Research Article |
Corresponding author: Kássio C. Araújo ( kassio.ufpi@gmail.com ) Academic editor: Angelica Crottini
© 2018 Kássio C. Araújo, Anderson Guzzi, Robson Avila.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Araújo KC, Guzzi A, Ávila RW (2018) Influence of habitat heterogeneity on anuran diversity in Restinga landscapes of the Parnaíba River delta, northeastern Brazil. ZooKeys 757: 69-83. https://doi.org/10.3897/zookeys.757.21900
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Anurans have close associations with environmental conditions and therefore represent an interesting vertebrate group for examining how resource availability and environmental variables influence species diversity. Associations between habitat heterogeneity and anuran species diversity were tested in the Restinga landscapes of the Parnaíba River delta in northeastern Brazil. Twenty-one anuran species were sampled in the rainy season during monthly excursions (December 2015 to June 2016) into areas of Restinga on two islands in the Parnaíba River delta. The fourth highest anuran diversity was found in this type of environment in Brazil and is the third in northeastern Brazil. Microenvironments, characterized by a combination of vernal pools with different vegetational and physical structures, better explained anuran species composition in the Parnaíba River delta.
Amphibians, heterogeneity, Parnaíba River delta
Scientists have long attempted to explain species distribution patterns and species richness worldwide, and several ecological hypotheses and theories have been proposed (e.g.,
The habitat heterogeneity hypothesis has since been used to explain distribution patterns and species richness throughout the world (e.g.,
Although the habitat heterogeneity hypothesis of
Vegetation structure in and around water bodies is an important resource for local diversity of anurans (
The Parnaíba River delta in northeastern Brazil is dominated by Restinga coastal vegetation with sandy soils and open herbaceous, shrubby, and arboreal plant formations (
Study area: The Parnaíba River Delta is contained within an Environmental Protection Area (EPA) created in August 1966, covering approximately 313,800 ha in the Brazilian states of Piauí, Maranhão, and Ceará (Fig.
Map of the Environmental Protection Area of Parnaíba River Delta (shaded area), northeastern Brazil, with the location of the study area featuring six sampling points (red triangles). Key: black square, Canárias Island, state of Maranhão; black circle, Ilha Grande de Santa Isabel Island, state of Piauí.
Sampling: Amphibians were collected in areas of Restinga from two islands in the Parnaíba River Delta: Ilha Grande de Santa Isabel Island in the state of Piauí (2°52'27"S, 41°47'20"W, WGS84 datum, 5 m a.s.l.) and Canárias Island in the state of Maranhão (2°48'09"S, 41°52'19"W, WGS84 datum, 8 m a.s.l.). First we selected the areas of Restinga in Parnaíba River Delta according to the soil type (
Anuran sampling was undertaken monthly on consecutive days during the rainy season (from December 2015 to June 2016) employing visual searches (
Habitat heterogeneity was quantified using seven environmental descriptors adapted from
Main characteristics of the six sampling points in the Parnaíba River Delta: duration (in months) of the water pond (MWP), size (in meters) of water pond (SWP), (DWP), approximate percentage of vegetation cover on water surface (PVC), types of vegetation within water (TVI), number of types of marginal vegetation (TMV) and types of margin (TM). Types of vegetation: herbaceous and macrophytes (HM), shrub (SH), and arboreal (AB). Types of margin: plans (MPMP), inclined (MI), and plan and inclined (MPI). Locality (LC) of the sampling points: Ilha Grande de Santa Isabel Island (ILG) and Canárias Island (ILC). In parentheses, the value of each environmental descriptors (1–4). Mean (Mean values of environmental descriptors).
Point I | Point II | Point III | Point IV | Point V | Point VI | |
---|---|---|---|---|---|---|
LC | ILG | ILG | ILG | ILG | ILC | ILC |
MWP | 5–8 (2) | 5–8 (2) | 5–8 (2) | 1–5 (1) | 1–5 (1) | 1–5 (1) |
SWP | 300 (2) | 700 (3) | 400 (2) | 300 (2) | 300 (2) | 400 (2) |
DWP | > 61 (3) | > 61 (3) | > 61 (3) | 31–50 (2) | 31–50 (2) | > 61 (3) |
PVC | 76–100 (4) | 76–100 (4) | 31–50 (2) | 31–50 (2) | 31–50 (2) | 31–50 (2) |
TVI | HM (2) | HM (2) | HM (2) | HM (2) | HM (2) | HM (2) |
TMV | AB (3) | AB (3) | AB (3) | AB (3) | AB (3) | AB (3) |
TM | MPI (2) | MPI (2) | MPI (2) | MP (1) | MPI (2) | MPI (2) |
Mean | 2.57 | 2.71 | 2.28 | 1.85 | 2 | 2.14 |
Species distributions and associations with Brazilian morphoclimatic domains (
Statistical analyses: the SHANNON-WIENER diversity index and EQUITY OF PIELOU (
The normal distribution assumption was tested for both diversity and habitat heterogeneity data using the SHAPIRO-WILK test (
1822 anuran specimens were recorded, belonging to six families (Bufonidae, Hylidae, Leptodactylidae, Microhylidae, Odontophrynidae, and Phyllomedusidae), 12 genera, and 21 species (see Appendix
The most abundant species belonged to the families Leptodactylidae and Hylidae (Fig.
The sample-based accumulation curve tended asymptote (Fig.
Anuran diversity in the Parnaíba River Delta (PRD), Ilha Grande de Santa Isabel Island (ILG) and Canárias Island (ILC), with data on species richness (CHAO 1 species richness estimator), dominant species (BERGER-PARKER index) and evenness (PIELOU’s index J’).
PRD | ILG | ILC | |
---|---|---|---|
Number of individuals | 1822 | 1465 | 357 |
Species richness (observed) | 21 | 18 | 14 |
Species richness (estimated) | 21.5 ± 3 | 18 ± 1 | 14 ± 3 |
Dominant species | P. mystacalis | P. mystacalis | L. fuscus |
Dominance observed | 14% | 14% | 19% |
Shannon - Wiener (H’) | 2.485 | 2.476 | 2.185 |
Pielou’s index J’ | 0.8165 | 0.8569 | 0.8282 |
Habitat heterogeneity, SHANNON-WIENER diversity index, evenness (Pielou’s index J’) and habitat heterogeneity value for each sampling point in the Parnaíba River Delta.
Sampled points | Diversity index | Pielou’s index J’ | Heterogeneity |
---|---|---|---|
Point I | H’ = 2.279 | J’ = 0.8637 | He = 2.57 |
Point II | H’ = 2.467 | J’ = 0.8708 | He = 2.71 |
Point III | H’ = 2.220 | J’ = 0.8935 | He = 2.28 |
Point IV | H’ = 1.768 | J’ = 0.8502 | He = 1.85 |
Point V | H’ = 1.815 | J’ = 0.7881 | He = 2 |
Point VI | H’ = 2.052 | J’ = 0.8557 | He = 2.14 |
The species richness at the six sampling points varied from 8 to 17 (Tab.
The linear regression analysis evidenced that the habitat heterogeneity of the Restinga environment in the Parnaíba River Delta is able to explain the anuran diversity (R² = 0.9204, p = 0.0015) (Fig.
The Restinga of the Parnaíba River Delta have the fourth highest anuran richness in this type of environment in Brazil and the third in northeastern Brazil (21 species). The Restinga areas with the highest anuran diversity were encountered in the municipalities of Mata de São João (34 species;
The anuran species composition of the Parnaíba River Delta was similar to that reported by
Nevertheless the Restinga of the Parnaíba River Delta differed greatly from Restinga sites in southeastern Brazil (states of São Paulo, Rio de Janeiro and Espírito Santo;
Increased habitat structural complexity results in greater species diversity (
Positive relationships between habitat heterogeneity and anuran diversity have been recorded in different morphoclimatic domains in Brazil, as well in the present study. Habitat heterogeneity has been shown to influence anuran diversity in Restinga areas in northeastern Brazil (
Anuran populations from the Restinga of the Parnaíba River Delta are influenced by habitat complexity and the variety of available microhabitats, in agreement with
Earlier studies highlighted the importance of pond size and edge vegetation to anuran diversity (
We are grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq for the research grant awarded to R.W.A (PQ # 303622/2015-6); Tássia G. P. Lima, Ocivana A. Pereira, and Arthur S. N. Ribeiro for their assistance during fieldwork and Marcelo F. Napoli for the valuable comments on the manuscript. We are grateful to the CNPq/FUNCAP/CAPES for financial support (PROTAX – Processes 440511/2015-1; 5574685/2017; 88882.156872/2016-01); and ICMBio for the collection license (Permit: ICMBio 7770-1, process: 29613). This study was approved by the Animal Ethics Committee of the Universidade Regional do Cariri (Comissão de experimentação e Uso de Animais – CEUA/URCA: process 00026/2015.2).
Anuran species obtained at the Restinga of the Parnaíba River delta, northeastern Brazil. Morphoclimatic domains (
Taxon | Voucher specimens | Sampling points (I–VI) | Morphoclimatic domains |
---|---|---|---|
Bufonidae | |||
Rhinella granulosa (Spix, 1824) | Photographed | I, II | CA, AT |
Rhinella jimi (Stevaux, 2002) | Photographed | All sampling points | CA, AT |
Rhinella mirandaribeiroi (Gallardo, 1965) | Photographed | V | CE |
Hylidae | |||
Dendropsophus minusculus (Rivero, 1971) | URCA-H12120 | I, II, V, VI | WD |
Dendropsophus nanus (Boulenger, 1889) | CZDP473 | I, II, III, V, VI | WD |
Hypsiboas raniceps (Cope, 1862) | URCA-H12115 | I, II, III, V | WD |
Scinax sp. (gr. ruber) | URCA-H12123 | II | No information |
Scinax x-signatus (Spix, 1824) | Photographed | All sampling points | WD |
Leptodactylidae | |||
Adenomera cf. hylaedactyla (Cope, 1868) | URCA-H12125 | V | AM, CE, AT |
Leptodactylus fuscus (Schneider, 1799) | Photographed | All sampling points | WD |
Leptodactylus macrosternum Miranda-Ribeiro, 1926 | Photographed | All sampling points | WD |
Leptodactylus pustulatus (Peters, 1870) | URCA-H12126 | II | CE |
Leptodactylus troglodytes Lutz, 1926 | CZDP485 | II, IV | CA, CE, AT |
Leptodactylus vastus Lutz, 1930 | Photographed | I, II, III | CA, CE, AT |
Physalaemus albifrons Spix, 1824 | Photographed | I, II, III, IV, VI | CA, CE, AT |
Physalaemus cuvieri Fitzinger, 1826 | CZDP470 | II | WD |
Pleurodema diplolister Peters, 1870 | Photographed | I, II, III, IV, VI | CA, CE, AT |
Pseudopaludicola mystacalis (Cope, 1887) | URCA-H12118 | I, II, III, V | WD |
Microhylidae | |||
Elachistocleis piauiensis Caramaschi and Jim, 1983 | URCA-H12124 | I, III, VI | CA, CE |
Odontophrynidae | |||
Proceratophrys caramaschii Cruz, Nunes and Juncá, 2012 | Photographed | VI | CA |
Phyllomedusidae | |||
Pithecopus nordestinus (Caramaschi, 2006) | Photographed | I, II, III, IV | CA, CE, AT |
Anurans recorded at the Restinga of the Parnaíba River Delta, Northeastern Brazil. In brackets, the vouchered specimen with the acronym of the scientific collection followed by the respective institutional registration number and specimen snout-vent length (SVL) in millimeters. Some species only have photographic records. (A) Rhinella granulosa, (B) R. jimi, (C) R. mirandaribeiroi, (D) Dendropsophus minusculus (URCA-H12120, SVL 18.4), (E) D. nanus (CZDP473, SVL 19.2), (F) Hypsiboas raniceps (URCA-H12115, SVL 62.6), (G) Scinax sp. (gr. ruber) (URCA-H12123, SVL 20.1), (H) S. x-signatus, (I) Adenomera cf. hylaedactyla (URCA-H12125, SVL 15.8), (J) Leptodactylus fuscus, (K) L. macrosternum, (L) L. pustulatus (URCA-H12126, SVL 41.2), (M) L. troglodytes (CZDP485, SVL 43.3), (N) L. vastus, (O) Physalaemus albifrons, (P) P. cuvieri (CZDP470, SVL 24.5), (Q) Pleurodema diplolister, (R) Pseudopaludicola mystacalis (URCA-H12118, SVL 11.9), (S) Elachistocleis piauiensis (URCA-H12124, SVL 30.2), (T) Proceratophrys caramaschii, (U) Pithecopus nordestinus. Photographs: Kássio C. Araújo and Ocivana A. Pereira.