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SEASONAL, ANNUAL, AND LONG‐TERM TRENDS IN COMMERCIAL FISHERIES FOR AGGREGATING REEF FISHES IN THE GULF OF CALIFORNIA, MEXICO

BRAD ERISMAN, ISMAEL MASCAREÑAS‐OSORIO, GUSTAVO PAREDES, YVONNE SADOVY DE MITCHESON, OCTAVIO ABURTO‐OROPEZA, PHILIP HASTINGS

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Fisheries Research 106 (2010) 279–288

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Seasonal, annual, and long-term trends in commercial fisheries for aggregating reef fishes in the Gulf of California, Mexico Brad Erisman a,∗ , Ismael Mascarenas b , Gustavo Paredes a , Yvonne Sadovy de Mitcheson c , Octavio Aburto-Oropeza a , Philip Hastings a a b c

Marine Biology Research Division, Scripps Institution of Oceanography, University of California at San Diego, La Jolla, CA 92093-0202, USA Centro de la Biodiversidad Marina y la Conservacion, La Paz, Baja California Sur, Mexico Swire Institute of Marine Science, Department of Ecology & Biodiversity, University of Hong Kong, Hong Kong

a r t i c l e

i n f o

Article history: Received 11 June 2010 Received in revised form 15 August 2010 Accepted 16 August 2010 Keywords: Fish spawning aggregations Gulf of California Reef fishes Artisanal fisheries

a b s t r a c t In order to assess the contribution of fish spawning aggregations and aggregating species to commercial marine fisheries in the Gulf of California, we: (1) investigated associations between the timing of spawning aggregations and monthly trends in commercial landings and ex-vessel revenues for aggregating reef fishes in the southwest Gulf of California and (2) compared present (2000–2005) and past (1956–1961) landings of aggregating species groups from the entire Gulf. Species known to form seasonal spawning aggregations comprised the eight most important commercial reef fish fisheries of the southwest Gulf with respect to landings and ex-vessel revenues, and three of these species increased in annual landings between 1999 and 2007. Peaks in mean monthly landings and revenues for five of eight aggregating species coincided with the timing of their spawning aggregations, whereas commercial fisheries for the remaining three species did not specifically target spawning aggregation periods. Comparisons of past and present landings showed an expansion of targeted species groups, increased landings for most aggregating species groups, and declines in the landings of several large-bodied species groups. Our results suggest that targeted management of spawning aggregations is needed for some but not all species, assessments on the interaction between fisheries and spawning aggregations are needed for most species, and restrictions on certain gear types are necessary to create sustainable fisheries for aggregating fishes in the Gulf. © 2010 Elsevier B.V. All rights reserved.

1. Introduction Many marine fishes form spawning aggregations, temporally and spatially discrete gatherings that are solely for the purpose of reproduction (Colin et al., 2003). Commercial fisheries often target these aggregations, since they tend to occur at the same locations and times each year and thus provide easy opportunities for large harvests with minimal effort (Sadovy and Domeier, 2005a). However, such predictability in time and space also makes fish spawning aggregations particularly vulnerable to overexploitation (Sadovy de Mitcheson and Erisman, 2010), which likely explains why 79% of documented aggregation sites in the tropics have declined (Sadovy

∗ Corresponding author at: Marine Biology Research Division, Scripps Institution of Oceanography, University of California at San Diego, 9500 Gilman Drive, Mail Code 0202, La Jolla, CA 92093-0202, USA. Tel.: +1 858 822 3765; fax: +1 858 822 3310.

E-mail addresses: berisman@ucsd.edu (B. Erisman), otolino@gmail.com (I. Mascarenas), gparedes@ucsd.edu (G. Paredes), yjsadovy@hkucc.hku.hk (Y. Sadovy de Mitcheson), maburto@ucsd.edu (O. Aburto-Oropeza), phastings@ucsd.edu (P. Hastings).

0165-7836/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2010.08.007

de Mitcheson et al., 2008). The lack of specific fisheries and biological information for aggregating species (i.e., those species that form spawning aggregations) in most areas, including quantitative information on the importance of aggregations to fisheries, locations of major spawning sites, seasonal timing of aggregations, or direct effects of fishing on aggregations seriously compromises our ability to make compelling arguments for the management of aggregating species using strategies that specifically target aggregation sites or time periods (Sadovy de Mitcheson and Erisman, 2010; Sadovy de Mitcheson et al., 2008).

The Gulf of California is one of the most important fisheries regions of the Tropical Eastern Pacific and the most productive fisheries region in Mexico (OECD, 2006). A large portion of this productivity stems from the commercial harvest of groupers, snappers, croakers, jacks and other coastal marine fishes that form spawning aggregations at specific sites during certain seasons (AburtoOropeza et al., 2008; Erisman et al., 2007; Román-Rodríguez, 2000; Sala et al., 2003). Persistent overfishing in the Gulf over the past three decades has decimated coastal fish populations and their associated fisheries (DOF, 2004; Ezcurra et al., 2009; McGoodwin, 1979; Sala et al., 2004). As part of this trend, targeted exploitation

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Table 1 Aggregating reef fishes of commercial importance in the southwest Gulf of California, their spawning seasons within the region, and references documenting their spawning and aggregating behavior.

Species

Spawning season

References

Balistes polylepis Hoplopagrus guentherii Lutjanus argentiventris Lutjanus peru Mycteroperca rosacea Paralabrax auroguttatus Paranthias colonus Seriola lalandi

May–September May–September May–September May–September March–June March–May May–September March–May

˜ Thomson et al. (2000), Avendano-Ibarra et al. (2004), Sánchez-Velasco et al. (2009) Thomson et al. (2000), Zapata and Herrón (2002) ˜ Sala et al. (2003), Aburto-Oropeza et al. (2009), Pinon et al. (2009) Dumas et al. (2004), Reyna-Trujillo (1993) Aburto-Oropeza et al. (2007a), Erisman et al. (2007), Sala et al. (2003) Pondella et al. (2001), Sadovy and Domeier (2005b), Erisman (unpublished data) Sala et al. (2003), Erisman and Aburto-Oropeza (unpublished data) Sala et al. (2003), Erisman (unpublished data)

of important spawning aggregation sites for several large-bodied species has contributed to the collapse of their fisheries, and these species are now endangered (Cisneros-Mata et al., 1995; Musick et al., 2000; Sáenz-Arroyo et al., 2005a; Sala et al., 2004). Despite such pervasive and dramatic declines and known interactions between fisheries and spawning aggregations, neither quantitative evaluations of the importance of spawning aggregations to fisheries nor the impacts of fisheries on these aggregations have been evaluated in the Gulf. As a result, only one aggregating species is protected from commercial harvest (totoaba; Totoaba macdonaldi), and the management of only one commercial species (Gulf corvina; Cynoscion othonopterus) includes any protection of its spawning season and spawning aggregation sites (Cisneros-Mata et al., 1995; Román-Rodríguez, 2000).

Here we evaluate the current contribution of fish spawning aggregations and aggregating species to commercial reef fisheries in the southwest Gulf of California and summarize annual and seasonal trends in landings and markets for aggregating species in the region. We also compare annual landings of fisheries for aggregating species in the entire Gulf during the 1950s with those during the period of 2000–2005 to identify long-term fisheries trends. Finally, we provide general recommendations for the management and research of fish spawning aggregations and associated fisheries in the region.

was used to confirm the existence of spawning aggregations for each of these eight species and to identify the months during which spawning aggregations occur (Table 1). We estimated the contribution of spawning aggregations to fisheries for each of the eight species by summing the landings recorded during spawning months and dividing these values by the total annual landings.

Based on prior research on the reproductive behavior of these species (see references listed in Table 1), we assumed that spawning aggregations persisted throughout the reproductive season rather than being limited to specific periods (e.g., full or new moons). We multiplied landings recorded during spawning months by monthly ex-vessel prices to estimate ex-vessel revenues from spawning aggregations.

A one-way ANOVA tested for differences in landings and exvessel prices among months. Where significant relationships were found, post hoc multiple comparisons were performed using Tukey tests. Monthly landings data were log transformed, because raw data did not conform to the assumptions of parametric testing.

Because mean monthly ex-vessel price did not differ significantly among months for any species (see Section 3.2), we used linear correlation to confirm that monthly trends in landings and ex-vessel revenue were not significantly different.

2. Materials and methods

A quantitative analysis of long-term trends in commercial fisheries for aggregating species of the entire Gulf was not possible, because official fisheries landings data for the Gulf of California are inconsistent across years and regions, long-term databases for the entire Gulf that record species-specific data do not exist, and data for most years are not available in electronic formats (Aburto-Oropeza et al., 2007b). Therefore, we relied on two databases that allowed general comparisons between species composition and mean annual landings of fisheries for aggregating species of the entire Gulf during the 1950s and 2000s.

The first database was published by the Mexican Navy and included annual landings data of marine species groups from the entire Gulf of California from 1956 to 1961. The second database was obtained from CONAPESCA and contained annual landings for marine species groups from the entire Gulf from 2000 to 2005.

Species groups for both databases were classified by regional common name, which varied considerably in taxonomic specificity from a single species (e.g., huachinango = Lutjanus peru) to a suite of species from the same family (e.g., cochito = Balistes polylepis, Pseudobalistes naufragium) or order (e.g., mantaraya = Myliobatiformes). Fisher interviews, market surveys, personal knowledge of the authors, online databases (www.fishbase.org; www.neotropicalfishes.org), and published reference materials were used to identify individual species associated with regional common names (Allen and Robertson, 1994; Fischer et al., 1995; Humann and DeLoach, 2004; Thomson et al., 2000).

2.1. Monthly and annual trends in commercial reef fish fisheries of the southwest Gulf of California We acquired commercial fisheries data directly from three local fisheries offices (Santa Rosalia, Loreto, La Paz; Fig. 1) of the Mexican National Commission of Fisheries and Aquaculture (CONAPESCA) in the state of Baja California Sur and compiled them into electronic formats. These data contained monthly records of landings (kg) and ex-vessel prices (pesos/kg), classified to the level of species, for all months from 1999 to 2007. Data prior to 1999 were either unavailable, incomplete in terms of lacking data for some months, or did not contain species level data. Calculations of fishing effort or catch-per-unit effort were not possible, because commercial fishers are not required to submit detailed daily logs of fishing activities. Despite the shortcomings, these data provided much higher taxonomic (i.e., species level) and temporal resolution (i.e., monthly) than fisheries data available at the central CONAPESCA office in Mazatlán, Sinaloa, Mexico (see Section 2.2).

Ex-vessel revenues were calculated by multiplying landings by ex-vessel prices, and the resulting values in Mexican pesos were then converted to US dollars using published monetary exchange rates.

We identified the eight most important commercial reef fishes known to form spawning aggregations based on mean annual landings and ex-vessel revenues (see Section 3.1). A combination of published data, unpublished data, and observations by the authors

2.2. Long-term fisheries trends for aggregating fishes of the Gulf of California

B. Erisman et al. / Fisheries Research 106 (2010) 279–288

281

Fig. 1. Map of Gulf of California, showing the location of three fisheries offices from southern Gulf (Santa Rosalia, Loreto, La Paz).

The analysis focused primarily on reef fishes reported or observed to form spawning aggregations; however, commercially important coastal species groups that inhabit nearshore, softbottom habitats (e.g., corvina, mullet) or coastal pelagic groups often observed on reefs (e.g., bonito, sierra) and have been reported or observed to form spawning aggregations in the Gulf or elsewhere were also included. Only one significant change in the management of artisanal finfish fisheries in the Gulf occurred between 1950 and 2005, the closure of the totoaba (T. macdonaldi) fishery. Therefore, we assumed that differences in landings among the two time periods were not affected significantly by management policy changes during the study period, except for T. macdonaldi.

3. Results 3.1. Contribution of aggregating species to commercial fisheries of the southwest Gulf Twenty-nine species of reef fishes were reported in the commercial fisheries landings of the southwest Gulf of California from 1999 to 2007, and 21 are known or reported to form spawning aggregations (Table 2). The top eight species all form spawning aggregations and comprised ca. 90% of the total commercial landings and total ex-vessel revenue for reef fish fisheries in the region during that period. Five of these species aggregate and spawn in the

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Table 2 Reef fish species recorded in commercial landings of southwest Gulf of California from 1999 to 2007, organized by landings and ex-vessel revenues.

Species *

Lutjanus peru Seriola lalandi* Lutjanus argentiventris* Mycteroperca rosacea* Paralabrax auroguttatus* Balistes polylepis* Hoplopagrus guentherii* Paranthias colonus* Epinephelus niphobles Lutjanus guttatus* Anisotremus interruptus* Haemulon sexfasciatum* Epinephelus acanthistius Gnathanodon speciosus* Mycteroperca xenarcha* Lutjanus jordani* Menticirrhus spp.

Lutjanus spp.

Microlepidotus inornatus* Epinephelus analogus Epinephelus spp.

Caranx caninus* Lutjanus novemfasciatus* Epinephelus labriformis Paralabrax maculatofasciatus* Lutjanus colorado Mycteroperca jordani* Sufflamen verres* Lutjanus aratus* *

Mean annual landings (tons)

Total landings (%)

Mean annual revenue (USD)

Total revenue (%)

598.49 338.45 156.43 147.37 110.32 99.23 83.45 51.81 40.18 24.93 24.54 21.49 20.33 16.14 9.70 9.61 4.55 4.25 3.67 3.29 1.27 0.66 0.59 0.19 0.18 0.03 0.03 0.03 0.02

33.79 19.11 8.81 8.32 6.23 5.60 4.71 2.93 2.27 1.41 1.39 1.21 1.15 0.91 0.55 0.54 0.26 0.24 0.21 0.19 0.07 0.04 0.03 0.01 0.01 <0.01 <0.01 <0.01 <0.01

$1,135,302 $291,823 $212,710 $281,983 $76,842 $56,273 $113,292 $39,718 $84,705 $33,307 $10,349 $10,582 $33,759 $8170 $19,699 $11,343 $2476 $22,800 $1614 $2695 $2919 $197 $879 $432 $336 $52 $60 $26 $19

46.26 11.89 8.67 11.49 3.13 2.29 4.62 1.62 3.45 1.36 0.42 0.43 1.38 0.33 0.80 0.46 0.10 0.93 0.07 0.11 0.12 0.01 0.04 0.02 0.01 <0.01 <0.01 <0.01 <0.01

Indicates species reported to form spawning aggregations.

summer (Mayâ&#x20AC;&#x201C;September), and three species spawn in the spring (Marchâ&#x20AC;&#x201C;June; Table 1). The fisheries landings of these eight aggregating species equated to 1585.5 tons in mean annual landings and $2,207,942 USD in mean annual ex-vessel revenue. Of these totals, means of 582 tons and $740,111 USD in annual ex-vessel revenue were generated during the spawning aggregation periods (Table 3).

The proportion of mean annual landings harvested during aggregation periods ranged from 17.0% to 61.3% (mean = 45.0%) per species, and the proportion of ex-vessel revenue from aggregation periods ranged from 18.1% to 59.9% (mean = 45.0%) per species.

3.2. Seasonal and annual trends in landings of aggregating species in the southwest Gulf Landings for L. peru, Seriola lalandi, Lutjanus argentiventris, Mycteroperca rosacea and Paralabrax auroguttatus varied among years (Fig. 2) and showed no directional trends. However, annual landings did increase over the study period for B. polylepis, Hoplopagrus guentherii, and Paranthias colonus. Five aggregating species showed significant differences in monthly landings, in which peak landings coincided with part or all of the spawning season (Fig. 3). Landings for B. polylepis were significantly higher from May to August

than during other months (F = 8.603, p < 0.01). Landings for L. argentiventris were highest during May and June (F = 3.876; p < 0.001), and M. rosacea landings peaked from March to May (F = 13.870, p < 0.001). Landings for P. auroguttatus peaked during March and April (F = 5.235, p < 0.001), and S. lalandi landings were highest from March to May (F = 6.982, p < 0.001).

Three species showed no clear relationship between monthly landings and the spawning season. Landings for L. peru (F = 1.657, p = 0.095) and H. guentherii (F = 1.387, p = 0.191) fluctuated throughout the year, and landings for P. colonus were highest in April (F = 2.192; p = 0.021) with a second, lesser peak in October (p > 0.05).

Mean monthly ex-vessel price did not differ significantly among months for any species (p > 0.5). Consequently, mean monthly exvessel revenue followed the same trend as mean monthly landings for all species (r2 > 0.45; p < 0.001).

3.3. Long-term fisheries trends for aggregating fishes of the entire Gulf Eighteen species groups of aggregating fishes from 14 different families were recorded in commercial landings from 1956 to 1961, but only 9 groups were recorded with mean annual land-

Table 3 Contribution of spawning aggregations to commercial landings and ex-vessel revenue for the eight most important reef fishes in the southwest Gulf of California from 1999 to 2007.

Species

Mean annual landings from aggregations (tons)

% of annual landings from aggregations

Mean annual revenue from aggregations (USD)

% of annual revenue from aggregations

Lutjanus peru Seriola lalandi Lutjanus argentiventris Mycteroperca rosacea Paralabrax auroguttatus Balistes polylepis Hoplopagrus guentherii Paranthias colonus

101.5 149.8 83.5 81.6 42.5 60.8 39.9 22.3

17.0 44.0 53.4 55.4 38.1 61.3 47.8 43.0

$205,490 $135,406 $109,758 $156,500 $30,045 $33,708 $51,888 $17,317

18.1 46.4 51.6 55.5 39.1 59.9 45.8 43.6

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B. Erisman et al. / Fisheries Research 106 (2010) 279–288 Table 4 Comparison of mean annual landings for aggregating fishes in the Gulf of California between 1956–1961 and 2000–2005.

Family

Group

Principal species

Balistidae Carangidae

Triggerfishes Jacks

Carangidae Carangidae Epinephelidae; Serranidae

Palometa Pampanos Small Groupers and Seabasses

Epinephelidae; Polyprionidae

Large Groupers and Seabasses

Gerreidae

Mojarras

Haemulidae

Grunts

Kyphosidae

Chubs

Lutjanidae Lutjanidae

Red Snapper Snappers

Mobulidae; Myliobatidae; Rhinopteridae Mugilidae Mullidae

Myliobatiform Rays*

Rhinobatidae Scaridae Sciaenidae

Guitarfishes* Parrotfishes Corvinas*

Sciaenidae Sciaenidae Sciaenidae Scombridae Scombridae Sphyraenidae Tetraodontidae

Croakers* Totoaba* White Seabass Bonitos Sierra Barracudas Pufferfishes

Balistes polylepis, Pseudobalistes naufragium Caranx caballus, Caranx sexfasciatus, Seriola lalandi Gnathanodon speciosus Trachinotus kennedyi, T. paitensis, T. rhodopus Mycteroperca prionura, M. rosacea, Paralabrax auroguttatus, Paranthias colonus Epinephelus itajara, Mycteroperca jordani, M. xenarcha, Stereolepis gigas Diapterus peruvianus, Eucinostomus dowii, Gerres cinereus Anisotremus interruptus, Orthopristis spp., Haemulon spp., Haemulopsis leuciscus, Microlepidotus spp., Pomadasys branickii Girella simplicidens, Kyphosus analogus, K. elegans Lutjanus peru Hoplopagrus guentherii, Lutjanus aratus, L. argentiventris, L. guttatus, L. novemfasciatus Manta birostris, Myliobatus longirostris, Mobula spp., Rhinoptera steindachnerii Mugil cephalus, M. curema Mulloidichthys dentatus, Pseudupeneus grandisquamis Rhinobatus productus, Zapteryx exasperata Scarus compressus, S. ghobban, S. perrico Cynoscion othonopterus, C. parvipinnis, C. reticulatus Micropogonias megalops, M. altipinnis Totoaba macdonaldi Atractoscion nobilis Sarda chiliensis, S. orientalis Scomberomorus sierra Sphyraena argentea, S. ensis, S. lucasana Sphoeroides annulatus, S. lobatus

Mullets* Goatfishes

Mean landings (tons) 1956–1961

2000–2005

Trend

0 168

647 778

+ +

12 1 266

28 333 469

+ + +

198

47

−

134

496

+

0

445

+

2

15

+

9 210

911 516

+ +

2

868

+

873 0

1921 323

+ +

0 3 1177

578 46 1300

+ + =

0 466 15 24 433 1 0

1600 0 17 14 2583 9 234

+ − = − + + +

+ Indicates an increase in landings; − indicates a decrease in landings; = indicates no change in landings; * indicates species groups not associated directly with reefs.

ings greater than 100 tons (Table 4). Conversely, 23 groups from 19 families were recorded in commercial landings from 2000 to 2005, and 16 groups were recorded with landings greater than 100 tons. Eighteen groups recorded landings during both the 1950s and the 2000s. Six groups (jacks, pampanos, red snapper, myliobatiform rays, parrotfishes, sierra) recorded landings that were markedly higher during the 2000s than in the 1950s, and the landings for one group (large groupers and seabasses) was considerably lower in the present than in the past. Six groups that are currently exploited (triggerfishes, grunts, goatfishes, guitarfishes, croakers, and pufferfishes) did not record landings in the past, while one group caught in the past (totoaba) is no longer recorded because the fishery has been closed (see Section 4.2).

4. Discussion 4.1. Contribution of spawning aggregations and aggregating species to commercial fisheries in the southwest Gulf of California Spawning aggregations and aggregating species in general make a significant contribution to commercial reef fish fisheries of the southwest Gulf of California, both in terms of production and revenue (this study; Arreguín-Sánchez et al., 2004; Díaz-Uribe et al., 2006). The eight most commercially important reef fishes form spawning aggregations, most of which are heavily exploited and generate peak landings and revenues for fishers. Moreover, nearly half of the total annual landings of these aggregating species are taken during the months in which spawning aggregations

occur, representing more than 580 tons in landings and more than $740,000 USD in ex-vessel revenue.

Aggregating reef fishes worldwide are harvested largely during their spawning aggregation periods, one of the few times that fish are gathered in numbers large enough for fishing to be profitable (Sadovy and Domeier, 2005a). Although commercial fishing activities in the southwest Gulf of California also focus on spawning aggregations, substantial landings of several aggregating species are recorded in the region throughout the year (this study; Díaz-Uribe et al., 2006), which could be related to several factors. First, several aggregating species in the region have prolonged reproductive seasons (e.g., May–September), and their spawning aggregations often persist throughout the reproductive season rather than being limited by certain lunar phases (Erisman et al., 2007; Sala et al., 2004). Second, certain species also form aggregations to feed (Aburto-Oropeza et al., 2008; Erisman et al., 2007). For example, P. colonus forms aggregations of several hundred individuals above reefs during the spring and fall to feed on the large plumes of zooplankton, at which time they are harvested in large numbers by artisanal gill net fisheries (Heemstra and Randall, 1993; Díaz-Uribe et al., 2006).

Spawning aggregations of certain reef fishes are not the main target of commercial fisheries in the Gulf of California. The commercial fishery for L. peru, the most productive and valuable reef fish fishery of the southwest Gulf, occurs year round and targets mainly juveniles of less than 40 cm and 3 years of age (Díaz-Uribe et al., 2004). These “plate-size” fish are highly prized as restaurant fare, particularly in tourist destinations. Although the highest landings

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Fig. 2. Annual commercial landings for eight species of aggregating reef fishes in the southwest Gulf of California from 1999 to 2007.

of H. guentherii occur during their summer spawning aggregation period, landings are relatively consistent throughout the year. In the southwest Gulf, juveniles are harvested in large numbers from mangroves, and similar to L. peru, are served as whole fish at local tourist restaurants. Finally, most reef fish fisheries in the southern Gulf are multi-species fisheries that utilize gill nets and nighttime spearfishing (Arreguín-Sánchez et al., 2004; Lluch-Cota et al., 2007).

These fishing methods are effective even when fish are more dispersed, allowing fishers to harvest large catches with minimal effort (Gillet and Moy, 2006).

4.2. Long-term changes and Gulf-wide trends The absence of a continuous, species-specific landings database for commercial fisheries of the entire Gulf of California prevented detailed evaluations of long-term trends in landings of aggregating species. However, the data we compiled did provide a means

to compare the relative importance of aggregating species groups to commercial fisheries of the past and present. Several aggregating species groups such as small and large groupers, corvinas, and snappers have supported commercial fisheries for over a half a century (Arvizu-Martinez, 1987; Cisneros-Mata, 2010). However, current fisheries appear to target a much wider variety of reef fishes than in the past, including several lower-trophic level species that were not targeted 50 years ago. For example, grunts (e.g., Microlepidotus, Anisotremus spp.) and chubs (e.g., Kyphosus spp.) ranked among the most important finfishes, both by abundance and biomass, landed by artisanal fisheries in the southeast Gulf during the late 1990s (Rojo-Vázquez et al., 2001). Pufferfishes (Sphoeroides spp.) now support a growing export market to Asia and suffer heavy by-catch mortality by the shrimp fishery (Amezcua et al., 2006; Chávez Sánchez et al., 2008). Finally, triggerfishes (e.g., B. polylepis) and sierra (Scomberomorus sierra) have become one of the most important reef fish fisheries in the Gulf in recent years

B. Erisman et al. / Fisheries Research 106 (2010) 279â&#x20AC;&#x201C;288

285

Fig. 3. Mean monthly commercial landings for eight aggregating species in southwest Gulf of California from 1999 to 2007. Lines indicate SE. Grey bars represent months that recorded peak landings identified by Tukey post hoc tests. Red horizontal bars indicate reported spawning seasons within the Gulf. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

(this study; Arvizu-Martinez, 1987; Cisneros-Mata, 2010; Sala et al., 2004). Overall, the increased diversity and quantities of commercial landings for aggregating fishes in the Gulf of California reported in this study are consistent with the dramatic growth in commercial marine fisheries that took place in the Gulf of California during the 1970s and 1980s (Arvizu-Martinez, 1987; Sala et al., 2004).

Fisheries for several large-bodied, aggregating fishes have declined or collapsed since the 1950s. The fishery for totoaba (T. macdonaldi), a large sciaenid endemic to the Gulf of California, yielded several thousand tons each year largely from the seasonal spawning aggregations that occurred along the coastlines of the northern Gulf from the 1930s to the early 1970s. The stock completely collapsed in the mid 1970s primarily due to overfishing, although the decline was also correlated to the cessation of

Colorado River flow and changes in the Pacific Decadal Oscillation Index (Lercari and ChĂĄvez, 2007; IUCN Redlist, 2010). The species is now restricted from commercial and recreational harvest in Mexico, is listed as critically endangered by the International Union for the Conservation of Nature (IUCN), and is regulated as an endangered species by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) (Cisneros-Mata et al., 1995; IUCN Redlist, 2010; Musick et al., 2000).

Fisheries for most large-bodied groupers and seabasses (Epinephelidae, Polyprionidae) have also collapsed, with several species currently listed as endangered by the American Fisheries Society (AFS) and the IUCN (e.g., Mycteroperca jordani, Mycteroperca xenarcha, Stereolepis gigas, Epinephelus itajara: Musick et al., 2000; IUCN Redlist, 2010). The Gulf grouper (M. jordani) comprised

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the main target for commercial reef fish fisheries throughout the central and southern Gulf during the 1950s through the 1970s, when one panga (small fishing boat) could harvest several hundred tons per month from a single aggregation site (Sáenz-Arroyo et al., 2005a,b). The fishery has since collapsed in most areas, and remaining landings are comprised almost entirely of juveniles (Aburto-Oropeza et al., 2008). Similarly, regional aggregation fisheries for the Goliath grouper (E. itajara) emerged in the 1970s but collapsed within a decade, and the species is now likely biologically extinct in the Gulf (Aburto-Oropeza, unpublished data; Sala et al., 2004).

The pattern known as “fishing down the food web” is the sequential replacement of high-trophic-level species with lessvaluable lower-trophic level species as the former are harvested to economic extinction (Pauly et al., 1998), although it can also occur through the serial addition of lower-trophic level species while fisheries for high-trophic-level species are maintained (i.e., “fishing through the food web”; Essington et al., 2006). Both trends are perceived as symptoms of overfishing associated with decreases in the mean trophic levels of fisheries landings and declines in the structure, function, and health of marine ecosystems. Our data provide qualitative support for both fishing down and fishing through marine food webs in the Gulf of California, but there are insufficient species-specific landings data to estimate changes in mean trophic levels quantitatively. Still, our results are consistent with those by Sala et al. (2004), who used information from interviews with fishers, fisheries statistics, and field surveys to demonstrate that coastal food webs in the Gulf of California have been “fished down” during the last 30 years and the maximum individual length of the landings has decreased ca. 45 cm in 20 years.

Although this study and most other studies on spawning aggregations focus on reef fishes, spawning aggregations of several non-reef fishes are also important to commercial fisheries of the Gulf of California. Manta rays (Manta birostris), mobula rays (Mobula spp.) and cownose rays (Rhinoptera steindachneri) mate in the summer within large aggregations, when peak landings occur (Bizzaro et al., 2007; Márquez-Farías, 2002; Notarbartolo-Di-Sciara, 1987). Similarly, guitarfishes (e.g., Rhinobatus productus) comprise a significant component of artisanal fisheries off the coast of Sonora in the northern Gulf and landings are highest when adults migrate inshore to form aggregations and breed (Bizzarro et al., 2009). Mullets have long been important to commercial fisheries (Arvizu-Martinez, 1987; SEMARNAP, 1997), with a recent growth in demand for use as agricultural feed for livestock (OA, personal observation). Although the importance of mullet spawning aggregations to commercial fisheries in the Gulf has not been examined, their spawning aggregations are heavily exploited in parts of the Indo-Pacific (Sadovy de Mitcheson and Erisman, 2010). Similarly, the Gulf corvina (C. othonopterus) and the bigeye croaker (Micropogonias megalops) are two of the most productive finfish fisheries of the northern Gulf, and fishing activities for these species exclusively target the large spawning aggregations that form in the spring at the mouth of Colorado River (Arvizu-Martinez, 1987; RománRodríguez, 2000).

4.3. Considerations for the conservation and management of fish spawning aggregations in the Gulf of California The importance of fish spawning aggregations and aggregating fishes to commercial fisheries, the large harvests and revenues generated directly from spawning aggregations, and the collapse of fisheries for several large-bodied aggregating species all indicate that management policies that specifically seek to protect aggregations (reviewed by Colin et al., 2003; Sadovy and Colin, 2005, 2010) are necessary for certain fish species whose aggregations are targeted by commercial fisheries (e.g., B. polylepis, L. argentiven-

tris, M. rosacea, M. jordani, C. othonopterus) in the Gulf of California.

However, the temporal and spatial dynamics of spawning aggregations vary considerably among species (Domeier and Colin, 1997), which suggests that no single management strategy will effectively manage them all (Sadovy and Domeier, 2005a). Species that migrate long distances to form only a few, large, aggregations for very brief periods (i.e., transient spawning aggregations) are likely to benefit from area closures at important spawning sites and fishing bans or other controls during spawning periods, whereas those that move only short distances to form large numbers of small aggregations over several months (i.e., resident spawning aggregations) may be sufficiently managed by daily catch limits, annual or seasonal quotas, gear restrictions or other traditional measures (Sadovy and Domeier, 2005a; Sadovy de Mitcheson and Erisman, 2010). Therefore, scientific investigations into the spatial and temporal dynamics of spawning aggregations of each species, interactions between fishing and spawning, biological effects of fishing aggregations, and the potential effects of different management scenarios on population growth (Heppell et al., 2006; Sadovy de Mitcheson and Erisman, 2010) need to be carried out for fishes that form seasonal spawning aggregations in the Gulf of California. The information required for such analyses is known for a few species (e.g., M. rosacea, L. argentiventris), but even the simplest fisheries (e.g., stock assessments) and biological (e.g., growth and longevity) data are missing for most commercial species that form spawning aggregations in the Gulf. Completion of any such analyses will also require substantial improvements in the resolution, consistency, and accuracy of fisheries data collected by CONAPESCA across years and among regions of the Gulf.

Several studies have called for the protection of fish spawning aggregations in the Gulf, particularly through the inclusion of aggregation sites within marine reserves and seasonal restriction of fishing activities during spawning aggregation periods (AburtoOropeza et al., 2008; Erisman et al., 2007; Sala et al., 2002, 2003, 2004). Unfortunately, wider consideration for the management and protection of spawning aggregations have yet to be embraced by policy-makers, conservation agencies, and other scientists working in the region. In fact, many of the most recent scientific investigations that propose ecosystem-based management of small-scale fisheries in the Gulf, which by definition seek to understand and maintain interactions between key ecological parameters and fisheries, fail to mention fish spawning aggregations as an important component that should be incorporated into current agendas that seek the creation of sustainable fisheries in the region (ArreguínSánchez et al., 2004; Díaz-Uribe et al., 2006; Cisneros-Mata, 2010).

Such pervasive ignorance is remarkable, given the recommendations by the Food and Agriculture Organization of the United Nations (FAO) Code of Conduct and FAO Fishery Manager’s Guide to protect fish spawning aggregation sites (Sadovy de Mitcheson, 2009). Indeed, only one aggregating species (T. macdonaldi) is fully protected from harvest while one other (C. othonopterus) is managed by regulations that partially protect its spawning aggregations (Cisneros-Mata et al., 1995; Román-Rodríguez, 2000). Conversely, management policies for some of the most valuable invertebrate fisheries (e.g., blue crab, shrimp, lobster, rock scallops) in the Gulf and elsewhere in Mexico focus on the protection of important breeding sites and seasons as a means to maintain a stable fishery (OECD, 2006).

Certain fishing methods and gear types used by commercial fisheries in the Gulf of California seriously threaten fish spawning aggregations and coastal fish populations in general. Nighttime spear fishing, in which divers (called ‘pistoleros’) supplied with hookah-based air supplies literally walk along the reef at night and spear fishes while they are resting, have emerged in many areas as the most common method used to harvest reef fishes, including aggregating species of groupers, snappers, croakers, and grunts

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(Arreguín-Sánchez et al., 2004; Cinti et al., 2010; Rodríguez-Quiroz et al., 2010; Lluch-Cota et al., 2007). Another popular method is to use teams of divers to drive fishes into large gill nets set on the reef.

These two activities are recognized as the largest threats to fish spawning aggregations and reef fish populations throughout the Pacific (Gillet and Moy, 2006). In the southwest Gulf, they are used to harvest ca. 1000 tons of reef fishes annually (http://seawatch.org) and are blamed for the demise of Gulf grouper populations (Sala et al., 2004). Night spearfishing and diver-set gill net fishing of reef fishes are both illegal, but enforcement is virtually non-existent and penalties for non-compliance are minimal (Cinti et al., 2010; Ezcurra et al., 2009).

Standard gill nets deployed from pangas are also widely used by artisanal fishers in the Gulf to capture fishes from spawning aggregations and were the main gear type used to harvest the once abundant and now endangered totoaba (Cinti et al., 2010; Cisneros-Mata et al., 1995; Rodríguez-Quiroz et al., 2010).

Gill nets are blamed for the collapse of two large aggregationforming fishes in southern California, the giant sea bass (S. gigas) and the white seabass (Atractoscion nobilis), that also occur in the northern Gulf. Commercial bans of gill nets in nearshore waters of southern California created the de facto protection of spawning aggregation sites and has resulted in the recovery of both species over the past decade (Pondella and Allen, 2008), suggesting that similar regulations, if enforced, could produce positive results for these and other aggregating species in the Gulf of California.

Acknowledgements We thank M. Craig for his thoughtful comments on this research.

The Walton Family Foundation, the David and Lucile Packard Foundation, and the Center for Marine Biodiversity and Conservation (CMBC) at Scripps Institution of Oceanography, University of California at San Diego provided financial or other support for this research. S. Aceves at Niparaja A.C. provided assistance in the collection of data from fisheries offices.

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