to calculate allele frequencies, expected and observed

heterozygosity and F–statistics.

Patterns of genetic structure were revealed through the analysis of allele frequencies using F–statistics (HEDRICK, 1983). The most commonly used statistic, Fst, is a measure of the extent to which subpopulations show spatial genetic heterogeneity. Fst values range from 0, suggesting lack of differentiation or panmixia, to 1, indicating fixation of alternate alleles and complete differentiation. Chi–square was used to test the significance of the allele frequency differences among populations: N2 = 2NFst(k – 1)

d.f. = (k – 1)(s – 1)

(BAKER, 1981; BILTON, 1992). N is the total number of individuals, k is the number of alleles for the locus and s is the number of subpopulations. The gene flow between trees within a site was estimated from F–statistics (HEDRICK, 1983): Fst = 1 / (4Nm + 1) where Nm is the average number of migrants

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between subpopulations per generation. This gene flow estimate is developed from an island model of population structure, with every subpopulation inhabiting an island equally accessible from every other, with a balance between genetic drift and migration. Although few populations actually conform to the assumption of this model it is useful as an approximation of the magnitude of gene flow, as dispersal has a strong correlation with the genetic structure in most populations (BOHONAK, 1999). The gene flow was not calculated at the site level, as the effects of genetic drift and migration were not considered to be in equilibrium there.

The genetic distance D (NEI, 1972) was calculated in both species at the site level for each pair of populations. The coefficient of correlation between D and the geographical distance was

calculated, and the statistical significance of the correlation was tested with a one–tailed Mantel test with 200 randomized values calculated (SOKAL & ROHLF, 1995).

Results In A. wideri only PGM was polymorphic, while in L. lata variation both in PGM and PGI was found.

However, in L. lata the heterozygotes of PGM did not segregate properly and it was therefore impossible to score the genotypes unambiguously.

It was therefore decided to omit this locus from further analysis. IDH was monomorphic throughout in both species and PGI was monomorphic in A. wideri.

At the PGM locus (A. wideri) four alleles were

Table 1. Allele frequencies at the PGM locus in populations of Allochernes wideri: Sample size. Number of individuals in the sample; Stand size. Roughly estimated number of hollow trees with wood mould; He Expected heterozygosity; Ho Observed heterozygosity; Frequency of alleles (Z. Very slow, S. Slow, M. Medium, F. Fast).

Tabla 1. Frecuencia de alelos en el locus PGM en una población de Allochernes wideri: Sample size. Número de individuos de la muestra; Stand size. Número estimado aproximado de huecos de árboles con moho de madera; He Heterocigosis esperada; Ho Heterocigosis observada; Frequencia de alelos (Z. Muy baja, S. Baja, M. Media, F. Alta).

A. Sites in southern Sweden situated 4–500 km from each other Frequency of alleles Locality

He

Ho

Z

S

M

Strömsholm

Sample size Stand size 26

100–200

0.50

0.58

0.00

0.56

0.44

0.00

F

Kinnekulle

27

50

0.48

0.48

0.00

0.33

0.65

0.02

Långvassudde

38

100–200

0.55

0.58

0.00

0.41

0.54

0.05

Bjärka–Säby

90

200

0.53

0.50

0.01

0.46

0.52

0.02

Tjärstad

29

1

0.61

0.52

0.03

0.19

0.57

0.21

Kättilstad

31

20

0.49

0.48

0.00

0.37

0.61

0.02

Sankt Anna

31

20–50

0.55

0.55

0.00

0.26

0.61

0.13

Strömserum

29

50–200

0.67

0.52

0.03

0.19

0.45

0.33

Halltorp

21

20

0.61

0.57

0.02

0.29

0.55

0.14

Yddingen

30

10–30

0.53

0.43

0.02

0.27

0.63

0.08

B. Trees within the Bjärka–Säby site, situated 100–300 m from each other 38

0.52

0.45

0.00

0.40

0.58

0.03

27

0.52

0.56

0.02

0.41

0.57

0.00

25

0.51

0.52

0.02

0.60

0.36

0.02

71

Animal Biodiversity and Conservation 25.2 (2002)

Table 2. Allele frequencies at the PGI locus in populations of Larca lata: Sample size. Number of individuals in the sample; Stand size. Roughly estimated number of hollow trees with wood mould; He Expected heterozygosity; Ho Observed heterozygosity; Frequency of alleles (S. Slow, M. Medium, F. Fast).

Tabla 2. Frecuencia de alelos en el locus PGI de una población de Larca lata: Sample size. Número de individuis de la muestra; Stand size. Número estimado aproximado de huecos de árboles con moho de madera; He Heterocigosis esperada; Ho Heterocigosis observada; Frequencia de alelos (S. Baja, M. Media, F. Alta).

A. Sites in Sweden, situated 7–500 km from each other Frequency of alleles Locality

Sample size

Stand size

He

Ho

S

M

F

Strömsholm

44

100–200

0.57

0.68

0.55

0.35

0.10

Bjärka–Säby

129

200

0.60

0.61

0.37

0.50

0.13

Grebo

49

130

0.62

0.57

0.52

0.28

0.20

Djursö

38

80

0.59

0.58

0.50

0.40

0.10

Strömserum

29

50–200

0.52

0.55

0.60

0.35

0.05

Hallands Väderö

27

50–100

0.33

0.19

0.80

0.00

0.20

B. Trees within the Bjärka–Säby site, 100–700 m from each other 36

0.48

0.50

0.39

0.61

0.00

30

0.65

0.77

0.35

0.43

0.22

30

0.60

0.57

0.38

0.50

0.12

33

0.64

0.63

0.35

0.45

0.20

found, one of which (Z) occurred in very low frequencies (< 5%, table 1). The three alleles at the PGI locus (L. lata) appeared in almost all samples except the rather frequent M allele, which was not found at Hallands Väderö (table 2).

The Ho did not deviate from Hardy–Weinberg equilibrium (table 2) when it was tested by N2 for each population (p > 0.05). This suggests that the samples were taken from fairly panmictic populations. The genetic differentiation between the populations (Fst) at sites was low in A. wideri and moderate in L. lata (table 3). However, without the Hallands Väderö population, the Fst in L. lata was considerably lower (Fst = 0.0241), yet still significantly above zero. The genetic differentiation between trees was low but significant in A. wideri, whereas in L. lata Fst did not deviate significantly from zero (table 3).

In A. wideri , there was no significant correlation between Nei’s genetic distance D and the geographic distance between sites (r = 0.03), as 19.5% of the correlation coefficients

Table 3. F st for four separate sets of samples: G. Geographic level; Np. Number of populations; Na. Number of alleles; ns.

Not significant; ** p < 0.01; *** p < 0.001.

Tabla 3. F st para cuatro grupos de muestras separadas: G. Nivel geográfico; Np. Número de poblaciones; Na. Número de alelos; ns. No significativo; ** p < 0,01; *** p < 0,001.

Species

A. wideri L. lata

G

Np

Na

Fst

Trees

3

4

0.0369**

Sites

10

4

0.0481***

Trees

4

3

0.0206 ns

Sites

6

3

0.0761***

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resulting from the Mantel test randomizations were higher than the observed correlation coefficient. In L. lata, the correlation between Nei’s genetic distance D and the geographical distance between sites was positive (r = 0.49) and statistically significant (3.5% of the correlation coefficients resulting from the Mantel test randomizations were higher than the observed correlation coefficients). The signficant relation arose because Hallands Väderö was geographically the most isolated site, and its population was the genetically most deviant. Without Hallands Väderö, no significant relation was found (r = – 0.48, 92.5% of the correlation coefficients from the Mantel randomizations were higher than the observed correlation coefficient.

The gene flow between trees in Bjärka–Säby was estimated from F–statistics (HEDRICK, 1983): Fst = 1 / (4Nm + 1)

Nm (the average number of migrants between trees per generation) was estimated to seven individuals for A. wideri and twelve for L. lata.

Discussion The small genetic differentiation between sites was not unexpected as until 150–200 years ago, old hollow oaks were a widespread habitat, probably occurring contiguously over large areas of southern Sweden (ELIASSON & NILSSON, 1999).

The generation time of the study species is unknown, but for other pseudoscorpion species the life time is 2–5 years (WEYGOLDT, 1969; GÄRDENFORS & WILANDER, 1992). Thus, the reduction in connectivity and population sizes should not yet be fully manifested in the genetic variation between sites, as fragmentation of the habitat has occurred within the last 100 generations of the pseudoscorpions and the population size per site may be relatively large. Many threatened invertebrates would be expected to show patterns similar to L. lata in this respect; they suffer from habitat fragmentation and become extinct from small sites (RANIUS & WILANDER, 2000). However, because the local populations are often still relatively large it is difficult to detect genetic effects of fragmentation before the population has disappeared for other reasons.

In L. lata, the genetic differentiation was larger than in A. wideri only when the Hallands Väderö population was included in the analysis. Also the correlation between genetic and geographic distances between sites was dependent on that the Hallands Väderö population was included.

This indicates that in L. lata the gene flow between Hallands Väderö, which is on an island, and the mainland might have been low or absent over a longer period than between the mainland populations. Thus, the larger differentiation between all sites in L. lata compared to A. wideri

does not suggest any difference in the migration rate between mainland populations.

Within the Bjärka–Säby site, the conditions would not be expected to have changed much over the past 150 years. Under the assumption that there is no selection that affects gene frequencies, the observed genetic variation between trees should therefore reflect the ongoing genetic drift, migration and extinction–colonization process. The extinction– recolonization turnover, which might take place in hollow trees within a stand, results in imprecise correlations between Fst and Nm, and most cases yielding too low estimates of Nm (WADE & MCCAULEY, 1988). In spite of this, the estimated migration rate was fairly high both in L. lata and A. wideri (12 and 7 tree-1 year-1, respectively). From observations in the field the population size was estimated as being five to 500 individuals per tree, and the mean might be 50 individuals per occupied tree for both species (calculated from the field data set used in RANIUS & WILANDER, 2000). The relatively frequent migrations that seem to occur in both species are almost certainly performed by phoresy, even though it has infrequently been observed for these species.

As there is a positive relation between occupancy per tree and stand size in L. lata, it has been hypothesized that the L. lata populations in stands conform to metapopulations, with each tree possibly sustaining a local population (RANIUS & WILANDER, 2000). The results from the present study suggest that the migration rate might be too high for metapopulation dynamics to be important at this scale, but as the estimates are very rough this hypothesis can not be rejected.

The underlying assumption of the Fst calculation is that there is no selection for any alleles. If selection maintains different alleles in high frequencies in different local populations, the Fst estimation indicates little or no gene flow even if it is actually large. Selection for heterozygosity, however, may generate similar gene frequencies for many local poulations and the Fst calculation then suggests a gene flow larger than reality. The loci used in this study are for two metabolically adjacent enzymes, PGI (phosphoglucose isomerase) and PGM (phosphoglocosemutase). Both these loci have been found to experience natural selection in studies on butterflies (PGM: GOULSON, 1993; PGI: CARTER & WATT, 1988, indications of selection in both: CARTER et al., 1989). Also in a beetle, Chrysomela aenicollis, natural selection probably acts on PGI (RANK, 1992). A further genetic study based on a larger number of loci would therefore be interesting to control possible effects of selection, chance or history which may act on individual alleles in the pseudoscorpion species.

Acknowledgements We thank Mattias Jonsson and Sven G. Nilsson for their valuable comments on the manuscript and Per Wilander for help with the species

Animal Biodiversity and Conservation 25.2 (2002)

identification. This study was financially supported

by Larsénska fonden, Kungliga Fysiografiska Sällskapet i Lund and Hierta–Retzius stipendiefond (Kungliga Vetenskapsakademien).

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New solutions to old problems: widespread taxa, redundant distributions and missing areas in event–based biogeography I. Sanmartín* & F. Ronquist

Sanmartín, I. & Ronquist, F., 2002. New solutions to old problems: widespread taxa, redundant distributions and missing areas in event–based biogeography. Animal Biodiversity and Conservation, 25.2: 75–93.

Abstract New solutions to old problems: widespread taxa, redundant distributions and missing areas in event–based biogeography.— Area cladograms are widely used in historical biogeography to summarize area relationships.

Constructing such cladograms is complicated by the existence of widespread taxa (terminal taxa distributed in more than one area), redundant distributions (areas harboring more than one taxon) and missing areas (areas of interest absent from some of the compared cladograms). These problems have traditionally been dealt with using Assumptions 0, 1, and 2, but the assumptions are inapplicable to event–based methods of biogeographic analysis because they do not specify the costs of alternative solutions and may result in non–overlapping solution sets. The present paper presents the argument that only widespread terminals pose a problem to event–based methods, and three possible solutions are described. Under the recent option, the widespread distribution is assumed to be the result of recent dispersal. The ancient option assumes that the widespread distribution is the result of a failure to vicariate, and explains any mismatch between the distribution and the area cladogram by extinction. The free option treats the widespread taxon as an unresolved higher taxon consisting of one lineage occurring in each area, and permits any combination of events and any resolution of the terminal polytomy in explaining the widespread distribution. Algorithms implementing these options are described and applied to Rosen (1978)’s classical data set on Heterandria and Xiphophorus.

Key words:: Historical biogeography, Widespread taxa, Missing areas, Redundant distributions, Assumptions 0, 1, and 2.

Resumen Nuevas soluciones a viejos problemas: taxones de amplia distribución, distribuciones redundantes y áreas ausentes en la biogeografía cladista de procesos.— El análisis biogeográfico cladista se basa en la comparación de cladogramas de áreas de organismos que habitan una misma región (sustituyendo el nombre de los taxones en la filogenia por las áreas que éstos ocupan) para obtener un patrón común, el cladograma general de áreas.

La construcción del cladograma de áreas se complica cuando existen taxones presentes en más de un área de distribución (“taxones de amplia distribución”), áreas que albergan más de un taxón (“distribuciones redundantes”), o áreas que no están presentes en alguno de los grupos (“áreas ausentes”). En biogeografía cladista de procesos, los taxones de amplia distribución se resuelven aplicando las Asunciones: 0, 1, y 2, que difieren en la relación cladogenética permitida entre las áreas donde se distribuye el taxon. Se proponen tres nuevas soluciones para abordar este problema dentro de un nuevo enfoque en biogeografía cladista que incorpora los procesos al análisis biogeográfico: “biogeografía cladista de procesos”. Estas opciones difieren no sólo en las relaciones entre las áreas implicadas sino también en los procesos biogeográficos que pudieron haber dado lugar a la distribución. La opción recent considera la amplia distribución como si fuera de origen reciente y la explica por dispersión. La opción ancient considera que la amplia distribución es ancestral y la explica mediante vicarianza y extinción. La opción free considera la amplia distribución como un taxón de alto rango con un linaje en cada una de las áreas implicadas y cuyas relaciones no han sido establecidas, permitiendo cualquier combinación de procesos biogeográficos y cualquier solución de la politomía para explicar la distribución. Se comparan estas opciones utilizando el famoso análisis de Rosen (1978) sobre Heterandria y Xiphophorus. También se discute brevemente como tratar las distribuciones redundantes y las áreas ausentes dentro de este nuevo enfoque.

ISSN: 1578–665X

© 2002 Museu de Ciències Naturals

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Palabras clave: Biogeografía histórica, Taxones de amplia distribución, Áreas ausentes, Distribuciones redundantes, Asunciónes 0, 1 y 2.

(Received: 11 I 02; Conditional acceptance: 25 IV 02; Final acceptance: 6 VI 02) Isabel Sanmartín & Fredrik Ronquist, Dept. of Systematic Zoology, Evolutionary Biology Centre, Uppsala Univ., Norbyvägen 18D, SE–752 36 Uppsala, Sweden. * Corresponding author: Isabel Sanmartin, Dept. of Systematic Zoology, Evolutionary Biology Centre, Uppsala Univ., Norbyvägen 18D, SE–752 36 Uppsala, Sweden.

E–mail: isabel.sanmartin@ebc.uu.se

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Introduction Cladistic biogeography seeks to summarize information on distribution and phylogenetic relationships of organisms in area cladograms, branching diagrams that express the inter– relationships of areas based on their biotas (fig. 1a). The analysis usually starts with taxon– area cladograms (TAC) (ENGHOFF, 1993; MORRONE & CRISCI, 1995), which are constructed by replacing the terminal taxa in a phylogeny with the areas in which they occur. Comparing area cladograms of different organisms that occur in the same region may reveal common biogeographic patterns that can be represented in a general area cladogram (GAC).

If every terminal taxon is endemic to a unique area and every area harbors only one terminal taxon, the TAC represents a valid hypothesis about area relationships. However, the situation becomes more complicated when the “one–area– one–taxon” assumption is violated, in which case the TAC may be incomplete or indicate conflicting area relationships. The sources of these problems are often divided into three categories: widespread taxa (taxa present in more than one area, fig. 1b), redundant distributions (areas harboring more than one taxon, fig. 1c), and missing areas (areas of interest absent from some of the compared taxon–area cladograms, fig. 1d).

The latter problem is only relevant when several TACs are analyzed simultaneously.

Problematic TACs can be converted into resolved area cladograms (RACs; that is, taxon– specific GACs), in which each area is represented by only one terminal (E NGHOFF , 1996), by applying Assumptions 0, 1, and 2 (fig. 2). These assumptions mainly differ in their treatment of widespread taxa. Assumption 0 (A0, ZANDEE & ROOS, 1987) regards the widespread distribution as the result of a failure to speciate in response to vicariance events affecting other lineages.

The areas inhabited by the widespread taxon are considered to form a monophyletic clade (fig. 2: RAC1) and the widespread taxon is thus treated as a synapomorphy of the areas in which it occurs. Assumption 1 (A1, NELSON & PLATNICK, 1981) explains the widespread distribution as the result of a failure to vicariate, possibly in combination with subsequent extinction. The areas inhabited by the widespread taxon are considered to form a monophyletic or paraphyletic group of areas (fig. 2: RACs 1–3) and the widespread taxon is treated as a symplesiomorphy of areas. Assumption 2 (A2, NELSON & PLATNICK, 1981), finally, allows failure to vicariate, extinction, dispersal, or any combination of these events, in explaining the origin of widespread distributions (V AN V ELLER et al., 1999). The areas inhabited by the widespread taxon are regarded as constituting a poly–, para– or monophyletic group of areas (fig. 2: RACs 1–7), and the widespread taxon is treated as a possible

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convergence of the areas. In practice, A2 is implemented by locking each of the areas inhabited by the widespread taxon in turn, while the other areas are allowed to “float” on the RAC (ENGHOFF, 1995; MORRONE & CRISCI, 1995).

The solutions allowed under the three assumptions form inclusive sets (PAGE, 1990; VAN VELLER et al., 1999): the A0 solutions are a subset of the A1 solutions, and these in turn are a subset of the A2 solutions (fig. 2). Usually, there are also solutions that violate all three assumptions, namely those in which none of the areas of a widespread taxon occurs in the RAC in the position predicted by the place of the widespread taxon in the TAC (fig. 2: RACs 8–15).

Thus, the A2 solutions are usually a small subset of the “Full Solution Set” (all possible branching arrangements of the studied areas).

Redundant distributions (sympatric taxa) are essentially handled in the same way as widespread distributions. Under A0 and A1, each occurrence of the redundant area is considered as equally valid, i.e., as representing duplicated area patterns. A2 also considers the possibility that the redundant distributions are the result of dispersal, that is, each occurrence of the redundant distribution is considered separately (ENGHOFF, 1995). Missing areas are treated as missing data under A1 and A2, and explained by primitive absence (the taxon has never been in the area), extinction (the taxon went extinct in the area) or inadequate sampling. Under A0, missing areas are considered as observations of true absence and explained as due to primitive absence or extinction (ENGHOFF, 1995; MORRONE & CRISCI, 1995).

Application of these assumptions to empirical data has been controversial, as results can differ greatly when the same data set is processed under different assumptions (M ORRONE & CARPENTER, 1994; ENGHOFF, 1995; DE JONG, 1998; VAN VELLER et al., 2000). A0 (and A1) has been criticized as being too restrictive and unrealistic because it does not consider the possibility of dispersal in explaining widespread distributions, which means that areas may be grouped together solely based on recent range expansion involving geographically adjacent areas (NELSON & PLATNICK, 1981; HUMPHRIES & PARENTI, 1986; PAGE, 1989, 1990; MORRONE & CARPENTER, 1994).

A2, on the other hand, has been considered as uninformative or indecisive in that it allows many more solutions than the stricter A0 and A1, and therefore often gives a less resolved result (ENGHOFF, 1995; VAN VELLER et al., 1999). It has also been argued that A2 (and A1) distort the historical (phylogenetic) relationships established in the original taxon cladogram from which the area cladogram is derived (ZANDEE & ROOS, 1987; WILEY, 1988; ENGHOFF, 1996; VAN VELLER et al., 1999, 2000) but this claim seems to arise from a confusion on the meaning of the assumptions: A2 and A1 are interpretations of

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Fig. 1. a. Steps of a cladistic biogeographic analysis: a taxon–area cladogram (TAC) is constructed by replacing the taxa in the phylogeny with the areas in which they occur. Comparing the taxon– area cladograms for different groups reveals the existence of a general biogeographic pattern (GAC). Conflicting area relationships (incongruence) may be indicated by the TAC if this includes: b. Widespread taxa; c. Redundant distributions; d. Missing areas.

Fig. 1. a. Un análisis biogeográfico cladista comprende dos pasos: construcción del cladograma de áreas (TAC) sustituyendo el nombre de los taxones en la filogenia por el área que ocupan y derivación del cladograma general de áreas (GAC). El cladograma de áreas puede indicar relaciones conflictivas entre las áreas si existen: b. Taxones de amplia distribución; c. Distribuciones redundantes; d. Áreas ausentes.

the relationships between areas, not between taxa (PAGE, 1989, 1990).

The problems of widespread taxa, redundancy, and missing areas have mainly been discussed within the traditional pattern–based approach to historical biogeography. Pattern–based methods search for general patterns of area relationships (general area cladograms) allegedly without making any assumptions about evolutionary processes (R ONQUIST , 1997; 1998a).

Biogeographic processes, such as dispersal or extinction, are only considered a posteriori (or using ad hoc procedures) in interpreting incongruence between the general area cladogram and the taxon–area cladograms (WILEY, 1988; PAGE, 1994). However, several different combinations of events can usually explain each case of incongruence, leaving the choice of a specific set of events that could explain the observations to the investigator. Pattern–based methods may also give counter–intuitive results in some cases because they do not necessarily favor reconstructions implying likely events over those implying improbable events (RONQUIST, 1995).

Event–based methods, which are explicitly derived from models of biogeographic processes, have gained in popularity recently (RONQUIST & NYLIN, 1990; PAGE, 1995; RONQUIST, 1995, 1998a, 1998b). Unlike pattern–based methods, the event–based reconstructions directly specify the ancestral distributions and the biogeographic events responsible for those distributions, and no a posteriori interpretation is necessary. Each type of biogeographic event in the reconstruction is associated with a cost that should be inversely related to the likelihood of that event occurring in the past: the more likely the event, the lower the cost. The optimal biogeographic reconstruction is found by searching for the reconstruction that minimizes the total cost of the implied events (R ONQUIST, 1998a, 1998b, in press).

The purpose of this paper is to reexamine the problems of widespread taxa, redundant distributions and missing areas in the light of the event–based approach to historical biogeography.

We find that it is only widespread terminal distributions that cause problems in the event– based approach. Because the pattern–based A0,

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Assumption 0

Assumption 1

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Fig. 2. Taxon–area cladogram with a widespread taxon and three alternative methods of resolution under the pattern–based approach: Assumptions 0, 1, and 2 (A0, A1, and A2). Note that A2 excludes some solutions that are part of the “Full solution set” (all 15 possible rooted binary trees on 4 taxa). (Modified from MORRONE & CRISCI, 1995.)

Fig. 2. Aplicación de las asunciones 0, 1 y 2 (A0, A1 y A2) a la resolución de un cladograma de áreas con un taxón de amplia distribución. Obsérvese que A2 excluye algunas de las soluciones que son parte del “Full solution set” (los 15 posibles cladogramas dicotómicos para 4 áreas).

(Adaptado de MORRONE & CRISCI, 1995.)

A1 and A2 only define the set of allowed solutions but not the cost of each solution nor the implied events, they cannot be applied to event–based analyses. Instead, this paper describes three event– based options that may be used to reconcile the occurrence of widespread terminals with the

common assumption of each lineage being restricted to a single area at a time: the recent, ancient and free options. We give algorithms that implement these options and illustrate their properties by reexamining a classical biogeographic data set, that of ROSEN (1978).

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The event–based method Event–based biogeographic methods rely on explicit models with states (distributions) and transitions between states (biogeographic processes). The most commonly used model includes four different processes (PAGE, 1995): vicariance, duplication, extinction and dispersal.

Vicariance (v) is allopatric speciation in response to a general dispersal barrier (i.e., a barrier affecting many organisms simultaneously).

Duplication ( d ) is sympatric speciation or, alternatively, allopatric speciation due to idiosyncratic events such as a temporary dispersal barrier affecting only a single organism lineage.

Extinction (e) may simply mean that organisms become extinct in an area but it can also result from the organisms occupying only part of a large ancestral area and therefore being absent in one of the fragments resulting from division of this area. Dispersal (i) occurs when organisms colonize a new area separated from their original distribution by a dispersal barrier; this is assumed to be followed by allopatric speciation separating the lineages in the new and old areas.

Once each event type is associated with a cost, the cost of fitting a TAC to a particular GAC can be found by simply summing over the implied events. The GAC with the lowest cost, the most parsimonious GAC, is that which best explains the taxon distributions in the TAC. This optimal GAC can be found, for instance, by explicit enumeration of all possible GACs or by heuristic search for the best GAC. Because inference is based on cost minimization, this approach may be referred to as parsimony–based tree fitting. Similar methods are applicable to problems in coevolutionary inference and in gene tree–species tree fitting (RONQUIST, 1995, 1998a; PAGE & CHARLESTON, 1998).

An important problem in event-based methods is to find the cost for each type of biogeographic process. The most common approach is to work with simple event–cost assignments that focus on one or two of the events and ignore the others (RONQUIST & NYLIN, 1990; RONQUIST, 1995).

An example of this is Maximum vicariance (or Maximum cospeciation; PAGE, 1995; RONQUIST, 1998a, 1998b), in which vicariance events are maximized by associating them with a negative cost (a “benefit”, v = – 1), whereas the other events are not considered in the calculations (duplication (d) = extinction ( e ) = dispersal (i) = 0). The other approach is to set the cost assignments according to some optimality criterion. A reasonable optimality criterion is to maximize the likelihood of finding phylogenetically conserved distribution patterns (RONQUIST, 1998a, 1998b, in press). Assume that we test for conserved distribution patterns by randomly permuting the terminal taxa of the TAC and comparing the cost of the permuted

data sets with the cost of the original data set.

Examination of simulated and real data suggests that, in most cases, chances of finding conserved patterns are best when duplication and vicariance events carry a small cost relative to extinctions and dispersals (RONQUIST, in press).

This occurs because both vicariance and duplication are phylogenetically constrained processes, whereas dispersal and extinction are not. In practice, it is often found that the optimal solution is the same under a relatively wide range of event–cost assignments. In the examples discussed in this paper, the cost of vicariance (v) and duplication (d) events are arbitrarily set to 0.01; extinction events (e) to 1.0; and dispersal events (i) to 2.0.

A simple example may illustrate parsimony– based tree fitting in historical biogeography.

Consider a TAC with four terminals distributed in four areas (fig. 3a). Each possible GAC for the four areas (there are 15 in all) is fitted in turn to the TAC. For example, only three vicariance events are needed to fit the TAC to GAC1 (fig. 3b), whereas extra dispersal and extinction events must be postulated to explain the observed TAC on GAC2 and GAC3 (figs. 3c–d), and extra duplication and extinction events are needed for GAC4 (fig. 3e). Clearly, GAC1 will be the most parsimonious solution among those considered in figure 3 given the chosen event– cost assignments. Actually, GAC1 will remain optimal under a much wider range of cost assignments: as long as dispersals and extinctions cost more than vicariance events, the optimal solution will be the same. By explicitly enumerating all the 15 GACs and finding the cost of fitting each of them to the given TAC, it can also be demonstrated that GAC1 is the optimal solution.

The optimal reconstruction and the cost for any TAC–GAC combination can be found using fast dynamic programming algorithms (RONQUIST, 1998b). This means that a particular GAC can be fitted to a large set of TACs quickly. Nevertheless, searching for the best GAC using exhaustive algorithms is impractical for problems with more than around 10 areas, in which case heuristic algorithms or other types of exact algorithms should be used instead.

Widespread taxa Cladistic biogeography focuses on hierarchical (“branching”) patterns, in which a sequence of vicariance events successively divides a continuous ancestral area and its biota into smaller components (fig. 4a). This history is described by the GAC (fig. 4b). The terminal branches in the GAC correspond to present areas (A, B, C) and the internal branches to ancestral areas (E, D), which are combinations of present areas.

In event–based methods (and in pattern–based

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vicariance duplication extinction dispersal

Fig. 3. Example of a reconstruction of the distribution history of a group of organisms in event– based methods: a. A taxon–area cladogram (TAC) distributed in four areas; b–e. Biogeographic reconstruction in which the TAC is fitted in turn into four GACs with alternative resolutions of the relationships between the areas occupied by the TAC. Fitting is evaluated as the cost of the biogeographic events that must be postulated to explain the observed distributions in the TAC according to the GAC. Four types of events are considered in the reconstruction: vicariance, duplication (sympatric speciation), extinction, and dispersal.

Fig. 3. Cómo reconstruir la historia biogeográfica de un grupo de organismos incorporando los procesos en la reconstrucción biogeográfica (“biogeografía cladista de procesos”). a. Cladograma de áreas (TAC) distribuido en cuatro áreas; b–e. Reconstrucción biogeográfica en la que se muestra el grado de congruencia ("ajuste") entre el TAC y cuatro cladogramas generales de áreas (GAC), que difieren en la relación cladogenética entre las áreas que forman parte de la amplia distribución. El “ajuste” se evalúa como el coste de los procesos biogeográficos que deben asumirse para explicar la distribución de los taxones en el TAC de acuerdo con las relaciones entre áreas establecidas por el GAC (ver texto). Se consideran cuatro tipos de procesos biogeográficos: vicariancia, duplicación o especiación simpátrica, extinción y dispersión.

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Fig. 4. a. Hierarchical scenario illustrated as a sequence of vicariance events successively subdividing a continuous ancestral area into smaller components; b. The same scenario represented in the form of a tree–shaped diagram, the general area cladogram (GAC).

Fig. 4. a. Escenario biogeográfico jerárquico en el que sucesivos eventos de vicariancia dividen un área ancestral continua en fragmentos más pequeños; b. El mismo escenario, pero representado como un diagrama de árbol, el cladograma general de áreas (GAC).

methods), organism lineages are commonly assumed to be restricted to a single area at a time (for an exception see RONQUIST, 1997); that is, an ancestral distribution must be either a single present area or one of the ancestral areas (combinations of present areas) specified by the GAC. The one area–one lineage assumption makes parsimony–based tree fitting mathematically more tractable but it is also biologically sound: evolving lineages are not normally expected to maintain their coherence over long time periods across major dispersal barriers. However, the assumption causes problems with widespread terminals: how do we reconcile the observation of widespread terminals with the assumption of one area per lineage? The problem is analogous to that of treating polymorphic characters in standard parsimony analysis, in which ancestors are normally assumed to be monomorphic (MADDISON & MADDISON, 1992).

An obvious way of solving the dilemma is to assume that the widespread terminal is in reality not a homogeneous evolutionary lineage but an unresolved higher taxon consisting of a number of lineages, each occurring in a single area (fig. 5a). This does not necessarily imply that the widespread taxon actually comprises different species that have failed to be distinguished (HUMPHRIES & PARENTI, 1986; WILEY, 1988; ENGHOFF, 1996; ZANDEE & ROOS, 1987; VAN VELLER et al., 1999) but it suggests that the widespread distribution is a temporary condition. Now, assuming that the widespread taxon is a soft (unresolved) terminal polytomy with one lineage for each area occupied by the

taxon, we can obtain the minimum cost over all possible resolutions of the polytomy for each ancestral distribution at the base of the polytomy (the node marked with a black dot in the TAC, fig. 5a). For each possible ancestral distribution (i.e., each area in the GAC; fig. 5b), the terminal polytomy is resolved such that the cost of that distribution being ancestral is minimized (fig. 5c). This cost, in turn, is used in the subsequent fitting of the TAC to the GAC. The cost will depend on the GAC because the same ancestral distribution of a widespread taxon may have different costs on different GACs (see fig. 6, table 1).

In determining the possible ancestral distributions of the widespread taxon, we suggest three different options: the recent, ancient and free options. These options constrain the possible ancestral distributions of the widespread taxon in different ways, just like the traditional Assumptions A0, A1 and A2. However, unlike the traditional assumptions, the event–based options constrain the solutions by explicitly specifying the processes allowed in explaining the origin of the widespread distribution.

Furthermore, each allowed solution is associated with a specific set of events and a specific cost.

When many solutions are allowed, they often differ in cost such that they still convey useful information about the grouping of areas in the GAC. On continuation, the event–based options are described in more detail and compared with Assumptions 0, 1, and 2, both in terms of how they explain the widespread distribution (fig. 5) and how they affect the testing of alternative GACs (fig. 6).

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Fig. 5. Resolving the problem of widespread taxa under the event–based approach: a. Taxon area cladogram with a widespread taxon represented as a terminal polytomy of single–area lineages; b.

General area cladogram; c. The down–pass cost of each area in the GAC being the ancestral distribution of the widespread taxon (the state at the node marked with a black dot in the TAC) is found by resolving the terminal polytomy in congruence with area relationships in the GAC and then running a down–pass optimization in this subtree. The recent, ancient and free options allow various sets of possible ancestral distributions. The recent option only allows the GAC terminals occupied by the taxon (B, C and E); the ancient option only allows the immediate ancestor in the GAC of these areas (H), and the free option allows both these possibilities plus all intermediates between them (F and G).

(Symbols: – Areas not considered as possible ancestral distributions and associated with infinite cost; ( ) Areas that are allowed as ancestral distributions but that will never occur in optimal reconstructions because there will always be more parsimonious solutions; Abbreviations: d–duplication, e–extinction, i–dispersal, v–vicariance).

Fig. 5. Tratamiento de taxones de amplia distribución en “biogeografía cladista de procesos”: a.

Cladograma de áreas (TAC) con un taxón de amplia distribución representado como una politomía terminal formada por varios linajes, cada uno distribuido en un área; b. Cladograma general de áreas (GAC); c. Para calcular el coste de cada una de las áreas del GAC como posible distribución ancestral del taxón de amplia distribución (el estado ancestral en el nodo señalado con un punto negro en el TAC), se resuelve la politomía terminal de acuerdo con las relaciones entre áreas establecidas por el GAC, y luego se realiza una optimización del coste moviéndose desde los terminales hacia la raíz del subárbol. Las opciones recent, ancient y free permiten diferentes soluciones de las posibles distribuciones ancestrales. La opción recent sólo permite las áreas del GAC ocupadas por el taxón (B, C y E); la opción ancient sólo permite el área que representa el “ancestro común más reciente” de esas áreas en el GAC (H), mientras que la opción free permite cualquiera de estas posibilidades más todas las áreas intermedias entre ellas (F y G). (Para los símbolos y abreviaturas ver arriba).

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Recent option This option is applicable when the widespread distribution can be assumed to be of recent origin. One of the areas inhabited by the widespread taxon is considered the true ancestral area (the center of origin of the taxon) and the others are treated as if added by recent, independent dispersal.

The possible ancestral distributions of the widespread taxon are only those terminal areas occupied by the taxon (B, C, E in fig. 5b).

Regardless of whether we are using Maximum Vicariance or any other set of cost assignments is used, the cost C of a present area being the ancestral distribution is simply determined by:

C = (n – 1)i where n is the number of areas inhabited by the widespread taxon and i is the dispersal cost (e.g., C = 2i in fig. 5c). The cost of all other GAC areas (terminal areas A, D and ancestral areas F–I in fig. 5b) is set to infinity (an arbitrary high cost) (fig. 5c), since they are not allowed as ancestral distributions.

In terms of explaining the widespread distribution, the recent option (“only dispersal allowed”) is not directly comparable to any of the traditional assumptions. In the context of testing alternative GACs, it will weight against A0 solutions in which the areas inhabited by the widespread taxon form a monophyletic clade (fig. 6b; table 1). It will also weight against “Full set” solutions in which all areas harboring the widespread taxon occur in the GAC in positions other than that predicted by the place of the widespread taxon in the TAC (fig. 6e, table 1).

These solutions, of course, violate A2.

Ancient option This option is applicable when the widespread distribution can be assumed to be of ancient origin. All areas inhabited by the widespread taxon are considered part of the ancestral distribution. Any mismatch between this distribution and the GAC is then explained as due to extinction; dispersals are not allowed.

Under the ancient option, the only possible ancestral distribution of the widespread taxon is the most recent common ancestor in the GAC (“MRCA”) of all of the areas inhabited by the widespread taxon (H in fig. 5b). The GAC areas that are not ancestral to all of the recent areas inhabited by the taxon (A–G in fig. 5b) will require at least one dispersal and are therefore disallowed under the ancient option and are assigned infinite cost (fig. 5c). Areas in the GAC that are ancestral to the MRCA (I in fig. 5b) are allowed but will never occur in optimal reconstructions, as they will always be more costly than the MRCA (fig. 5c).

The cost of the MRCA is calculated assuming that the terminal polytomy is resolved so that the topology fits the GAC perfectly. Under these conditions, only extinction and vicariance events need to be considered because duplications are not required and dispersals are, of course, not allowed. The cost ( C) of the MRCA is then given by

C = pe + (n – 1)v where p is the number of required extinction events, n is the number of areas inhabited by the widespread taxon, and e and v the costs of the extinction and vicariance events, respectively.

The number of required extinction events (p) is computed as follows: In the GAC, focus on the subtree subtended by the MRCA: ((B, C), (D, E)) in fig. 5b. Assign 1 to the areas harboring the taxon (B, C, E) and 0 to the other areas (D). Then, find the number of losses (p) in this presence/absence character assuming irreversibility (1 → 0). In fig. 5b, there would be only one loss in area D so the cost is

C = 1e + (3 – 1)v = 2v + e In terms of explaining the widespread distribution, the ancient option is similar to A1 in that it allows extinctions but not dispersals. In the context of testing alternative GACs, however, it will strongly favor A0 solutions in which the areas inhabited by the widespread taxon form a monophyletic clade (fig. 6b; table 1). Thus, widespread taxa provide strong evidence for grouping the areas inhabited by them under the ancient option.

Free option Under the free option, all possible ancestral areas are considered and any mismatch between the areas inhabited by the widespread taxon and the GAC is explained by the most favorable combination of events. The minimum cost of each possible ancestral distribution is calculated without any constraints on the type of assumed events: dispersals, extinctions, duplications and vicariance events are all allowed.

For the Maximum Vicariance method, the optimal cost of each possible ancestral distribution is found if the terminal polytomy is resolved so that it becomes congruent with the GAC. This might hold for more complex event– cost assignments as well, if the cost of the ancestral distributions is found with algorithms ignoring the complexity of dispersals, the so– called lower bound algorithms (RONQUIST, 1995, 1998b, in press). Why the complexity of dispersals should be ignored is because optimal solutions may occasionally require combinations of dispersals that are impossible on terminal trees congruent with the GAC, but it seems that

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Fig. 6. a. TAC with a widespread taxon; b–e. Four GACs with alternative resolutions of the relationships between the areas occupied by the widespread taxon. These solutions are associated with the traditional pattern–based Assumptions A0, A1, and A2 as follows: A0 would allow only the first solution (b), in which the areas of the widespread taxon form a monophyletic clade; A1 would also allow the second GAC (c), in which the areas are paraphyletic; A2 would allow the third GAC (d), in which the areas are polyphyletic. Finally, the “Full solution set” would include some solutions (e) in which neither of the areas occurred in the position in the GAC predicted by the TAC. Fig. 6. a. Un TAC con un taxón de amplia distribución; b–e. Cuatro GACs mostrando soluciones distintas de la relacion entre las áreas ocupadas por el taxón. Estas soluciones están relacionadas con A0, A1 y A2, de la siguiente manera: A0 permitiría sólo el primer GAC (b), en el que las áreas ocupadas por el taxón de amplia distribución forman un grupo monofilético; A1 permitiría además el segundo GAC (c), en el que las áreas son parafiléticas; A2 permitiría el tercer GAC (d), en el que las áreas son polifiléticas. Finalmente, el “Full solution set” incluiría algunas soluciones (e) en las que ninguna de las áreas en el GAC aparecen en la posición en la que se encuentran en el TAC.

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these conflicts can always be solved by rearranging the terminal tree without increasing the total cost (Ronquist, unpublished data). The lower–bound algorithms are computationally extremely efficient so the implementation of the free option is straightforward if this conjecture is true.

In terms of explaining the widespread distribution, the free option is similar to A2 in that it allows all types of events. However, in the context of comparing alternative GACs, the free option will favor solutions in which the areas inhabited by the widespread taxon form a monophyletic clade, i.e., A0 solutions (fig. 6b, table 1). The relative cost difference between other solutions will depend on the set of areas inhabited by the widespread taxon and their position in the GAC (table 1). It is interesting to note that, although the free option is similar to A2 in terms of allowed events, it obviates one of the main criticisms raised against A2, namely that it is indecisive. According to the traditional view of A2, GACs 1–3 (figs. 6b–6d) would be equally probable solutions, whereas the free option selects GAC 1 (fig. 6b) as the most parsimonious solution. Thus, in this case the free option allows effective selection among alternative GACs.

Missing areas and redundant distributions In pattern–based methods, missing areas (B in fig. 1d) and redundant distributions (A in fig. 1c) are often identified in the TACs prior to the analysis and different protocols (A0, A1, and A2) are then used to determine the possible RACs. For instance, missing areas can be treated either as missing data or as observations of true absence.

If treated as missing data (A1, A2), absence may be due to primitive absence, extinction, or inadequate sampling and the missing area can thus occupy any position in the RAC. If treated as true absence (A0), only primitive absence or extinction are possible explanations. For instance, if several areas are missing from the TAC, this may be taken as evidence that these areas should be grouped in the RAC (extinction) or that the non–missing areas should be grouped (primitive absence). Redundant distributions can be treated under A0, A1 (all occurrences due to ancestry, and any GAC–TAC mismatch explained by duplication and extinction) or under A2 (some of the occurrences possibly due to dispersal).

In event–based methods, it is difficult to separate potential cases of incongruence that can be identified in TACs prior to analysis (observed) from missing areas and redundant distributions that are introduced during the TAC–GAC fitting process (inferred). If an area is redundant or missing in a TAC simply depends on the general area cladogram (GAC) being analyzed and on the particular events postulated by the reconstruction fitting the TAC to the GAC. The reconstruction

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may postulate TAC redundancy that is not apparent before analysis or change the interpretation of which areas are truly missing from the TAC. For instance, a TAC fitted to a congruent GAC will have no missing or redundant areas (figs. 3a, 3b) but if the same TAC is fitted to an incongruent GAC (fig. 3c) one must postulate that some TAC distributions are missing or redundant. A lineage (5) may have become extinct in area D and another taxon (4) may have secondarily re–colonized the same area (fig. 3c).

In this reconstruction, there is both a missing area (the absence of taxon 5 in area D) and a redundant distribution (the presence of taxon 4 in area D).

However, a different incongruent GAC (fig. 3d) postulates a different set of missing and redundant areas: in this case area C is both the missing area (the absence of taxon 5) and the redundant distribution (the presence of taxon 3). Therefore, a priori (observed) and a posteriori (inferred) cases of redundancy and missing areas should be treated in the same way in event–based methods; there is no need for special protocols dealing with these cases of incongruence prior to analysis.

The treatment of missing areas in event–based methods is of particular interest. Event–based methods treat missing areas as true absence and explain them as due to primitive absence or extinction. If the missing data interpretation were allowed, then parsimony–based tree fitting would not work because any analysis would be swamped by low–cost solutions postulating events that left no trace in the observed TAC (RONQUIST, in press).

A simple example will illustrate the eventbased treatment of missing areas: assume that we have a “two–taxa–two–area” TAC and a four area GAC (fig. 7). GAC 1 (fig. 7a) groups the TAC areas into a monophyletic group (C–D) so a vicariance event is sufficient to explain the history of the organisms; absence of the group in areas A and B is explained as primitive absence. This could mean that the ancestor of the TAC dispersed from an area outside of the considered GAC to the area in the GAC ancestral to C and D, that the outgroups of the TAC occur in areas A and B, or some other alternative. Since we have no information about the outgroups, we cannot distinguish among the alternatives.

GAC 2 (fig. 7b) groups the TAC areas into a paraphyletic group so a vicariance and an extinction event are required to explain the history of the organisms. In GAC 3 (figs. 7c–d), the TAC areas form a polyphyletic group. The TAC can be mapped onto this GAC either by introducing a vicariance and two extinction events (fig. 7c) or one dispersal event (fig. 7d). If vicariance and duplication events are associated with a low cost and dispersal and extinction with high cost, as suggested above, GAC 1 would clearly be favored over GAC 2 and GAC 3. Thus, in searching for the optimal GAC, event–based methods favor scenarios in which the missing areas are explained as being

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Table 1. Testing alternative GACs using the event–based approach. For each of the GACs in figs.

6b–e, the minimal cost of fitting them to the TAC in figure 6a is calculated using three different options for treating widespread taxa (recent, ancient and free), and two different event–based methods having different event–cost assignments (parsimony–based tree fitting and maximum vicariance). For parsimony–based tree fitting, the costs of the events are: duplications (d) = vicariance (v) = 0.01, extinction (e) = 1.0 and dispersal (i) = 2.0. For maximum vicariance the event costs are d = e = i = 0 and v = – 1. In calculating the costs, note that the constraints implied by the recent and ancient options ("only dispersals allowed" or "no dispersals allowed", respectively) were applied only to the ancestral distribution of the widespread taxon, not to the distributions of the rest of the nodes in the TAC. Each of the GACs (figs. 6b–e) corresponds to one of the pattern–based Assumptions 0, 1 or 2 or the “Full solution set” (see text of fig. 6): * In general, the maximum vicariance reconstruction can be obtained directly from the parsimony– based reconstruction by replacing the cost assignments (d = i = e = 0, v = – 1). However, in this case the least costly reconstruction in parsimony–based tree fitting is cheaper (v + 2i) than the one with the maximum number of vicariance events (d + 2v + 4e).

Tabla 1. Comparación de distintos GACs utilizando las opciones recent, ancient y free en la resolución de taxones de amplia distribución. Para cada uno de los GACs en las figuras 6b–6e, calculamos el coste mínimo de “ajuste” al TAC (fig. 6a), utilizando tres opciones diferentes para resolver taxones de amplia distribución (recent, ancient, y free) y dos métodos distintos que difieren en el coste asignado a cada proceso (parsimony–based tree fitting y maximum vicariance).

En parsimony–based tree fitting, el coste de cada proceso es: duplicación (d) = vicariancia (v) = 0.01, extinción (e) = 1.0 y dispersión (i) = 2.0. En maximum vicariance, los costes son d = e = i = 0 y v = – 1. Obsérvese que, al calcular los costes, las restricciones impuestas por las opciones reciente y ancestral (“sólo se permiten dispersiones” o “no se permiten dispersiones”) se aplican sólo a la distribución ancestral del taxón de amplia distribución, no a las distribuciones del resto de nodos en el TAC. Cada uno de los GACs (figs. 6b–6e) corresponde a una de las tradicionales Asunciones 0, 1 y 2, o al “Full solution set” (ver pie de figura 6): * En general, la reconstrucción con el método de maximum vicariance se obtiene directamente de la reconstrucción con parsimony–based tree fitting remplazando los costes de los procesos por (d = i = e = 0, v = – 1).

Sin embargo, en este caso el coste de la reconstrucción óptima en parsimony–based tree fitting es menor (v + 2i) que la que se obtendría considerando el número máximo de eventos de vicariancia (d + 2v + 4e).

Option

GAC1, fig. 6b

GAC2, fig. 6c

GAC3, fig. 6d

GAC4, fig. 6e

(Assumption 0)

(Assumption 1)

(Assumption 2)

(“Full solution set”)

Parsimony–based tree fitting Recent

2v+e+i = 3.02

2v+i = 2.02

2v+e+i = 3.02

v+2i = 4.01

Ancient

3v = 0.03

d+2v+3e = 3.03

d+2v+4e = 4.03

d+2v+4e = 4.03

Free

3v = 0.03

2v+i = 2.02

2v+e+i = 3.02

v+2i = 4.01

Recent

–2

–2

–2

–1

Ancient

–3

–2

–2

–2

Free

–3

–2

–2

– 2*

Maximum vicariance

due to primitive absence, and the rest of the GAC fits the TAC perfectly (GAC1, fig. 7a). The relative cost of other GACs depends on the event–cost assignments. Generally speaking, extinction explanations are favored over dispersal explanations unless the extinction cost is considerably higher than the dispersal cost.

Consider, for instance, the two different ways of

fitting the TAC to GAC3 (figs. 7c–d). The extinction explanation (fig. 7c; one vicariance (cost v) and 2 extinctions (cost 2e)) is favored over the dispersal explanation (fig. 7d; one dispersal (cost i)) unless i < 2e + v. This is an event–cost assignment scheme that in most cases has a low probability of discovering phylogenetically constrained distribution patterns.

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Fig. 7. Treatment of missing areas in the event–based approach. A two–taxon–two–area TAC is fitted to a four–area GAC: a. If the TAC areas are monophyletic in the GAC, only one vicariance event is required; b. If the TAC areas are paraphyletic in the GAC, one extinction and one vicariance event are required; c–d. If the TAC areas are polyphyletic in the GAC, either a vicariance and two extinction events (c) or a dispersal event (d) are required. (Symbols as in figure 3.)

Fig. 7. Tratamiento de las “áreas ausentes“ en “biogeografía cladista de procesos”. Un cladograma de áreas con dos taxones distribuidos en dos áreas superimpuesto en un GAC de cuatro áreas: a.

Si las áreas del TAC son monofiléticas en el GAC, sólo se requiere un evento de vicarianza para explicar las distribuciones en el TAC; b. Si las áreas del TAC son parafiléticas en el GAC, una extinción y un evento de vicarianza son necesarios para explicar la distribución; c–d. Si las áreas del TAC son polifiléticas en el GAC, se necesitan o bien una vicarianza y dos eventos de extinción (c) o un evento de dispersión (d). (Símbolos como en la figura 3.)

As this example clearly demonstrates, absence data are informative in the search for the optimal GAC with event–based methods. The cost of extinction events determines the extent to which absence data influence the search for the GAC: the lower the weight of extinction, the smaller the effect of absence data. A low extinction cost downplays the importance of absence data, regardless of whether this is caused by poor sampling or true absence. Thus, an event–based method with a low extinction cost mimics the missing data treatment of true absences in pattern–based methods. This is a good argument for assigning a lower cost to extinctions than to dispersals in event– based methods of biogeographic absence.

Which assumption should we choose?

Of the three event–based options described above for treating widespread taxa, there is none that is ideally suited to all kinds of problems. Each option has its strengths and weaknesses, and the choice should therefore depend on the nature of the data. The free option is more general in that it allows more processes in explaining widespread terminal distributions. On the negative side, it is computationally more demanding than the other options and because it allows more solutions, it may also be associated with loss of information concerning the optimal GAC. To some extent, however, the potential information loss may be

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Heterandria

Xiphophorus

variatus–group (1) milleri (2)

species A (6)

maculatus (2)

H. jonesi (1)

pygmaeus (1)

species B (9)

nigrensis (1)

species C (4,5)

montezumae (1)

species D (10)

cortezi (1)

species E (7)

clemenciae (3)

Chajmaic bimaculata (8)

alvarezi (4,5,6) Molagua–Polochic– Honduras helleri (9,10)

other bimaculata (2)

Chajmaic helleri (8) other helleri (2)

Recent

Assumption 2

Ancient

Free

Assumption 0

Assumption 1

Fig. 8. Example of the application of the event–based options to treat widespread taxa. Taxon– area cladograms for the poeciliid fish genera: Heterandria (a) and Xiphophorus (b) (After ROSEN, 1978), with areas 4 and 5 combined in accordance with PAGE (1989); c–e. General area cladogram derived with TreeFitter 1.0 (RONQUISt, 2001) for Heterandria / Xiphophorus under the three different options to treat widespread taxa: recent, ancient, and free; f–h. General area cladograms obtained with Component 2.0 (PAGE, 1993) under A0, A1, and A2 (After VAN VELLER et al., 2000).

Fig. 8. Ejemplo del tratamiento de taxones de amplia distribución en “biogeografía cladista de procesos”. Cladograma de áreas (TAC) para los géneros de Poeciliidae: Heterandria (a) y Xiphophorus (b) (modificado de ROSEN, 1978); las áreas 4 y 5 han sido combinadas en una sola área de distribución como en PAGE (1989); c–e. GACs obtenidos con Tree Fitter 1.0 (RONQUIST, 2001) para Heterandria / Xiphophorus utilizando tres opciones diferentes para resolver taxones de amplia distribución: recent, ancient y free; f–h. GACs obtenidos con Component 2.0 (PAGE, 1993) utilizando las opciones tradicionales A0, A1 y A2 (adaptado de VAN VELLER et al., 2000).

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Heterandria

Xiphophorus

Recent

Ancient

Free

Fig. 9. Event–based reconstructions showing the fit between the TACs of Heterandria and Xiphophorus (figs. 8a, 8b) and the GACs obtained under the event–based options to treat widespread taxa (figs. 8c–8e). Biogeographic reconstructions of Heterandria and Xiphophorus: a–b. Under the recent option; c–d. Under the ancient option; e–f. Under the free option. The cost of the reconstruction is indicated under each figure (d = v = 0, e =1.0, i = 2.0). Symbols as in figure 3. Small black arrows: dispersal events within the terminals that are not considered in the cost of the reconstruction under the recent option because they are invariable across the possible GACs (“only dispersal allowed”). Hollow circles: vicariance events within the terminals that are not considered in the cost of the reconstruction under the ancient option because they are invariable across the GACs (“only vicariance and extinction allowed”). Hollow arrows: dispersal events within the terminals that are included in the cost of the free reconstruction, since this option allows all types of events in explaining the widespread distribution.

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counteracted by the differences in the cost associated with the allowed solutions. The ancient option makes the boldest assumptions about the origin of the widespread distributions. If the assumptions are warranted, the search for the optimal GAC should gain in power; if they are not, the result of the analysis may be flawed. For instance, the ancient option might be useful in analyzing the distribution history of old groups that are very unlikely to have dispersed, or in which the widespread taxon has lost the ability to disperse (e.g., a wingless species in a fully winged group).

In many cases, it is quite clear that the widespread terminals are younger than any of the ancestral areas in the GAC, in which case the recent option would be the only defensible choice. The recent option may also be advantageous in the identification of phylogenetically constrained biogeographic patterns because it does not allow vicariance events within widespread terminals, in contrast to the free and ancient options. Assume that we test for constrained distributions by comparing the cost of the observed TAC with that of random TACs obtained either by randomly drawing new TAC topologies or randomly shuffling the TAC terminals. Because the widespread terminals are the same in both the observed and random TACs, the terminal events will not contribute to distinguishing the observed TAC from the random TACs. However, it is quite likely that several of the “terminal” events could be pushed onto the ancestral nodes in the observed TAC but not in the random TACs. This potential support for the GAC is ignored by the free and ancient options. The recent option forces vicariance events onto ancestral nodes in the TAC and is therefore more powerful in separating phylogenetically constrained distribution patterns from random data in this kind of test. For an empirical example, see SANMARTÍN et al. (2001).

Software The Recent, Ancient and Free event-based options have been implemented in the computer program TreeFitter 1.0 (RONQUIST, 2001). TreeFitter is a program for finding the optimal biogeographic reconstruction/s (GACs), given one or more TACs. TreeFitter is available as free software on the website: http://www.ebc.uu.se/systzoo/research/ treefitter/treefitter.html.

An empirical example: Xiphophorus and Heterandria (Rosen, 1978) R OSEN (1978)’s study on the poeciliid fishes Heterandria and Xiphophorus is probably the most widely used benchmark data set in the development of biogeographic methods. Because the solutions under Assumptions 0, 1, and 2 for this data set are well known, it provides a useful comparison with the results of the event–based options.

Figure 8 shows the taxon-area cladograms for Heterandria (fig. 8a) and Xiphophorus (fig. 8b).

They include widespread taxa (e.g., X. alvarezi in areas 4, 5, 6), redundant distributions (e.g., area 2 in Xiphophorus), and missing areas (e.g., area 3 in Heterandria or area 7 in Xiphophorus).

Using TreeFitter 1.0 (R ONQUIST , 2001), we searched for the optimal GAC for the two genera treating widespread taxa under the different event–based options.

The recent option (fig. 8c) finds an optimal GAC that basically follows the pattern of area relationships in Heterandria. The areas included in widespread (4–5, 6, 9 and 10) or redundant (2) distributions in Xiphophorus are positioned in the optimal GAC according to the TAC of Heterandria; only area 3, missing in Heterandria, is placed according to its position in Xiphophorus (basal to areas 4–5). The optimal GAC under the recent option is one of the three GACs found

Fig. 9. Reconstrucción biogeográfica mostrando el grado de ajuste entre los TACs de Herterandria y Xiphophorus (figs. 8a, 8b) y los tres GACs obtenidos con las tres opciones para resolver taxones de amplia distribución: recent, ancient y free (figs. 8c–8e) en la resolución de taxones de amplia distribución (figs. 8c–8e). Reconstrucción de la historia biogeográfica de Heterandria y Xiphophorus: (a–b) con la opción recent, (c–d) la opción ancient y (e–f) la opción free. Debajo de cada reconstrucción se indica su coste en términos de procesos biogeográficos (v = d = 0, e = 1.0, i = 2.0). Símbolos como en la figura 3. Pequeñas flechas negras: dispersiones dentro de los terminales no consideradas en el coste de la reconstrucción bajo la opción recent porque estarían presentes en todos los posibles GAC (“sólo se permite dispersión”, ver texto). Círculos blancos: vicarianzas dentro de los terminales no consideradas en el coste de la reconstrucción ancient porque estarían presentes en todos los posibles GAC (“sólo se permite vicarianza y extinción”, ver texto). Flechas blancas: dispersiones dentro de los terminales incluidas en el coste de la reconstrucción free porque esta opción permite cualquier tipo de evento (dispersión, vicarianza, o extinción) para explicar la amplia distribución.

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under A2 (fig. 8f) by PAGE (1989) and VAN VELLER et al. (2000) but is different from the single GAC obtained under either A0 (fig. 8g) or A1 (fig. 8h).

The optimal GAC under the ancient option (fig. 8d) agrees mainly with the relationships among areas in Xiphophorus. Areas 1 and 3 are placed basally in the cladogram, whereas areas 4– 5 and 6, and areas 9 and 10, are grouped together as sister–areas. This is the same GAC found by VAN VELLER et al. (2000) using COMPONENT 2.0 (PAGE, 1993) under A0 (fig. 8g), which is not surprising considering that both the ancient option and A0 group areas based on widespread distributions. It is also similar to the GAC obtained under A1 (fig. 8h) except that the areas forming part of the widespread distribution are not monophyletic in A1. This assumption, like the ancient option, considers the widespread distribution to be ancestral and only allows extinction and vicariance events as possible explanations. In this case, treating the widespread taxa as fully informative about area relationships conflicts with the evidence from endemic taxa because for each pair of areas in a widespread terminal in the Xiphophorus TAC (e.g., 9 and 10), the corresponding endemic taxa in the Heterandria TAC are not closely related ( species B and species D ).

Nevertheless, the grouping information provided by the widespread taxa is strong enough to override the signal from the endemic taxa.

The free option finds the same optimal GAC as the recent option. Thus, the widespread terminal distributions in Xiphophorus are best explained as due to recent dispersal when all processes are allowed and the cost of all implied events, ancestral as well as terminal, is considered (see fig. 9). As mentioned above, this GAC is one of the three solutions found under A2 by PAGE (1989: his fig. 10) and VAN VELLER et al. (2000: their fig. 13c). The other two solutions place area 3 basal to area 9 or areas 3 and 9 in a monophyletic clade, in both cases requiring an extra extinction event in the event–based framework. For these data, A2 is clearly associated with a loss in resolving power compared to A0 and A1 because it allows three instead of one solution. This information loss does not occur for the free option in the event– based analyses.

Our analyses of the Rosen data show some of the similarities and differences between the traditional pattern–based assumptions and the event–based options. Clearly, there is no one– to–one correspondence between the options and assumptions. Both the recent and free options share properties with A2, whereas the ancient option is more similar to A0 and A1. For Rosen’s data, the results obtained with the free option support those obtained with the recent option.

This suggests that the ancient option may force unrealistic constraints onto the analysis and that the optimal GAC under the free and recent options may be preferable. This is also the GAC

that is better supported by the phylogenetically determined (as opposed to the within–terminal) area relationships in the two TACs.

Conclusions The controversy surrounding the treatment of widespread taxa, missing areas and redundant distributions in historical biogeography has been difficult to resolve because of the lack of a common theoretical framework. The event–based approach provides such a framework within which the nature of different methodological options and their effect on biogeographic reconstruction can easily be understood. We hope that our exploration of event–based solutions to the resolution of incongruence in biogeographic inference will contribute to a more focused debate on these issues in the future. The event– based solutions described here should be applicable not only to biogeographic analysis but also to coevolutionary inference.

Acknowledgments We thank Henrik Enghoff and an anonymous reviewer for useful comments on this manuscript.

This research was supported by the Swedish Natural Science Research Council (grant to Fredrik Ronquist) and through a European Community Marie Curie Fellowship (Isabel Sanmartín) under the Improving Human Potential programme (Project MCFI–2000–00794).

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"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 25.2 (2002)

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Dos nuevas especies de Anillini cavernicolas pertenecientes al género Speleotyphlus Jeanne, 1973 (Coleoptera, Carabidae) J. Vives†, O. Escolà & E. Vives

Vives†, J., Escolà, O. & Vives, E., 2002. Dos nuevas especies de Anillini cavernícolas pertenecientes al género Speleotyphlus Jeanne, 1973 (Coleoptera, Carabidae). Animal Biodiversity and Conservation, 25.2: 95–99.

Abstract Two new species of subterranean Anillini belonging to genus Speleotyphlus Jeanne, 1973 (Coleoptera, Carabidae).— Speleotyphlus comasi n. sp. and S . virgilii n. sp. from two caves Cueva del Turcacho (Teruel province) and Cova Bonica in Ulldecona (Tarragona province) are described. The former was collected in 1981 and was a female. Despite several attempts the male was not found. Only one other species S. fideli Viñolas & Escolà has been described for the province of Teruel but S. comasi clearly differs regarding the shape of the elytra and umbilicate series. S. virgilii n. sp. is very similar to S. fadriquei Español, 1999 but is slightly larger and the pronotum is transverse rather than elongated as in S. fadriquei Español.

Key words: Speleotyphlus comasi n. sp., Speleotyphlus virgilii n. sp., Coleoptera, Carabidae, Anillini, Spain.

Resumen Dos nuevas especies de Anillini cavernícolas pertenecientes al género Speleotyphlus Jeanne,1973 (Coleoptera, Carabidae) .— Se describen dos nuevas especies Speleotyphlus comasi sp. n. y S. virgilii sp. n. procedentes de dos cuevas: Cueva del Turcacho (provincia de Teruel) y Cova Bonica de Ulldecona (provincia de Tarragona). La primera fue recolectada en 1981 y es una hembra. A pesar de muchos intentos, no se pudo localizar el macho. En la provincia de Teruel sólo se ha descrito otra especie S. fideli Viñolas & Escolà aunque S. comasi difiere claramente de ella en la forma de los elitros y las series umbilicadas. S. virgilii sp. n. es muy simlar a S. fadriquei Español, 1999 pero es ligeramente más larga y el pronoto es transverso más que alargado como en S. fadriquei Español.

Palabras clave: Speleotyphlus comasi sp. n.; Speleotyphlus virgilii sp. n., Coleoptera, Carabidae, Anillini, España.

(Received: 9 IV 02; Conditional acceptance: 22 V 02; Final acceptance: 27 VIII 02) Oleguer Escolà1 & Eduard Vives2, Museu de Ciències Naturals (Zoologia), Passeig Picasso s/n, 08003 Barcelona, Espanya (Spain).

1 2

†

E–mail: oescola@mail.bcn.es E–mail: eduard_vives@hotmail.com Joan Vives i Duran deceased in 15 XI 2000

ISSN: 1578–665X

© 2002 Museu de Ciències Naturals

96

Introducción En 1966 Español describió una especie de Anillini cavernícola, Microtyphlus aurouxi Español, 1966, procedente de las capturas de Lluís Auroux en el Avenc de Serenge, Cabanes (Castelló). Posteriormente el mismo autor describió también Catalanotyphlus jusmeti Español, 1971 para otros ejemplares de Anillini cavernícolas de Coves de Vinromà, también en el norte de la provincia de Castelló. Estas dos especies muy próximas sistemáticamente, fueron englobadas en una nueva división de los Anillini euro–mediterráneos, creada por J EANNE (1973), para incluir aquellas especies cavernícolas de forma alargada y convexa cuya serie umbilicada de poros elitrales se ajustaba al tipo B de JEANNEL (1963).

Recientemente ESPAÑOL ha descrito otra nueva especie Speleotyphlus fadriquei Español, 1999; procedente de una sima del sur de la provincia de Tarragona, en el término municipal de Serra d’Almos, también con una facies típicamente cavernícola.

Con estas nuevas aportaciones el género Spelotyphlus alcanza la cifra de cinco especies conocidas, S. aurouxi, S. jusmeti, S. fadriquei, S. comasi sp. n. y S. virgilii sp. n. Muy probablemente aparecerán más especies de este género en las numerosas cavidades de Tarragona, Castelló y Teruel, especialmente en la zona montañosa de Ports de Caro (también denominados de Tortosa o Beceite), donde hasta la fecha se conocen otros carábidos cavernícolas como Paraphaenops breuilianus Jeannel, 1916 y Cephalosphodrus lassallei Mateu, 1989; pero no se ha recolectado ningún representante de Carabidae Anillini (ZABALLOS & JEANNE, 1994).

Material y métodos Gracias a las exploraciones espeleológicas de nuestros colegas Florentino Fadrique y de Jordi Comas, han sido colectadas dos nuevas especies procedentes del sur de la provincia de Tarragona y del sureste de la provincia de Teruel respectivamente. Estas dos nuevas especies que aquí se describen se incluyen perfectamente entre los representantes conocidos del mencionado género Speleotyphlus, si bien se pueden separar por los caracteres que se indican en su descripción.

Descripción

Vives et al.

Descripción Longitud, 2 mm. Anchura, 0,8 mm. Coloración testácea, con las patas y antenas levemente más claras casi amarillas. Aspecto general largo y subparalelo, con la cabeza grande, netamente mas larga que ancha, con ausencia total de ojos, que tan solo están indicados por una leve mancha amarillenta y una seda supraorbital anterior muy larga y otra posterior más corta y arqueada.

Antenas de once artejos, con el primero mucho mas largo y robusto que el segundo, éste netamente estrechado en su mitad, del tercero al sexto son subiguales, siempre mucho más largos que anchos del séptimo al décimo subcuadrados, el onceavo es ovalado y aplanado. Las mandíbulas son algo salientes y con su ápice curvado. El labro es rectangular, y está provisto de cuatro sedas en su reborde anterior.

El protórax es tan largo como ancho en su cuarto anterior, con sus lados arqueados y sinuados en el tercio posterior que es mucho más estrecho.

Los ángulos posteriores son agudos y salientes, y presentan una larga seda umbilicada. El surco lateral está rebordeado y provisto de una larga seda en su cuarto anterior. El disco pronotal es aplanado y posee un leve surco longitudinal mediano. Toda la superficie protorácica está recubierta por unas cortas sedas espaciadas, más numerosas en el reborde marginal.

Los élitros son largos y subparalelos, casi el doble de largos que anchos en la zona basal. Los húmeros son muy salientes y están fuertemente dentados. El reborde marginal es ancho y bien trazado, levemente estrechado en el quinto apical; todo él provisto de largas sedas umbilicadas tal como se indica en la figura 1. La superficie elitral es convexa en el disco y levemente aplanada en el ápice, con el ángulo apical poco marcado. El ápice elitral está levemente truncado, dejando al descubierto el último segmento abdominal. La serie umbilicada presenta nueve poros setígeros con largas sedas, una pequeña seda yuxtaescutelar y tres largas sedas discales alineadas. La superficie elitral es fuertemente chagrinada, sin restos de estrías y algo brillante.

Las patas son cortas, con los fémures anteriores poco ensanchados en su parte distal. Las tibias intermedias y posteriores son finas y estan algo sinuadas en su primer tercio. Todas las patas y tarsos estan recubiertos por unas cortas sedas doradas.

Etimología El nombre de esta especie está dedicado a su descubridor, Jordi Comas i Navarro, en reconocimiento a su larga labor bioespeleológica.

Speleotyphlus comasi n. sp. (fig. 1) Material estudiado Holotipo: 1} Cueva del Turcacho, Iglesuela del Cid, Teruel, 19 IV 1981, Jordi Comas leg. Depositado en el Museu de Zoologia de Barcelona, (MZB nº 2002–0192).

Comentarios Especie cavernícola hasta la fecha tan solo conocida por un ejemplar hembra recolectado en la Cueva del Turcacho, provincia de Teruel. Durante años esta cueva ha sido visitada por numerosos bioespeleólogos sin poder recolectar ningún

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1 mm

1 mm

Fig. 1. Speleotyphlus comasi sp. n., habitus del holotipo.

Fig. 2. Speleotyphlus virgilii sp. n., habitus del holotipo.

Fig. 1. Speleotyphlus comasi n. sp., habitus of the holotype.

Fig. 2. Speleotyphlus virgilii n. sp. habitus of the holotype.

ejemplar más de dicha especie. Al parecer se trataría de un endogeo de cueva al igual que otros Anillini cavernícolas mediterráneos.

Es la segunda especie de carábido cavernícola conocida como procedente de la provincia de Teruel, ya que recientemente VIÑOLAS & ESCOLÀ (1999) han descrito otro Anillini correspondiente al género Microtyphlus, también procedente de una cavidad de Teruel. Sin embargo S.comasi n.sp. es muy diferente de Microtyphlus fideli Viñolas & Escolà, 1999; especialmente por la forma de sus élitros y la topografía de la serie umbilicada.

10} 10 I 2000; 4} 11 II 2000; 1} 19 II 2000; 4{ 2 III 2000; 1{ y 1} 8 IV 2000. Recolectados por F. Fadrique. Depositados en el Museu de Zoologia de Barcelona y en la colección J. & E. Vives (Terrassa).

Speleotyphlus virgilii sp. n. (figs. 2–4) Material estudiado Holotipo: 1{ Cova Bonica, Ulldecona (Tarragona–S) 10 I 2000, F. Fadrique leg. Depositado en el Museu de Zoologia de Barcelona (MZB nº 2000–0342).

Paratipos: 28 ejemplares de Cova Bonica, Ulldecona (Tarragona–S); 1} 13 III 2000, 6{ y

Descripción Longitud, 2 mm. Anchura 0,8 mm. Coloración amarillo testácea. Cabeza y protórax de color caramelo. Aspecto general largo y subparalelo, con la cabeza alargada, sin rastros de zona ocular y con varias largas sedas en la zona orbital. El labro es rectangular y está provisto de seis sedas, las centrales más cortas (fig. 3). El cuello es grueso y sin estrechamiento posterior. Las antenas son cortas, justo alcanzando la base elitral, con el primer artejo en forma de escapo y levemente más corto que el segundo; del tercero al quinto tienen forma fusiforme y del sexto al décimo son subglobulares; el undécimo es fusiforme y aplanado.

El protórax es levemente más ancho que largo en su borde anterior, con sus lados arqueados y

Vives et al.

98

0,50 mm

Figs. 3, 4. Speleotyphlus virgilii sp. n.. 3. Labro: a. Visión dorsal; b. Visión ventral. 4. Edeago, visión lateral.

Figs. 3, 4. Speleotyphlus virgilii n. sp. 3. Labrum: a. Dorsal view; b. Ventral view. 4. Oedeagus, lateral view.

sinuados en el tercio posterior, formando unos pequeños ángulos agudos en su base posterior, muy poco salientes y provistos de una larga seda. El reborde lateral está bien marcado y provisto de una larga seda en el quinto anterior, además de una serie de pequeñas sedas cortas repartidas por todo el disco protorácico y sus bordes laterales. El disco pronotal está dividido por un surco mediano longitudinal que no alcanza el borde anterior ni el posterior.

Los élitros son largos y paralelos, levemente más largos y convexos en el macho, y algo más aplanados en la hembra, con lo húmeros redondeados y levemente dentados. El reborde marginal es estre-

cho y no alcanza el ápice elitral; está provisto de una serie umbilicada de macroquetas según la topografía que se aprecia en la figura 2. La superficie elitral es chagrinada y con brillo opaco. El ángulo apical apenas está indicado en el macho, y es practicamente ausente en la hembra. Las patas son cortas y finas, con el primer artejo de los protarsos dilatado en los machos, y provistos de un leve diente en su lado interno.

El órgano copulador masculino es corto y grueso, sin piezas esclerotizadas aparentes en su saco interno (fig. 4). Los parámeros laterales son anchos en su base y acuminados en el ápice, provistos de dos largas macroquetas.

Tabla 1. Caracteres diferenciales de Speleotyphlus comasi sp. n. y Spelotyphlus virgilii sp. n.

Table 1. Diferential characters of Speleotyphlus comasi n. sp. and Spelotyphlus virgilii n. sp.

Speleotyphlus comasi sp. n.

1. Presencia de dos sedas supraorbitales La posterior muy corta 2. Labro con cuatro sedas 3. Protórax tan largo como ancho 4. Angulos posteriores de protórax agudos y salientes 5. Elitros casi doble largos que anchos en su base (8/4) 6. Húmeros angulosos y muy salientes

Speleotyphlus virgilii sp. n.

1. Presencia de varias sedas orbitales cortas 2. Labro con seis sedas 3. Protórax levemente más ancho que largo 4. Ángulos posteriores del protórax poco salientes 5. Elitros más cortos y más convexos (7/4) 6. Húmeros redondeados y poco salientes

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Clave de las especies del género Speletyphlus Jeanne, 1973 actualizada.

Updated key of species of genera Speletyphlus Jeanne, 1973.

1

2

3

4

Superficie del cuerpo lisa, sin micro escultura; húmeros redondeados, nada salientes Superficie del cuerpo provista de micro escultura; húmeros marcados y salientes Talla igual o menor de 2 mm; cuerpo paralelo y convexo; superficie elitral fuertemente rugosa Talla mayor de 2 mm; cuerpo de contorno no paralelo, muy poco convexo; superficie poco rugosa; protórax poco estrechado en la base Protórax transverso o casi; con los ángulos posteriores rectos, apenas salientes Protórax más largo que ancho; con los ángulos posteriores muy agudos y salientes Los élitros casi el doble largos que anchos (8/4); los húmeros muy salientes Los élitros mas cortos (7/4) con la zona humeral redondeada y dentada

S. aurouxi (Español) 2 3

S. jusmeti (Español) 4

S. fadriquei Español S. comasi sp. n.

S. virgilii sp. n.

Etimología Dedicado como prueba de agradecimiento a Joaquim Virgili que ha colaborado en numerosas campañas espeleológicas de la región con sus estudios sobre arte rupestre de Ulldecona desde hace más de 25 años y que en compañía de nuestro colaborador Florentino Fadrique del Hospitalet de l´Infant colectaron tan interesante especie.

los dibujos que acompañan el presente trabajo.

También hemos de agradecer al amigo Florentino Fadrique, que tan activamente está realizando una fructífera labor bioespeleológica de exploración sistemática de las cavidades levantinas.

Comentarios Esta especie tiene una morfología similar a Speleotyphlus fadriquei Español, 1999; del que se separa principalmente por su tamaño algo mayor, el color elitral mucho más claro que S. fadriquei, y especialmente por el protórax transverso en S. virgilii y alargado en S. fadriquei. El edeago es algo más corto y robusto en S. virgilii.

Las dos especies pueden separase fácilmente según sus caracteres diferenciales (tabla 1).

Se actualiza la clave de las especies del género Speleotyphlus Jeanne, 1973, publicada por Español, 1999 y que permite una mayor discriminación de las cinco especies conocidas.

ESPAÑOL, F., 1966. Interesantes descubrimientos bioespeleológicos en la provincia de Castellón.

P. Inst. Biol. Apl., 40: 67–79.

– 1971. Nuevos Anillini cavernícolas del NE de España (Col. Trechidae). P. Inst. Biol. Apl., 51: 79–88.

– 1999. Descripción de Speleotyphlus fadriquei sp. n., con revisión del género (Coleoptera, Carabidae). Misc. Zool., 22.1: 53–57.

J EANNE , C., 1973. Sur la classification des bembidiides endogés de la Region euro– mediterranéenne. Nou. Rev. Ent., 3: 83–102.

J EANNEL , R.,1963. Monographie des Anillini Bembidiides endogés (Coleoptera, Trechidae).

Mém. Mus. Nat. Hist. Nat., Ser. A, Zool., 35(2): 33–204.

VIÑOLAS, A. & ESCOLÀ, O., 1999. Microtyphlus fideli sp. n. de Anillina de la sima Latonero, Castellote, Teruel (Coleoptera, Carabidae, Bembidiini). Misc. Zool., 22.2: 85–89.

ZABALLOS, J. P. & JEANNE, C., 1994. Nuevo catálogo de los carábidos (Coleoptera) de la Península Ibérica. Monografías S. E. A., 1. Zaragoza.

Agradecimientos Ante todo tenemos que agradecer a nuestro colega de tantos años, el Sr. Jordi Comas, por su amabilidad en ceder el único ejemplar de S. comasi, así como por su artística colaboración al realizar

Referencias

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

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Animal Biodiversity and Conservation 25.2 (2002)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (abans Miscel·lània Zoològica) és una revista inter­ disciplinària publicada, des de 1958, pel Museu de Zoologia de Barcelona. Inclou articles d'inves­tigació empírica i teòrica en totes les àrees de la zoologia (sistemàtica, taxo­nomia, morfo­logia, biogeografia, ecologia, etologia, fisiologia i genètica) procedents de totes les regions del món amb especial énfa­ sis als estudis que d'una manera o altre tinguin relevància en la biología de la conservació. La revista no publica catàlegs, llistes d'espècies o cites puntuals. Els estudis realitzats amb espècies rares o protegides poden no ser acceptats tret que els autors disposin dels permisos corresponents. Cada volum anual consta de dos fascicles.

Animal Biodiversity and Conservation es troba registrada en la majoria de les bases de dades més importants i està disponible gratuitament a inter­ net a http://www.museuzoologia.bcn.es/servis/servis3. htm, de manera que permet una difusió mundial dels seus articles.

Tots els manuscrits són revisats per l'editor executiu, un editor i dos revisors independents, triats d'una llista internacional, a fi de garantir–ne la qualitat. El procés de revisió és ràpid i constructiu. La publicació dels treballs acceptats es fa normalment dintre dels 12 mesos posteriors a la recepció.

Una vegada hagin estat acceptats passaran a ser propietat de la revista. Aquesta es reserva els drets d’autor, i cap part dels treballs no podrà ser reproduïda sense citar–ne la procedència.

Normes de publicació Els treballs s'enviaran preferentment de forma elec­ trònica (publicacionsmuseuciencies@mail.bcn.es). El format preferit és un document Rich Text Format (RTF) o DOC que inclogui les figures (TIF). Si s'opta per la versió impresa, s'han d'enviar quatre còpies del treball juntament amb una còpia en disquet a la Secretaria de Redacció. Cal incloure, juntament amb l'article, una carta on es faci constar que el treball està basat en investigacions originals no publicades anterior­ment i que està sotmès a Ani­ mal Biodiversity and Conservation en exclusiva. A la carta també ha de constar, per a aquells treballs en que calgui manipular animals, que els autors disposen dels permisos necessaris i que compleixen la normativa de protecció animal vigent. També es poden suggerir possibles assessors.

Quan l'article sigui acceptat, els autors hauran d'enviar a la Redacció una còpia impresa de la versió final acompanyada d'un disquet indicant el programa utilitzat (preferiblement en Word).

Les proves d'impremta enviades a l'autor per a la correcció, seran retornades al Consell Editor en el termini de 10 dies. Aniran a càrrec dels autors les despeses degudes a modificacions substancials introduïdes per ells en el text original acceptat.

ISSN: 1578–665X

El primer autor rebrà 50 separates del treball sense càrrec a més d'una separata electrònica en format PDF. Manuscrits Els treballs seran presentats en format DIN A­–4 (30 línies de 70 espais cada una) a doble espai i amb totes les pàgines numerades. Els manus­crits han de ser complets, amb taules i figures. No s'han d'enviar les figures originals fins que l'article no hagi estat acceptat.

El text es podrà redactar en anglès, castellà o català. Se suggereix als autors que enviïn els seus treballs en anglès. La revista els ofereix, sense cap càrrec, un servei de correcció per part d'una persona especialitzada en revistes científiques. En tots els casos, els textos hauran de ser redactats correctament i amb un llenguatge clar i concís. La redacció del text serà impersonal, i s'evitarà sempre la primera persona.

Els caràcters cursius s’empraran per als noms cien­ tífics de gèneres i d’espècies i per als neologismes intraduïbles; les cites textuals, independentment de la llengua, seran consignades en lletra rodona i entre cometes i els noms d’autor que segueixin un tàxon aniran en rodona.

Quan se citi una espècie per primera vegada en el text, es ressenyarà, sempre que sigui possible, el seu nom comú.

Els topònims s’escriuran o bé en la forma original o bé en la llengua en què estigui escrit el treball, seguint sempre el mateix criteri.

Els nombres de l’u al nou, sempre que estiguin en el text, s’escriuran amb lletres, excepte quan precedeixin una unitat de mesura. Els nombres més grans s'escriuran amb xifres excepte quan comencin una frase.

Les dates s’indicaran de la forma següent: 28 VI 99; 28, 30 VI 99 (dies 28 i 30); 28–30 VI 99 (dies 28 a 30).

S’evitaran sempre les notes a peu de pàgina.

Format dels articles Títol. El títol serà concís, però suficientment indi­ cador del contingut. Els títols amb desig­nacions de sèries numèriques (I, II, III,...) seran acceptats previ acord amb l'editor.

Nom de l’autor o els autors.

Abstract en anglès que no ultrapassi les 12 línies mecanografiades (860 espais) i que mostri l’essència del manuscrit (introducció, material, mètodes, resultats i discussió). S'evitaran les especulacions i les cites bibliogràfiques. Estarà encapçalat pel títol del treball en cursiva.

Key words en anglès (sis com a màxim), que orientin sobre el contingut del treball en ordre d’importància.

Resumen en castellà, traducció de l'Abstract. De la traducció se'n farà càrrec la revista per a aquells autors que no siguin castellano­parlants.

Palabras clave en castellà. © 2002 Museu de Ciències Naturals

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Adreça postal de l’autor o autors.

(Títol, Nom, Abstract, Key words, Resumen, Palabras clave i Adreça postal, conformaran la primera pàgina.)

Introducción. S'hi donarà una idea dels antecedents del tema tractat, així com dels objectius del treball.

Material y métodos. Inclourà la informació pertinent de les espècies estudiades, aparells emprats, mètodes d’estudi i d’anàlisi de les dades i zona d’estudi.

Resultados. En aquesta secció es presentaran úni­ cament les dades obtingudes que no hagin estat publicades prèviament.

Discusión. Es discutiran els resultats i es compa­ raran amb treballs relacionats. Els sug­geriments de recerques futures es podran incloure al final d’aquest apartat.

Agradecimientos (optatiu).

Referencias. Cada treball haurà d’anar acompanyat de les referències bibliogràfiques citades en el text. Les referències han de presentar–se segons els models següents (mètode Harvard): * Articles de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of species richness for conservation of biological diversity: conceptual and methodological issues.

Ecological Applications, 6: 763–773. * Llibres o altres publicacions no periòdiques: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Treballs de contribució en llibres: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for con­ servation biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Tesis doctorals: Merilä, J., 1996. Genetic and quantitative trait vari­ ation in natural bird populations. Tesis doctoral, Uppsala University. * Els treballs en premsa només han d’ésser citats si han estat acceptats per a la publicació: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim.

Biodivers. Conserv.

La relació de referències bibliogràfiques d’un tre­ ball serà establerta i s’ordenarà alfabè­ticament per autors i cronològicament per a un mateix autor, afegint les lletres a, b, c..., als treballs del mateix any. En el text, s’indi­caran en la forma usual: “... segons Wemmer (1998) ... ”, “...ha estat definit per Robinson & Redford (1991)...”, “...les prospeccions realitzades (Begon et al., 1999)...” Quan en el text s’anomeni un autor de qui no es dóna referèn­cia bibliogràfica el nom anirà en rodo­na: “...un altre autor és Caughley...”

Taules. Les taules es numeraran 1, 2, 3, etc. i han de ser sempre ressenyades en el text. Les taules grans seran més estretes i llargues que amples i curtes ja que s'han d'encaixar en l'amplada de la caixa de la revista.

Figures. Tota classe d’il·lustracions (gràfics, figures o fotografies) entraran amb el nom de figura i es numeraran 1, 2, 3,... i han de ser sempre ressenya­ des en el text. Es podran incloure fotografies si són imprescindibles. La mida màxima de les figures és de 15,5 cm d'amplada per 24 cm d'alçada. S'evitaran les figures tridimensionals. Tant els mapes com els dibuixos han d'incloure l'escala. Els ombreigs preferibles són blanc, negre o trama. S'evitaran els punteigs ja que no es repro­dueixen bé.

Peus de figura i capçaleres de taula. Els peus de figura i les capçaleres de taula seran clars, concisos i bilingües en la llengua de l’article i en anglès.

Els títols dels apartats generals de l’article (Intro­ ducción, Material y métodos, Resultados, Discu­ sión, Conclusiones, Agradecimientos y Referencias) no aniran numerats. No es poden utilitzar més de tres nivells de títols.

Els autors procuraran que els seus treballs originals no passin de 20 pàgines (incloent–hi figures i taules).

Si a l'article es descriuen nous tàxons, caldrà que els tipus estiguin dipositats en una insti­tució pública.

Es recomana als autors la consulta de fascicles recents de la revista per tenir en compte les seves normes.

III

Animal Biodiversity and Conservation 25.2 (2002)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (antes Miscel·lània Zoològica) es una revista inter­ disciplinar, publicada desde 1958 por el Museo de Zoología de Barcelona. Incluye artículos de investigación empírica y teórica en todas las áreas de la zoología (sistemática, taxo­nomía, morfolo­ gía, biogeografía, ecología, etología, fisiología y genética) procedentes de todas las regiones del mundo, con especial énfasis en los estudios que de una manera u otra tengan relevancia en la biología de la conservación. La revista no publica catálogos, listas de especies sin más o citas puntuales. Los estudios realizados con especies raras o protegidas pueden no ser aceptados a no ser que los autores dispongan de los permisos correspondientes. Cada volumen anual consta de dos fascículos.

Animal Biodiversity and Conservation está registrada en todas las bases de datos importan­ tes y además está disponible gratuitamente en internet en http://www.museuzoologia.bcn.es/servis/ servis3.htm, lo que permite una difusión mundial de sus artículos.

Todos los manuscritos son revisados por el editor ejecutivo, un editor y dos revisores independientes, elegidos de una lista internacional, a fin de garan­ tizar su calidad. El proceso de revisión es rápido y constructivo, y se realiza vía correo electrónico siempre que es posible. La publicación de los trabajos aceptados se realiza con la mayor rapidez posible, normalmente dentro de los 12 meses siguientes a la recepción del trabajo.

Una vez aceptado, el trabajo pasará a ser pro­ piedad de la revista. Ésta se reserva los derechos de autor, y ninguna parte del trabajo podrá ser reproducida sin citar su procedencia.

Normas de publicación Los trabajos se enviarán preferentemente de forma electrónica (publicacionsmuseuciencies@mail.bcn. es). El formato preferido es un documento Rich Text Format (RTF) o DOC, que incluya las figuras (TIF). Si se opta por la versión impresa, deberán remitirse cuatro copias juntamente con una copia en disquete a la Secretaría de Redacción. Debe incluirse, con el artículo, una carta donde conste que el trabajo versa sobre inves­tigaciones originales no publi­cadas an­te­rior­mente y que se somete en exclusiva a Animal Biodiversity and Conservation.

En dicha carta también debe constar, para trabajos donde sea necesaria la manipulación de animales, que los autores disponen de los permisos necesarios y que han cumplido la normativa de protección animal vigente. Los autores pueden enviar también sugerencias para asesores.

Cuando el trabajo sea aceptado los autores deberán enviar a la Redacción una copia impresa de la versión final junto con un disquete del ma­ nuscrito preparado con un pro­cesador de textos e ISSN: 1578–665X

indicando el programa utilizado (preferiblemente Word). Las pruebas de imprenta enviadas a los autores deberán remitirse corregidas al Consejo Editor en el plazo máximo de 10 días. Los gastos debidos a modificaciones sustanciales en las prue­ bas de im­pren­­ta, introducidas por los autores, irán a ­cargo de los mismos.

El primer autor recibirá 50 separatas del tra­ bajo sin cargo alguno y una copia electrónica en formato PDF. Manuscritos Los trabajos se presentarán en formato DIN A–4 (30 líneas de 70 espacios cada una) a doble espa­ cio y con las páginas numeradas. Los manuscritos deben estar completos, con tablas y figuras. No enviar las figuras originales hasta que el artículo haya sido aceptado.

El texto podrá redactarse en inglés, castellano o catalán. Se sugiere a los autores que envíen sus trabajos en inglés. La revista ofre­ce, sin cargo ninguno, un servicio de corrección por parte de una persona especializada en revistas científicas.

En cualquier caso debe presentarse siempre de forma correcta y con un lenguaje claro y conciso.

La redacción del texto deberá ser impersonal, evitán­dose siempre la primera persona.

Los caracteres en cursiva se utilizarán para los nombres científicos de géneros y especies y para los neologismos que no tengan traducción; las citas textuales, independientemente de la lengua en que estén, irán en letra redonda y entre comi­ llas; el nombre del autor que sigue a un taxón se escribirá también en redonda.

Al citar por primera vez una especie en el tra­ bajo, deberá especificarse siempre que sea posible su nombre común.

Los topónimos se escribirán bien en su forma original o bien en la lengua en que esté redactado el trabajo, siguiendo el mismo criterio a lo largo de todo el artículo.

Los números del uno al nueve se escribirán con letras, a excepción de cuando precedan una unidad de medida. Los números mayores de nueve se escri­ birán con cifras excepto al empezar una frase.

Las fechas se indicarán de la siguiente forma: 28 VI 99; 28, 30 VI 99 (días 28 y 30); 28–30 VI 99 (días 28 al 30).

Se evitarán siempre las notas a pie de página.

Formato de los artículos Título. El título será conciso pero suficientemente explicativo del contenido del trabajo. Los títulos con designaciones de series numéricas (I, II, III, etc.) serán aceptados excepcionalmente previo consentimiento del editor.

Nombre del autor o autores.

Abstract en inglés de 12 líneas mecanografiadas (860 espacios como máximo) y que exprese la esencia del manuscrito (introducción, material, métodos, resultados y discusión). Se evitarán las © 2002 Museu de Ciències Naturals

IV

especulaciones y las citas bibliográficas. Irá enca­ bezado por el título del trabajo en cursiva.

Key words en inglés (un máximo de seis) que especifiquen el contenido del trabajo por orden de importancia.

Resumen en castellano, traducción del abstract. Su traducción puede ser solicitada a la revista en el caso de autores que no sean castellano hablan­tes.

Palabras clave en castellano.

Dirección postal del autor o autores.

(Título, Nombre, Abstract, Key words, Resumen, Palabras clave y Dirección postal conformarán la primera página.)

Introducción. En ella se dará una idea de los antecedentes del tema tratado, así como de los objetivos del trabajo.

Material y métodos. Incluirá la información refe­ rente a las especies estudiadas, aparatos utilizados, metodología de estudio y análisis de los datos y zona de estudio.

Resultados. En esta sección se presentarán úni­ camente los datos obtenidos que no hayan sido publicados previamente.

Discusión. Se discutirán los resultados y se compara­ rán con otros trabajos relacionados. Las sugerencias sobre investigaciones futuras se podrán incluir al final de este apartado.

Agradecimientos (optativo).

Referencias. Cada trabajo irá acompañado de una bibliografía que incluirá únicamente las publica­ ciones citadas en el texto. Las referencias deben presentarse según los modelos siguientes (método Harvard): * Artículos de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of species richness for conservation of biological diversity: conceptual and methodological issues.

Ecological Applications, 6: 763–773 * Libros y otras publicaciones no periódicas: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Trabajos de contribución en libros: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for con­ servation biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Tesis doctorales: Merilä, J., 1996. Genetic and quantitative trait vari­

ation in natural bird populations. Tesis doctoral, Uppsala University. * Los trabajos en prensa sólo se citarán si han sido aceptados para su publicación: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim.

Biodivers. Conserv.

Las referencias se ordenarán alfabética­men­te por autores, cronológicamen­te para un mismo autor y con las letras a, b, c,... para los tra­bajos de un mismo autor y año. En el texto las referencias bibliográficas se indicarán en la forma usual: "... según Wemmer (1998)...", "...ha sido definido por Robinson & Redford (1991)...", "...las prospeccio­ nes realizadas (Begon et al., 1999)..." Cuando en el texto se mencione un autor no incluido en la bibliografía el nombre irá en redonda: "...otro autor es Caughley..."

Tablas. Las tablas se numerarán 1, 2, 3, etc. y se re­ señarán todas en el texto. Las tablas grandes deben ser más estrechas y largas que anchas y cortas ya que deben ajustarse a la caja de la revista.

Figuras. Toda clase de ilustraciones (gráficas, figuras o fotografías) se considerarán figuras, se nume­ rarán 1, 2, 3, etc., y se citarán todas en el texto.

Pueden incluirse fotografías si son imprescindibles.

El tamaño máximo de las figuras es de 15,5 cm de ancho y 24 cm de alto. Deben evitarse las figuras tridimen­sionales. Tanto los mapas como los dibujos deben incluir la escala. Los sombreados preferibles son blanco, negro o trama. Deben evitarse los punteados ya que no se reproducen bien.

Pies de figura y cabeceras de tabla. Los pies de figura y cabeceras de tabla serán claros, concisos y bilingües en castellano e inglés.

Los títulos de los apartados generales del artículo (Introducción, Material y métodos, Resultados, Discusión, Agradecimientos y Referencias) no se numerarán. No utilizar más de tres niveles de títulos.

Los autores procurarán que sus trabajos originales no excedan las 20 páginas incluidas figuras y tablas.

Si en el artículo se describen nuevos taxones, es imprescindible que los tipos estén depositados en alguna institución pública.

Se recomienda a los autores la consulta de fascículos recientes de la revista para seguir sus directrices.

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Animal Biodiversity and Conservation 25.2 (2002)

Animal Biodiversity and Conservation

Manuscripts

Animal Biodiversity and Conservation (formerly Miscel·lània Zoològica) is an inter­­dis­ci­pli­nary journal which has been published by the Zoolo­ gical Museum of Bar­celona since 1958. It includes empirical and theoretical research in all aspects of Zoology (Systematics, Taxo­nomy, Morphology, Bio­geography, Ecology, Etho­logy, Physio­logy and Genetics) from all over the world with special emphasis on studies that stress the relevance of the study of Conservation Biology. The journal does not publish catalogues, lists of species (with no other relevance) or punctual records. Studies about rare or protected species will not be accepted unless the authors have been granted all the relevant permits. Each annual volume consists of two issues.

Animal Biodiversity and Conservation is registered in all principal data bases and is freely available on­ line at http://www.museuzoologia.bcn.es /servis/ABCag. htm, thus assuring world–wide access to articles published therein.

All manuscripts are screened by the Executive Edi­ tor, an Editor and two independent reviewers in order to guarantee the quality of the papers. The process of review is rapid and constructive. Once accepted, papers are published as soon as practicable, usually within 12 months of initial submission.

Upon acceptance, manuscripts become the prop­ erty of the journal, which reserves copyright, and no published material may be reproduced without quoting its origin.

Manuscripts must be presented on A–4 format page (30 lines of 70 spaces each) with double spacing.

Number all pages. Manuscripts should be complete with figures and tables. Do not send original figures until the paper has been accepted.

The text may be written in English, Spanish or Catalan. Authors are encouraged to send their con­ tributions in English. The journal provides a FREE service of correction by a professional translator specialized in scientific publications. Care should be taken in using correct wording and the text should be written concisely and clearly. Wording should be impersonal, avoiding the use of the first person.

Italics must be used for scientific names of genera and species as well as untrans­latable neologisms.

Quotations in whatever language used must be typed in ordinary print between quotation marks.

The name of the author following a taxon should also be written in small print.

The common name of the species should be written in capital letters. When referring to a spe­ cies for the first time in the text, both common and scientific names must be given when possible.

Place names may appear either in their origi­ nal form or in the language of the manuscript, but care should be taken to use the same criteria throughout the text.

Numbers one to nine should be written in full in the text except when preceding a measure. Higher numbers should be written in numerals except at the beginning of a sentence.

Dates must appear as follows: 28 VI 99, 28,30 VI 99 (days 28th and 30th), 28–30 VI 99 (days 28th to 30th).

Footnotes should not be used.

Information for authors Electronic submission of papers is encouraged (publi­ cacionsmuseuciencies@mail.bcn.es). The preferred format is a document Rich Text Format (RTF) or DOC, including figures (TIF). In the case of sending a printed version, four copies should be sent together with a copy on a computer disc to the Editorial Office. A cover letter stating that the article reports on original research not published elsewhere and that it has been submitted exclusively for consi­ deration in Animal Biodiversity and Conservation is also necessary. When animal manipulation has been necessary, the cover letter should also es­ pecify that the authors follow current norms on the protection of animal species and that they have obtained all relevant permissions. Authors may suggest referees for their papers.

Once an article has been accepted, authors should send a printed copy of the final version together with a disc. Please identify software (preferably Word).

Proofs sent to the authors for correction should be returned to the Editorial Board within 10 days.

Expenses due to any substantial alterations of the proofs will be charged to the authors.

The first author will receive 50 reprints free of charge and an electronic version of the article in PDF format.

ISSN: 1578–665X

Formatting of articles Title. The title must be concise but as infor­mative as possible. Part numbers (I, II, III,...) should be avoided and will be subject to the Editor’s consent.

Name of author or authors.

Abstract in English, no longer than 12 type­written lines (840 spaces), covering the con­tents of the article (introduction, material, methods, results and discussion). Speculation and literature citation must be avoided. Abstract should begin with the title in italics.

Key words in English (no more than six) should express the precise contents of the manuscript in order of importance.

Resumen in Spanish, translation of the Abstract.

Summaries of articles by non­–Spanish speaking au­ thors will be trans­lated by the journal on request.

Palabras clave in Spanish.

Address of the author or authors.

(Title, Name, Abstract, Key words, Resumen, Palabras clave and Address should constitute the first page.)

Introduction. The introduction should in­clude the historical background of the sub­ject as well as the © 2002 Museu de Ciències Naturals

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aims of the paper.

Material and methods. This section should provide relevant information on the species studied, ma­ terials, methods for collecting and analysing data and the study area.

Results. Report only previously unpublished results from the present study.

Discussion. The results and their comparison with related studies should be discussed. Sug­gestions for future research may be given at the end of this section.

Acknowledgements (optional).

References. All manuscripts must include a bi­ bliography of the publications cited in the text.

References should be presented as in the following examples (Harvard method): * Journal articles: Conroy, M. J. & Noon, B. R., 1996. Mapping of species richness for conservation of biological diversity: conceptual and methodological issues.

Ecological Applications, 6: 763–773. * Books or other non–periodical publications: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Contributions or chapters of books: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for con­ servation biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Ph. D. Thesis: Merilä, J., 1996. Genetic and quantitative trait vari­ ation in natural bird populations. Ph. D. Thesis, Uppsala University. * Works in press should only be cited if they have been accepted for publication: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim.

Biodivers. Conserv.

References must be set out in alphabetical and chronological order for each author, add­

ing the letters a, b, c,... to papers of the same year. Biblio­graphic citations in the text must appear in the usual way: "...according to Wemmer (1998)...", "...has been defined by Robinson & Redford (1991)...", "...the pros­pec­tions that have been carried out (Begon et al., 1999)..." When an author is men­tioned in the text but no biblio­ graphical re­ference is given, the name must appear in ordinary print: "...another of these authors is Caughley..."

Tables. Tables must be numbered in Arabic nu­ merals with reference in the text. Large tables should be narrow (across the page) and long (down the page) rather than wide and short, so that they can be fitted into the column width of the journal.

Figures. All illustrations (graphs, drawings or photographs) must be termed as figures, num­ bered consecutively in Arabic numerals and with re­ference in the text. Glossy print photographs, if essential, may be included. Maximum size of figures is 15.5 cm width and 24 cm height. Figures will not be tridimen­sional. Both maps and drawings must include scale. The preferred shadings are white, black and bold hatching. Avoid stippling, which does not reproduce well.

Legends of tables and figures. Legends of tables and figures must be clear, concise, and written both in English and Spanish.

Main headings (Introduction, Material and methods, Results, Discussion, Acknowled­ge­ments and Refe­ rences) should not be number­ed. Do not use more than three levels of headings.

Manuscripts should not exceed 20 pages inclu­ ding figures and tables.

If the article describes new taxa, type material must be deposited in a public institution.

Authors are advised to consult recent issues of the journal and follow its conventions.

Animal Biodiversity and Conservation 25.2 (2002)

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Les cites o els abstracts dels articles d’Animal Biodiversity and Conservation es resenyen a / Las citas o los abstracts de los artículos de Animal Biodiversity and Conservation se mencionan en / Animal Biodiversity and Conservation is cited or abstracted in: Abstracts of Entomology, Agrindex, Animal Behaviour Abstracts, Anthropos, Aquatic Sciences and Fisheries Abstracts, Behavioural Biology Abstracts, Biological Abstracts, Biological and Agricultural Abstracts, Current Primate References, Ecological Abstracts, Ecology Abstracts, Entomology Abstracts, Environmental Abstracts, Environmental Periodical Bibliography, Genetic Abstracts, Geographical Abstracts, Índice Español de Ciencia y Tecnología, International Abstracts of Biological Sciences, International Bibliography of Periodical Literature, International Developmental Abstracts, Marine Sciences Contents Tables, Oceanic Abstracts, Recent Ornithological Literature, Referatirnyi Zhurnal, Science Abstracts, Serials Directory, Ulrich’s International Periodical Directory, Zoological Records.

ISSN 1578–665X

Animal Biodiversity and Conservation 25.2 (2002)

Índex / Índice / Contents

1–5 Deharveng, L. & Smolis, A. Pronura bidoup n. sp. (Collembola, Neanuridae, Neanurinae, Paleonurini) from southern Vietnam 7–45 Fowler, C. W. & Hobbs, L. Review Limits to natural variation: implications for systemic management 47–51 Martínez–Abrain, A., Oro, D., Ferris, V. & Belenguer, R. Is growing tourist activity affecting the distribution or number of breeding pairs in a small colony of the Eleonora’s Falcon?

53–66 Nekola, J. C. Review Effects of fire management on the richness and abundance of central North American grassland land snail faunas

67–74 Ranius, T. & Douwes, P. Genetic structure of two pseudoscorpion species living in tree hollows in Sweden 75–93 Sanmartín, I. & Ronquist, F. New solutions to old problems: widespread taxa, redundant distributions and missing areas in event–based biogeography 95–99 VivesH, J., Escolà, O. & Vives, E. Dos nuevas especies de Anillini cavernícolas pertenecientes al género Speleotyphlus Jeanne, 1973 (Coleoptera, Carabidae)