Diversity and distribution of anuran in two islands of Parnaíba River Delta, Northeastern Brazil by Dr. A. H. Kabir

J. Bio. Env. Sci. 2016 Journal of Biodiversity and Environmental Sciences (JBES) ISSN: 2220-6663 (Print) 2222-3045 (Online) Vol. 8, No. 2, p. 74-86, 2016 http://www.innspub.net RESEARCH PAPER

OPEN ACCESS

Diversity and distribution of anuran in two islands of Parnaíba River Delta, Northeastern Brazil Etielle Barroso de Andrade1,2,3*, José Roberto Souza Almeida Leite2, Gilda Vasconcelos de Andrade1 ¹Postgraduate Program in Biodiversity and Conservation, Department of Biology,Federal University of Maranhão, Maranhão, Brazil 2

Research Center for Biodiversity and Conservation, Federal University of Piauí, Piauí, Brazil

Federal Institute of Education, Science and Technology of Piauí, Piauí, Brazil Article published on February 11, 2016

Key words: Anuran fauna, Biogeography, Communities ecology, Conservation, Parnaíba River.

Abstract The distribution and composition of communities are influenced by factors that determine the environmental characteristics in a particular region. In order to obtain more information regarding the fauna of frogs in the region of the Parnaíba River Delta, Northeastern Brazil, we performed a quantitative ecological study to compare the composition and distribution of the amphibian communities. The study was conducted in the two largest islands of Deltafrom September 2008 to August 2009. Fifteen ponds were selected and slowly covered in search of males in calling activity. We recorded 21 frog species, distributed in five families and 11 genera. Ilha Grande de Santa Isabel(21 spp.) had higher species richness than the Ilha das Canárias (11 spp.). Although most species are considered to be common in open areas, they were highly influenced by the structural complexity of the vegetation. The highest richness was observed in environments with greatest availability of microhabitats for reproduction. The preservation of different environments found in the two islands, associated with the maintenance of suitable habitats for reproduction of each species, will contribute to the conservation of amphibian communities of the Parnaiba Delta River. *Corresponding

Author: Etielle Barroso de Andrade  etlandrade@hotmail.com

74 | Andrade et al.

J. Bio. Env. Sci. 2016 Introduction The

the marine coastal zone. Thus, this region is and

particularly interesting for studies that focus on

distribution patterns of the natural organisms are

knowledge

the

species

diversity

diversity and species distribution in relation to

fundamental tools to understand the effects of

environmental features between the different islands.

environmental changes in the natural ecosystems (Heyer et al., 1994). In addition, information on the

Some studies on the amphibian fauna of the Parnaíba

biogeographical patterns of species are of great

Delta River region have already been conducted (Silva

importance for the development of conservation

et al., 2007;Loebmannand Mai, 2008;Leite Jr et al.,

strategies in a given region(Fisher and Robertson,

2008a, b; Andrade et al., 2014), however,the present

2002;Fu et al., 2006). Distribution patterns vary

study is the first to address the diversity and

according to several principles that act on different

distribution

observation scales (local or regional) (Chase and

environments in the delta. We compare the species

Leibold, 2002) and are influenced by a larger number

composition

of ecological processes (predation, competition,

assemblages in the two largest islands in the Parnaíba

dispersion)

Delta River, analysing the distribution and the use of

(McCarthy,

1997;

McCarthy

and

Lindenmayer, 2000,Eterovick and Sazima, 2000).

anurans

and

the

between

structure

different amphibian

habitats used for reproduction by species with different reproductive modes.

Due to some biological (biphasic life cycle) and physiological

characteristics

(permeable

skin)

Materials and methods

amphibians are highly sensitive to changes in

Study area

environment (Burkett and Thompson, 1994). This

The delta region comprises an area with about 2,750

turns them into key species to assess long-term

km² and is influenced by the eastern Amazonian

global, regional or local changes of the environment

coast and by the semi-arid Brazilian coast. The

(Pounds et al., 1999). Furthermore, ecological factors

climate is characterized by mean temperatures

such as migration, predation and extinction, may lead

ranging from 25 to 30°C and average annual rainfall

the amphibian species show different responses to

exceeding 1,200 mm, concentrated mainly from

different size scales (mainland-island), both positive

January to May (IBAMA, 1998). The Delta vegetation

relations (reproductive effort and clutch size) as

is frequently flooded during the tides. This differs

negative (egg size and body size) (Wang et al., 2009).

mainly due to variations in composition and soil depth in relation to groundwater, being classified as

Several studies on the amphibian communities has

mangrove,

riparian

been made in recent years (Eterovick and Sazima,

(CEPRO, 1996).

and

floodplain

vegetation

2000;Bernarde and Machado, 2001; Vasconcelos and Rossa-Feres, 2005; Santos et al., 2007, 2008),

The study was conducted in the two largest islands of

however,

Brazilian

Delta: Ilha Grande de Santa Isabel (state of Piauí) and

amphibians remain scarce (Giarettaet al., 2008),

Ilha das Canárias (state of Maranhão), with 240 km²

especially in the Northeast region. The Parnaíba Delta

and 132 km², respectively. Together the two islands

River, third largest in the world (MMA/SDS, 2002),

occupy about 14% of the total area of the Delta.

ecological

data

most

consists of about 80 islands and is located in northeastern Brazil between the states of Piauí (35%)

Ilha

Grande

and Maranhão (65%). Geomorphologically it is a

coordinates2º51’ S and 41º49’ W, is separated from

dynamic area and from an ecological point of view it

the mainland by an effluent of the Parnaíba River

has a potential to harbor a high biodiversity due to

(about 150 m wide). The island’s soil is mainly formed

the influence of the Caatinga and Cerrado biomes and

by sand dunes and during the rainy months (January

75 | Andrade et al.

Santa

Isabel,

located

J. Bio. Env. Sci. 2016 to May) forms several temporal ponds. The island was

island, is characterized by an open area with restinga

divided into three different areas (Fig. 1), each one

vegetation (TPR1, TPR2, TPR3, TPR4) (Table 1).

containing four temporary ponds (TP). These areas were selected by represent the different environments

Ilha das Canárias is located at coordinates 2º46’ S

on the island. Area “A” is predominantly composed of

and 41º51’ W, distant about 1,200 m from the

shrub vegetation and suffers a strong anthropogenic

mainland. It is formed by a complex mosaic of

influence. It’s located further south of the island and

ecosystems and has large number of streams that

presents temporal ponds in an inter-dune region

assure the maintenance of riparian areas and flooded

(TPD1, TPD2, TPD3 e TPD4); area “B”, located in the

fields that are affected by the tide (CEPRO, 1996).

central-west region of the island, has temporal ponds

Due to difficult access, sampling on the Ilha das

surrounded by woody vegetation (TPW1, TPW2,

Canárias was performed only in area “D” (Fig. 1),

TPW3, TPW4). Area “C”, located at the north of the

were two flooded swamp areas (FS1, FS2) and a permanent pond (PP) were visited.

Fig. 1.Schematic map of the islands sampled in the Parnaíba Delta River. The capital letters represent the sampling areas: area A, B and C, located on Ilha Grande de Santa Isabel, and area D, located on the Ilha das Canárias. The dotted line represents the political division between the municipalities of Ilha. Anuran sampling

merge during the rainy station (March to May).

Samples were realized monthly from September 2008 to August 2009. Observations began at dusk (18:00

The abundance of species in calling activity was

h) and ended according to the decrease in the frogs

measured by counting the number of calling males,

vocalizing activity. We performed time limited

when those had low densities (< 20 individuals). For

standardized acoustic surveys at the breeding sites

small choirs (estimated between 20 to 35 individuals

(Heyeret al., 1994). Each pond was slowly coveredfor

in calling activity) a value of 35 was used as a

an hour in search of males in calling activity. The

maximum number of individual calls recorded. For

water bodies nearest of the collections points were

large choirs (> 35 individuals) with overlap in the

considered as single sample unit because they could

vocalizations, we used 60 as the maximum number of

76 | Andrade et al.

J. Bio. Env. Sci. 2016 individual calls recorded (adapted from Crouch and

The change in faunal composition between the water

Paton, 2002). This procedure was adopted to avoid

bodies (β diversity) was determined using the

disturbance in analysis caused by very abundant

Sørensensimilarity coefficient (Cs) (Krebs, 2000). Cs

species. To avoid a tendency in determining richness

values ≤ 0.50 were considered as indicative of high

and abundance of species, the sequence in the sample

species

of ponds was always alternated.

environments. The influence of distance between

substitution

between

the

compared

ponds on the β diversity and the influence of To avoid overestimation of population abundance due

geographic distances from the mainland on the

to recount of individuals in successive samples, we

composition of species in each water body was

considered the total abundance of species in each

evaluated using Mantel test (Manly, 1994) with 5,000

pond as being equal to the month with highest

permutations. In the latter case, as comparisons were

abundance (Bertoluciand Rodrigues, 2002). Voucher

made

specimens

the

composition) and dissimilarity (using Euclidean

were

collected

ColeçãoZoológica

Delta

and

similarity

matrices

(species

(CZDP)

distance), a resulting negative “r” coefficient was interpreted as positive correlation between the

Campus

compared matrices (Santos et al., 2007).

Reis

Parnaíba

the

(Zoological Collections of the Panaíba Delta River), Ministro

housed

among

Veloso

(UFPI/CMRV),

Universidade Federal do Piauí. To compare the ponds based on species composition Statistical analysis

and abundance we used Sørensen (Cs) and Morisita-

To assess the efficiency of the sample methods and to

Horn (CH) similarity indices, respectively, with

compare species richness between the two studied

subsequent analysis of the clustering by Unweighted

islands, we made a rarefaction curve using the

Pair Group Average Method (UPGAM) (Krebs, 2000).

software Biodiversity Pro 2 (McAleeceet al., 1997).

Only groups with arrangements with CH > 0.70 were

For this we used the highest abundances recorded in

considered valid. The representativeness of the

each water body. The total richness for each island

similarity matrix was evaluated by the cophenetic

were estimated by nonparametric estimators Chao 1

correlation

and

obtained from the correlation matrix with the original

Chao

(Colwell

andCoddington,

1994),

considering records made in selected water bodies, by

coefficient

(r)

(Romesburg,

1984),

similarity matrix generated from the dendrogram.

extrapolating the rarefaction curve. To check the influence of structural complexity on the The diversity in each pond was estimated by

species

calculating the Shannon-Wiener diversity index and

correlation coefficient (r) (Zar, 1999). For this

Pielou equitability (Krebs, 2000). According to the

analysis

number of areas and occupied water bodies, species

reproductive modes of the species and the numbers of

were classified into three categories of distribution

vegetation types observed in the surroundings (1 = no

(adapted from Nascimentoet al.,1994) (Table 2): (1)

vegetation, 2 = only one type of vegetation, 3 = two

wide, where the number of occupied areas was greater

types of vegetation, 4 = three types of vegetation, 5 =

than two and more than eight water bodies were

more than three vegetation types) and inside (1 = no

occupied; (2) preferred, in which the number of

group, 2 = homogeneous group in part or all of the

occupied areas was less than or equal to two and

pond, 3 = 2 to 4 groups and 4 = more than 4 group) of

occupation occurred in five to eight ponds, and (3)

each water bodies. Diversity and similarity analyses

restrict, in which occupation of the ponds was less

were generated using the software PAST 1.4 (Hammer

than or equal to four in one single area.

al.,

77 | Andrade et al.

composition we

considered

2001).

used the

Correlation

the

total

tests

Spearman number

(Mantel

and

J. Bio. Env. Sci. 2016 Spearman) were run using the software BioEstat 5.0

representatives in this island and those with the

(Ayres et al., 2007).

lowest number of species were Cycloramphidae and Microhylidae. The toad Rhinella mirandaribeiroiwas

Results

foundonly in Ilha Grandede Santa Isabel andoutside

We recorded 21 species belonging to five families and

the sampling units (ponds) therefore was excluded

11 genera (Table 2). Families that showed the highest

from the analysis. In Ilha das Canárias were recorded

species richness were Leptodactylidae (10 spp.) and

11 species, being the families Leptodactylidae and

Hylidae (7 spp.). In the Ilha Grande de Santa Isabel

Hylidae the richest and Leiuperidae and Bufonidae

was recorded 21 species (see Andrade et al., 2014).

present only one species. Scinax fuscomarginatus

Families Leptodactylidae e Hylidae were the most

was found calling only at Ilha das Canárias.

Table 1. Main characteristics of water bodies studied in Ilha Grande de Santa Isabel and the Ilha das Canárias, Parnaíba Delta River, Brazil. Water bodies: TPD - Temporary ponds inter dunes in urban areas (numbered 1 to 4); TPW - Temporary ponds that have trees closed around it (numbered 1 to 4); TPR - Temporary ponds located in the area of restinga (numbered 1 to 4); FS - Flooded swamp areas (1 and 2), PP - Permanent pond. Vegetation types: (g) grass; (sh) shrub; (ab) arboreal vegetation; (aq) aquatic vegetation; (ta) taboa; (bs) bare soil. Ponds

Coordinates

Area (m²)

TPD1 TPD2 TPD3 TPD4 TPW1 TPW2 TPW3 TP4 TPR1 TPR2 TPR3 TPR4

2°50.140’ S - 41°49.146’ W 2°50.125’ S - 41°49.120’ W 2°50.115’ S - 41°49.069’ W 2°50.206’ S - 41°49.022’ W 2°49.314’ S - 41°49.470’ W 2°49.458’ S - 41°49.413’ W 2°49.459’ S - 41°49.410’ W 2°49.589’ S - 41°49.467’ W 2°46.021’ S - 41°48.278’ W 2°46.063’ S - 41°48.247’ W 2°46.164’ S - 41°47.967’ W 2°46.415’ S - 41°48.101’ W

FS1 FS2 PP

2°47.675’ S - 41°52.083’ W 2°47.700’ S - 41°52.381’ W 2°47.659’ S - 41°52.515’ W

Hidroperiod

Ilha Grandede Santa Isabel 1,098 Temporary 2,441 Temporary 1,253 Temporary 11,667 Temporary 3,032 Temporary 3,609 Temporary 1,820 Temporary 62,597 Temporary 5,443 Temporary 71,000 Temporary 140,500 Temporary 267,441 Temporary Ilha das Canárias 8717 Temporary 12289 Temporary 19342 Permanent

Vegetation within

marginal Vegetation

g, sh, aq g, aq g, sr, aq, ta, g, sr, ab, ta g, sr, ab, aq, ta g, sr, ab, aq, ta g, sr, aq, ta g, sr, ab g, aq, ta, g, sr, aq, ta g, aq, ta g, aq, ta

g, sr, ab g, sr, ab, bs g, sr g, sr, ab, bs g, sr, ab g, sr, ab g, sr, ab g, sr, ab g, sr, g, sr, bs g, bs g, bs

g, aq g, aq, ta aq, ta

g, sr g, sr g

The rarefaction curves did not reach an asymptote in

largest richness and the largest numbers of males in

any of the two islands (Fig.2). The comparison of

calling activity.

richness

between

both

islands,

through

the

rarefaction method, indicated that the Ilha Grande de

Together they represent 28.5% of the total number of

Santa Isabel has statistically a greater number of

frogs recorded on Ilha Grande de Santa Isabel.

species (17) than Ilha das Canárias (11). Chao 1 and

However, TPD4 showed a slightly greater diversity

Chao 2 indices estimated a total richness of 19 ± 0.25

than pond TPW1 due to higher species richness. In

and 19.91 ± 1.68 for Ilha Grande de Santa Isabel and

Ilha das Canárias, the greatest richness and largest

11 ± 0 and 11.4 ± 0.87 for Ilha das Canárias.

abundance was registered at pond FS2, where 48.28% of all frogs recorded for the island were found (Table

The ponds TPD4 and TPW1 show respectively the

2).

78 | Andrade et al.

J. Bio. Env. Sci. 2016 Table 2. Abundance, distribution and reproductive modes of the 20 species recorded in both islands in the Parnaíba Delta River (Ilha Grande de Santa Isabel and Ilha das Canárias), Brazil, in each of the ponds studied from September 2008 to August 2009. Total - total abundance of calling males of the recorded species in each pond. S - total richness observed in each pond; H'- Shannon-Wiener diversity index and J' - Pielou evenness index. Abbreviations and characteristics of water bodies in Table 1. Values equal to 35 and 60 indicate the formation of small and large chorus in which the individual calls are indistinguishable and can’t estimate more precisely the number of individuals.Rhinella mirandaribeirowas not included in the analysesand is not presented in the table (see text). Species/Ponds

TPD1

TPD2

TPD3 TPD4

TPW1

TPW2

TPW3

TPW4

TPR1 TPR2

TPR3

TPR4

FS1

FS2 PP

Total Reprod. Mode

Categ. distribution

Leptodactylidae Leptodactylus fuscus Leptodactylus sp. Leptodactylus macrosternum

0 0 0

3 0 0

7 0 3

4 4 5

0 0 0

0 0 4

0 12 0

4 0 60

8 0 10

13 0 6

8 0 6

6 3 0

2 15 4

0 0 0

55 34 98

30 32 11

Preferred Preferred Wide

Leptodactylusnatalensis Leptodactylus pustulatus Leptodactylusvastus Physalaemusalbifrons Physalaemuscuvieri Pseudopaludicolamysta calis Pleurodemadiplolister Hylidae Dendropsophus minusculus

0 60

0 4

0 60

0 12

1 60

0 60

0 35

0 60

0 0

0 10

0 60

0 0

0 60

0 0

1 541

3 11

Preferential Restrict

1 3 0 0

1 1 0 7

2 9 0 35

5 2 2 60

3 5 0 60

1 3 0 2

2 2 0 35

1 0 0 60

0 5 0 0

0 35 0 0

0 60 0 3

0 35 0 0

0 0 0 60

16 160 2 442

13 11 11 1

Restrict Preferred Wide Restrict

Restrict

655

Preferred

Dendropsophusnanus Hypsiboasraniceps Scinax fuscomarginatus Scinax gr. ruber Scinax x-signatus Phyllomedusa nordestina Bufonidae Rhinella jimi Odontophrynidae Proceratophryscaramas chii Microhylidae Elachistocleispiauiensis TOTAL S H’ J’

60 7 0 0 3 5

0 2 0 0 0 0

7 5 0 35 35 2

20 60 0 35 35 4

60 60 0 35 35 12

60 5 0 0 4 2

60 35 0 0 35 5

35 7 0 0 0 1

60 3 0 0 4 20

7 4 0 0 35 6

0 0 0 0 35 0

3 0 0 0 35 0

0 35 35 2 5 0

0 35 60 5 5 0

0 13 60 0 0 0

372 271 155 112 266 57

1 1 1 1 1 24

Wide Wide Wide Restrict Wide Wide

Restrict

0 174 8 1,46 0,70

0 37 7 1,40 0,72

4 259 13 2,01 0,78

3 323 17 2,26 0,80

0 405 15 2,21 0,81

0 199 10 1,48 0,64

0 273 10 1,93 0,84

0 236 8 1,63 0,78

7 283 10 1,83 0,80

0 105 7 1,62 0,83

0 127 6 1,38 0,77

0 147 6 1,42 0,79

0 208 9 1,66 0,75

0 306 10 1,90 0,82

0 14 193 3 1,27 0,92

Restrict

The analysis of anuran assemblage in each pond

similar, two first have more heterogeneous vegetation

showed an evident separation between species

allowing the presence of Phyllomedusanordestina

composition of the two islands and the formation of

and Hypsiboasraniceps. Four cluster was formed by

four clusters (Fig. 3). The first cluster was formed by

ponds of inter-dunes area (“A”) (TPD1, TPD3 and

ponds that presented highest species richness at Ilha

TPD4) and of arboreal vegetation area (“B”) (TPW1,

das Canárias (FS1 and FS2) and shared eight

TPW2, TPW3 and TPW4). The pond TPD2 remained

species.The second (TPR1 and TPR2) and the third

isolated, showing fewer than eight species and

(TPR3 and TPR4) cluster were formed by water

absence of Dendropsophus nanus and P. nordestina.

bodies located in the resting area (“C”) of Ilha Grande de Santa Isabel. Although these four ponds are very

The difference in species composition (β diversity)

79 | Andrade et al.

J. Bio. Env. Sci. 2016 between sampled water bodies was high (Cs ≤ 0.5) for

TPR2, TPW4 - TPR3 and TPW4 - TPR4; 6000 m)

33 (31.42%) of 105 pairs of combinations (Table 3).

presented

There was a strong and highly significant correlation

composition in each water body was few influenced

between the distance of water body matrix and the

by the distance of mainland(r = - 0.3658; p <

similarity matrix of β diversity (r = - 0.6796; p <

0.0001). However, structural heterogeneity of the

0,001). At Ilha Grande de Santa Isabel, nearby waters

vegetation provide greater diversity of reproductive

body (TPW2 - TPW3; 140 m) had high similarity

modes among the species (rs = 0.6429; p = 0.0097) in

(0.90) in composition while distant ponds (TPW4 -

both island.

lower

similarity

(0.29).

Species

Table 3. Similarity (Sorensen) between the 15 water bodies studied in both islands in the Parnaíba Delta River (Ilha Grande and Ilha das Canárias), based on the species composition of frogs. Values equal or below 50% (in bold) indicate the pairs of ponds where β diversity was considered high. In italics, number of mutual species between pairs of lakes. Abbreviations and characteristics of water bodies in Table 1. TPD1 TPD2 TPD3 TPD4

TPW1 TPW2

TPW3

TPW4 TPR1

TPR2

TPR3

TPR4 FS1

TPD1

66.67 76.19

64.00

69.57 88.89

88.89

75.00 77.78 57.14

42.86

57.14

FS2

TPD2

70.00 58.33

63.64 70.59

70.59

66.67 47.06 30.77

46.15

30.77 50.00 47.06 54.55

TPD3

86.67

85.71

78.26

66.67 78.26 52.63

52.63

52.63 63.64 60.87 35.29

TPD4

81.25 74.07

74.07

56.00 74.07 52.17

52.17

53.85 59.26 28.57

TPW1

72.00

80.00

69.57 72.00 57.14

57.14

66.67 72.00 31.58

TPW2

90.00

77.78 70.00 50.00

50.00

50.00 42.11

50.00 42.86

TPW3

77.78 80.00 62.50

62.50

62.50 42.11

60.00 42.86

TPW4

55.56 28.57

28.57

28.57 47.06 55.56 50.00

TPR1

75.00

62.50

75.00 42.11

TPR2

66.67

83.33 40.00 50.00 20.00

TPR3

83.33 40.00 62.50 20.00

TPR4

26.67 50.00 0.00

FS1

84.21 61.54

FS2

57.14

35.29 44.44 33.33

60.00 28.57

The analysis of spatial distribution showed the

Leptodactylus fuscus, Physalaemus albifronsand

formation of six distinct groups (Fig. 4): (1)

Scinax x-signatuswere more abundant in the resting

Physalaemus cuvieri, Proceratophryscaramaschii

ponds

and

Leptodactylus

Pleurodemadiplolister

presented

higher

TPR2,

TPR3

and

natalensis,

TPR4.

The

species

Leptodactylus

sp.

abundance in TPD4 which has a greater structural

andScinax fuscomarginatuswere not included in any

complexity in the area “A”; (2) Leptodactylus

of the groups due to your low similarity values.

macrosternum, P. nordestina and Elachistocleis piauiensisshowed higher abundances in pond TPR1of

The species L. pustulatus, P. albifrons, H. raniceps, S.

area “C”; (3) Leptodactylus vastus, Scinax gr.

x-signatus,

ruberand Rhinella jimiwere more abundant in TPD3,

considered widely distributed while L. natalensis and

TPD4 and TPW1; (4)Dendropsophusminusculus,

P. cuvieri had their distribution restricted to only one

Pseudopaludicolamystacalisand H. raniceps were

pond studied (TPW1 and TPD4, respectively) (Table

2). Other species showed a preferential pattern, for

abundant

Leptodactylus

Ilha

das

pustulatusand

Canárias;

(5)

Dendropsophus

example,

nanusand

nordestinawere

vastus

nanusshowed higher abundances in the area “B”

Dendropsophusminusculusthat

(TPW1,

environments with high diversity structural.

TPW2,

TPW3

and

TPW4);

and

(6)

80 | Andrade et al.

occurred

and in

J. Bio. Env. Sci. 2016 Discussion

piauiensis). However, Mantel test revealed a weak

The difference in species number between the two

correlation between distance from the mainland and

islands may be related to geographical isolation and

species composition of the two islands indicating the

proximity of dispersion sources, which facilitate the

influence of other factors on species composition in

colonization of species with dispersion difficulty (E.

the islands.

Fig. 2. Rarefaction curves of species in both islands sampled in the ParnaĂba Delta River between September 2008 and August 2009. The intersection line corresponds to the comparison of richness based on the rarefaction method (minimum number of individuals). The rarefaction curves revealed that species richness

local (house construction, touristic activities and

is potentially higher than registered. Loebmann and

deforestation, etc.) generated by human action may

Mai (2008) found 21 species during an amphibian

lead to changes in composition and abundance of

assessment at seven localities along the coast of PiauĂ.

species. The intermediate disturbance hypothesis

Of these, four were not recorded in our study

(Connell, 1978) which refers to intensity and

(Dendropsophus

minutus,

Scinax

frequency of disorders that affect diversity patterns

nebulosus,Trachycephalustyphonius

and

can offer an additional explanation for high species

Leptodactylus troglodytes). On the other hand, four

richness and diversity found in this pond. In regions

taxa recorded in our study were not found by these

showing

authors (S. fuscomarginatus, L. natalensis, L.

communities are distributed between the mosaics of

pustulatusand Leptodactylus sp.). This indicates the

available habitats, thus favoring high species diversity

need to use additional sampling methods (e.g. pitfall

(Ricklefs, 2003). Although disturbed, this pond is

traps, active collecting, sampling of tadpoles), since

located inside a rural area where it suffers moderate

the survey at breeding sites is few efficient to record

levels of disturbance compared to other urban areas

species with an explosive reproduction (Conte

within the island.

moderate

levels

disturbance

the

andRossa-Feres, 2006). The

species

composition

analysis

revealed

Pond TPD4 located in disturbed area presented

relationship with the distance from water bodies

greatest species richness (17 spp.; 80.9% of total)

(greater similarity in the shorter distances) and the

when compared with other natural environments.

availability of microhabitats (greater variety of species

Besides

greatest

with different reproductive modes in ponds with

environment heterogeneity and greatest diversity of

the

pond

TPD4

presented

greater environmental heterogeneity). The partition

reproductive modes. Structural modifications in this

in habitat use (calling sites) is strongly related to

81 | Andrade et al.

J. Bio. Env. Sci. 2016 reproductive modes of anurans (Crump, 1971) and the

area farthest) presented higher β diversity when

areas that have greater structural complexity of

compared with the other areas. However, in some

vegetation showed a greater diversity of reproductive

cases, high β diversity may be caused by difference in

modes.

species richness of two pond located in same area as observed between TPR3 and TPR4 (area “C”) andFS1

Some of the studied ponds had high species turnover

and PP (area “D”). The high turnover rate of species

and were more strongly influenced by the distance

found in ponds within the same island shows the wide

between ponds than by geographic distance in

range of environments occupied by amphibians in the

relation to mainland. This indicates possible species

region and shows also the importance of conserving

segregation in specific environments in the islands.

the various areas that comprise the Delta of the

On Ilha Grande de Santa Isabel, resting area (sampled

Parnaiba River.

Fig. 3. Similarity in the species composition among the 15 water bodies, based on the Sørensen similarity index (cophenetic correlation coefficient r = 0.7348). The numbers represent the clusters with similarity above 70%. Abbreviations and characteristics of water bodies in Table 1. The highest species richness on each island and the

reproductive modes

and

present

resistance

larger diversity of reproductive modes were observed

desiccation and insolation imposed by environmental

in ponds that had greater vegetation heterogeneity

conditions (Haddad and Prado, 2005).

(Table 2) in the surroundings as well as in its interior. Currently, 39 reproductive modes are recognized for

The number of anurans that exploit a particular

amphibians (Haddad and Prado, 2005). The most

habitat has been related to the environmental

generalists exhibit external egg fertilization with

complexity in various biomes (Kopp andEterovick,

deposition and tadpole development in the water

2006; Bastaziniet al.,2007; Vieira et al., 2009). This

while more specialized species lay eggs outside water

occurs because more structurally complex habitats

with aquatic tadpoles or deposit terrestrial eggs with

may provide more niches and different possibilities

direct

1994).

for resource use and thus show an increase in species

Reproductive success of some species that inhabit

diversity (BernardeandKokubum, 1999). According to

environments with open vegetation depend largely on

Werner andGlennmeier

a greatest structural diversity of the vegetation at the

vegetation cover along the margins of ponds is a

temporal

(EterovickandFernandes,

crucial factor in the choice of breeding sites in frogs.

2001), although most of them show more generalized

Especially among hylids the great number of species

development

water

(DuellmanandTrueb,

bodies

82 | Andrade et al.

(1999), the density

J. Bio. Env. Sci. 2016 appears to be associated to a greater diversity and

and diversity of hylidswas observed in the resting

availability of local calling sites, since the presence of

area, where only one species (S. x-signatus) was

all vegetational strata provides several microhabitats

common to all ponds in that region that had more

for use of these animals (AfonsoandEterovick, 2007).

homogeneous vegetation.

This relationship between the structural complexity

Fig. 4. Similarity in the spatial distribution, based on the abundance of calling male from 20 frog species recorded in the two islands of ParnaĂba Delta River, northeastern Brazil, from September 2008 and August 2009. Cophenetic correlation coefficient (r = 0.7451). The numbers represent the clusters with similarity above 70%. Species:

Sxs

x-signatus;

Sru

Scinax

gr.

ruber;Sfu

fuscomarginatus;

Dmi

Dendropsophusminusculus; Dna = D. nanus; Hra = H. raniceps; Pno = P. nordestina; Lna = L. natalensis; Lma = L. macrosternum; Lfu = L. fuscus; Lva = L. vastus; Lsp = Leptodactylus sp.; Lpu = L. pustulatus; Pal = P. albifrons; Pcu = P. cuvieri; Pdi = P. diplolister; Pmy = Pseudopaludicolamystacalis; Rji = R. jimi; Pca = P.caramaschii; Epi = E. piauiensis. Most species found in the region can be considered

including the populations of PiauĂ state.

typical of open formations of South America and of wide geographical distribution, both in open areas as

Conclusion

well as in forested areas (Frost, 2015). Some species

The number of species recorded in this study is below

still have their taxonomy not clearly resolved and may

the real richness present in the Delta region due to

be considered as belonging to a species complex, as

the large territory and a variety of environments that

Leptodactylus

ruber,

form the delta complex, several still poorly explored.

Dendropsophus

This work represents an important accumulation of

minusculus. The latter species was treated by some

knowledge on local amphibian communities and

authors

microcephalus,

should be used for the setup of monitoring programs

including being considered as a possible new

and species management plans as well as to subside

species(Loebmann and Mai, 2008; Loebmann and

appropriate

Haddad, 2010; Andrade et al., 2014). However, in a

environments.

recent study, Zina et al. (2014) used molecular tools

preservation of different environments distributed

and confirmed the identification of D. minusculus,

throughout the complex ecosystems found in the two

increasing the limits of their distribution to the

islands (regional heterogeneity) associated with the

southern region of Bahia, northeastern Brazil,

maintenance of suitable reproduction habitats of each

sp.,

fuscus,

Scinaxgr.

Pseudopaludicolamystacalisand as

Dendropsophus

gr.

83 | Andrade et al.

conservation According

strategies to

our

for

natural

data,

the

J. Bio. Env. Sci. 2016 species (local heterogeneity) will contribute to the

São João, Bahia, Brazil. Herpetology 63, 459–471.

effective conservation of the amphibian community of the Parnaíba Delta River.

Bernarde PS, Kokubum MNC. 1999. Anurofauna do Município de Guararapes, estado de São Paulo,

Acknowledgement

Brasil

(Amphibia,

This study received financial support from the CNPq

Leopoldensia 21, 89-97.

Anura).

Acta

Biologica

Project Universal 480997/2007-1/Edital MCT/CNPq 15/2007. We thank Coordenação de Aperfeiçoamento

Bernarde PS, Machado RA. 2001. Riqueza de

de Pessoal de Nível Superior – CAPES for the

espécies, ambientes de reprodução e temporada de

scholarship

Pós

vocalização da anurofauna em Três Barras do Paraná,

Graduaçãoem Biodiversidade e Conservação; IBAMA

Brasil (Amphibia: Anura). Cuadernos de Herpetología

for granting a collecting authorization (Licence nº

14, 93-104.

granted

the

Programa

17687-1/2009); We also thank Leonardo Carvalho and Suzana Gomes Lopes for suggestions on the

Bertoluci J, Rodrigues JT. 2002. Seasonal

manuscript.

Rocha,

patterns of breeding activity of Atlantic Rainforest

Geilson Faustino da Rocha and Rafael Guimarães

anurans at Boracéia, Southeastern Brazil. Amphibia-

Macedo for help during fieldworks. Special thanks

Reptilia 23, 161-167.

Ednaldo

Nascimentoda

Pedro Militão and Maria das Graças for their hospitality during the research, and Pedro da Costa

Burkett DW, Thompson BC. 1994. Wildlife

Silva, who besides sharing his deep knowledge of the

association with human-altered water sources in

Delta region, was the key piece during our field trips.

semiarid

Thanks CNPq and CAPES for financial support.

Biology 8, 682-690.

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