NORTH-WESTERN JOURNAL OF ZOOLOGY 12 (1): 78-90 ©NwjZ, Oradea, Romania, 2016 Article No.: e151508 http://biozoojournals.ro/nwjz/index.html
Diversity of lizards and microhabitat use in a priority conservation area of Caatinga in the Northeast of Brazil
Sérgio Luiz da Silva MUNIZ*, Leonardo da Silva CHAVES, Carina Carneiro de Melo MOURA, Eliana-Sofia Fajardo VEGA, Ednilza Maranhão dos SANTOS and Geraldo Jorge Barbosa de MOURA
Universidade Federal Rural de Pernambuco, Departamento de Biologia, Laboratório de Estudos Herpetológicos e Paleoherpetológicos, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos - CEP: 52171-900 - Recife/PE, Brazil. Corresponding author, S.L.d.S. Muniz, E-mail: [email protected]
Received: 24. January 2014 / Accepted: 25. June 2015 / Available online: 29. May 2016 / Printed: June 2016
Abstract. The aim of the present study was to assess the lizard community of the Environmental Protection Area (EPA) of Chapada do Araripe in terms of diversity, spatial distribution, niche breadth and niche overlapping. Three different vegetation types were sampled (Caatinga, cerradão and secondary forest) for a year, with one campaign per month. The collections were conducted by means of an active search, which was limited by time, and pitfall traps. Twenty species belonging to 12 families were recorded. The richness and abundance values were different between the three sample areas. The caatinga area contained the highest number of species (s= 14), whereas the cerradão area exhibited the highest abundance levels (n= 99). The most common lizards were Ameiva ameiva, Colobosaura modesta and Norops brasiliensis in the caatinga, cerradão and secondary forest, respectively. The lizards were more abundant in the dry season compared to the rainy season. Upon comparison of the diversity of the present study with previous studies of other biomes (Amazon rainforest, Atlantic forest, Cerrado and Caatinga), it is notable that the diversity index of the Araripe EPA was high, suggesting that a greater sampling effort in different vegetation areas is the main factor in relation to high richness and diversity in semi-arid areas. Analysis based on null models indicated no significant values of microhabitat overlapping, confirming that the competition for space does not regulate the structure of the studied communities. This may be determined by other factors, including historical factors or the selection of a microhabitat based on diet.
Key words: Lacertilian, assemblage, structure of communities, semiarid, niche overlapping.
Introduction nan 1993). Communities can be defined as the relation- Lizards are used in many ecological studies as ships that exist between populations coexisting in they are relatively easy to find in the wild, they space and time and being subject to constant in- live in different environments, they have a short teraction (Begon et al. 1990). The parameters used life cycle and they are not difficult to identify to describe the structure of a community are the taxonomically (Huey et al. 1983, Pianka and Vitt following: richness; absolute and relative abun- 2003). These animals directly or indirectly influ- dance; spatial distribution and ecological attrib- ence human populations. They are fundamental utes, such as diet and the use of microhabitat elements in the dynamic ecology of natural sys- (Brooks & Mclennan 1993; Mcpeek & Miller 1996). tems, since they occupy specific positions within Communities are structured when these ecological the trophic organization of ecosystems (Huey et al. parameters are arranged regularly among the spe- 1983, Vitt & Pianka 1994, Pianka & Vitt 2003). cies that make up the community (Gotelli 2000, Ecologists believe that competition is one of the 2001). A number of factors have been identified as key mechanisms in determining the relationships exerting a great influence on the abundance, rich- and dynamics of biological systems (Schoener ness and diversity of assemblages, including cli- 1974, Seale 1980, Tilman 1982) and that it exerts a matic, geographic and historical factors, as well as great influence on the structure of a community. the primary productivity of the environment However, other factors may also be determinants, (Schall & Pianka 1978, Gentry 1988, Silva Jr & Sites including the structural complexity of the envi- Jr 1995, Woinarski et al. 1999, Fischer & Linden- ronment, seasonal variations of environmental mayer 2005, Mesquita et al. 2006a, Vitt et al. 2007). conditions, resource sharing, ecological relation- The structure of communities can also be affected ships such as parasitism, and the evolutionary his- by deterministic events (historical/ecological) or tory of the group (Pianka 1973, Brooks & Mclen- random/stochastic events (Gotelli & McCabe Diversity of lizards and microhabitat use in a priority conservation area of Caatinga 79
2002, Gainsburry & Colli 2003). Therefore, two composition, richness and abundance of the casual levels can be observed molding the com- lizard communities in areas of the Chapada do munity: the current ecological processes and the Araripe Environmentally Protected Area (EPA), in historical evolutionary processes (Brooks & order to determine if structuration occurs in rela- Mclennan 1991, Losos 1996). tion to the use of habitat, and to investigate if dif- The structure of lizard communities has been ferences exist between the dry and rainy seasons. previously studied in Brazil (Vitt 1991, Vitt 1995, Mesquita et al. 2006a, Carvalho et al. 2007, Wer- neck et al. 2009). However, studies in the North- Materials and methods east of the country, particularly in areas of caat- Study Areas inga, are scarce, and the most relevant studies The Environmental Protection Area (EPA) of Chapada do were carried out decades ago (Amaral 1937, Van- Araripe covers sections of the States of Ceará, Piauí and zolini 1974, Vanzolini 1976, Vanzolini et al. 1980, Pernambuco (Fig. 1), with an area of ca. 8000 km2 (Viana Vitt 1995). Consequently, the patterns of lizard & Neumann 2002), including the Araripe National Forest community structure in this biome are not well (FLONA-Araripe). It is located within the morphoclimatic understood. domain of caatinga and contains a number of transition The Chapada do Araripe is located in the semi- belts with traces of rainforest (hillside forest) and cerrado (Projeto Araripe 1999). Areas with different phytophysi- arid Northeast region of Brazil. A large portion of ognomies within the Chapada do Araripe EPA were se- its vegetation cover belongs to the morphoclimatic lected: domain of Caatinga, which has different types of Caatinga - 7°39'11.88"S / 39°15'52.71"W: Located in phytophysiognomies (caatinga bushes and trees, the Araripe National Forest (FLONA), within the EPA of remnants of cerrado and remnants of sub- Araripe and near the Municipality of Jardim, State of evergreen tropical forest). It is considered a con- Ceará. It is about 676 m.a.s.l and the predominant vegeta- servation priority because of its biodiversity tion is xerophytic open bushy caatinga, with some rocky outcrops and few trees. The soil is quite sandy and stony, (MMA 2007). Studies on the ecology of herpeto- with a fine layer of leaf litter in the areas with greatest fauna are scarce, particularly those addressing di- vegetation cover. Human interference is notable in certain versity and use of habitat by lizards in different stretches, where firewood has been taken and agriculture phytophysiognomies of caatinga areas (Borges- has been introduced. Nojosa & Caramaschi 2003, Ribeiro et al. 2008, Hillside forest - 7°22'5.12"S / 39°20'18.83"W: Located Loebmann & Haddad 2010, Ribeiro et al. 2012). within the EPA of Chapada do Araripe, at a elevation of 720 One of the main difficulties in proposing con- m, with steep slopes and quite irregular terrain (foot hills), crossed by temporary water courses, which pro- servation strategies or efficient management plans mote siltation of the land in certain stretches. The pre- is the lack of basic studies about the composition dominant vegetation is sub-evergreen pluvio-nebular of species and the use of habitat, particularly in tropical forest, although babussu palms (Orbignya phaler- conservation units of sustainable use (MMA 2003). ata) are abundant, which are characteristic of secondary Therefore, the aim of this work was to study the forests. It has an elevated and dense canopy that protects
Figure 1. Geographical location of Chapada do Araripe, northeast of Brazil, and sampling points: dark grey: Chapada do Araripe EPA; light grey: Chapada do Araripe; Black: Chapada do Araripe National Forest; Star: Caatinga; Triangle: Cerrado; Circle: hillside Forest. 80 S.L.d.S. Muniz et al.
Figure 2. Historical mean of the abiotic data (precipitation, temperature and hu- midity) for the last 13 years (2000 to 2012) in the Environmental Protection Area of Chapada do Araripe (source: Meteorologi- cal station of Barbalha, Ceará, National Institute of Meteorology- INMET).
the interior of the forest from sunlight and direct rain, as of 60 buckets of 30 liters buried with the edge along the well as other medium sized tree species and bushy vege- ground, connected to the surface by a buried plastic can- tation. The constant falling of babussu leaves forms a thick vas (15 x 50 cm), which was used to intercept and direct litter, covered by a thick layer of sparse leaf litter. the animals into the buckets. These buckets were organ- Cerradão - 7°25'27.92"S / 39°17'45.90"W: Located in ized in 12 lines of 5 buckets, with 5 m between them. the interior of the Araripe National Forest, quite high and There were four lines in each phytophysiognomy studied, flat, with an elevation of 940 m and vegetation typical of with a distance of 200 m between them. The buckets re- the cerrado (semi-deciduous xerophyte tropical forest). mained open for five consecutive days of sampling per The forest is dense, with tall trees and open areas, caused month, totaling 7200 days-bucket. by falling trees. The sample area did not contain natural All of the traps were checked twice daily (in the water courses, although there was an artificial reservoir, morning and at the end of the afternoon). The specimens built to trap rainwater, which attracted certain animals. were killed with lidocaine, fixed in 10% formalin, con- The soil has a dense layer of leaf litter which, together served in 70% alcohol and deposited in the Herpetology with the large quantity of trunks and branches that have and Paleoherpetology Collection of the Biology Depart- fallen and decomposed, guarantees shelter for small liz- ment in the Universidade Federal Rural de Pernambuco. ards. Data Analysis Definition of the seasons: dry and rainy The richness of species recorded in each area was consid- The year when the present study was conducted was ered as the total number of species found (s). The abun- atypical, with less rain than usual. Thus, the definitions of dance was considered as the number of individuals col- the dry and rainy season were based upon historical lected (n). Relative abundance was also calculated (Ar). mean values from the years 2000 to 2012 (Fig. 2), available In order to determine whether the present study in the database of the Instituto Nacional de Meteorologia conducted satisfactory sampling, the real richness, ob- (INMET) in Barbalha, Ceará. A minimum value of 60 mm tained from the estimators (ACE, jack1, Chao1 and boot- was established (historical mean) to consider the period strap) was compared with the observed richness. To do as rainy and values below this were considered as dry. so, rarefaction curves of the species were created, with Consequently, the rainy season was considered as the 500 randomizations generated based on the matrix of months between December and May, while the remain- abundance data for each area and for each sampling pe- der of the year was considered as the dry season. riod (12 samples). This was performed using EstimateS® 8.0 (Colwell 2005). Methodology of the sampling The Shannon-Wiener index (H'), which gives greater Data collection was performed monthly between August weight to rare species, was used to assess diversity (Ma- 2011 and July 2012, with each campaign lasting 5 days. gurran 1988). Pielou’s evenness index was calculated to Two methodologies were used: an active search limited indicate how evenly the abundance of the species was by time and a passive search using pitfall traps. distributed. This index ranges from 0 to 1 (Wootton 1995). The active searches were conducted monthly by four The Morisita index, which attributes greater weight to the observers/collectors, with each campaign involving 6 h of most abundant species was used to analyze the similarity searching, for 3 days (one day for each collection area). between the locations in terms of species composition, us- This involved 3 h in the morning (8 to 11h) and 3 h at ing Past 2.04 (Hammer et al. 2000) and posterior cluster- night (18 to 21h), totaling 72 h/person of sampling per ing analysis. The chi-squared test was used to assess the campaign. The most varied types of habitats and micro- occurrence of significant differences between the rainy habitats used by lizards were explored, as described by and dry seasons for abundance and richness, with the Vitt et al. (2003). level of significance set at (p) ≤ 0.05. The passive collections were conducted using pitfall Microhabitats were analyzed considering only the traps with drift-fences, following Gibbons & Semlitsch lizards found with the active search method. Once ob- (1981) and Corn (1994). The pitfall traps were composed Diversity of lizards and microhabitat use in a priority conservation area of Caatinga 81 served in the environment, they were attributed to the Results categories for the recorded species. Niche breadth values were calculated using the inverse of the Simpson index Richness, abundance and diversity (Simpson 1949). The interval of variation of the index was A total of 238 lizard specimens were recorded in from 1.0 to 11. Only the most common species were in- cluded in the niche breadth analysis (n > 5). Overlapping the three samples areas, representing 20 species microhabitat use was calculated using Pianka’s equation from the following 12 families: Gekkonidae (3 (1973). The interval of variation of this index was from 0.0 spp.), Phyllodactylidae (2 spp.), Sphaerodactylidae (no overlapping) to 1 (complete overlapping).. The exis- (1 sp.), Mabuyidae (1 sp.), Dactyloidae (1 sp.), Ig- tence of non-random overlap niche patterns was tested uanidae (1 sp.), Leiosauridae (1 sp.), Polychrotidae with the niche overlap module of EcoSim 7.0 (Gotelli & (1 sp.), Tropiduridae (2 spp.), Diploglossidae (1 Entsminger 2004). The sample observed was not consid- sp.), Gymnophthalmidae (3 spp.), and Teiidae (3 ered to be a random sample of the environment if the level of significance was (p) ≤ 0.05. Past 2.04 was used to spp.) (Table 1). develop the dendogram of the lizard species in relation to The sampling effort for the present study cor- niche overlapping (Hammer et al. 2000). responded to 86,400 hours/bucket for the passive collection method (pitfall traps) and 840 hours/man (number of hours multiplied by 4 in- vestigators) for the active collection method, total- ing 87,264 h for both methods. The active collec-
Table 1. Species of lizards recorded in the sampling areas of the Environmental Protection Area of Chapada do Araripe between August/2011 and July/2012. Environments studied: caa- caatinga; mat- hillside forest; cer- cerradão. (n): abundance.
Taxonomic group vegetation types (n) period dry (n) period rainy Squamata/Lizards Gekkonidae Hemidactylus brasilianus (Amaral, 1935) cer 2 1 Hemidactylus mabouia (Moreau de Jonnès, 1818) caa, mat 0 3 Lygodactylus klugei (Smith, Martin & Swain, 1977) caa, mat 1 3 Phyllodactylidae Gymnodactylus geckoides Spix, 1825 caa 11 4 Phyllopezus pollicaris (Spix, 1825) caa, mat 1 3 Sphaerodactylidae Coleodactylus meridionalis (Boulenger, 1888) mat 5 3 Mabuyidae Copeoglossum arajara (Rebouças-Spieker, 1981) cer, mat 20 2 Dactyloidae Norops brasiliensis (Vanzolini & Williams, 1970) cer, mat 34 12 Iguanidae Iguana iguana (Linnaeus, 1758) caa, cer, mat 1 4 Leiosauridae Enyalius bibronii Boulenger, 1885 cer 0 1 Polychrotidae Polychrus acutirostris Spix, 1825 caa 1 1 Tropiduridae Tropidurus hispidus (Spix, 1825) caa, mat 7 3 Tropidurus semitaeniatus (Spix, 1825) caa, mat 3 1 Diploglossidae Diploglossus lessonae Peracca, 1890 caa 0 1 Gymnophthalmidae Micrablepharus maximiliani (Reinhardt & Luetken, 1862) caa, cer, mat 16 8 Vanzosaura multiscutata (Amaral, 1933) caa, cer 8 1 Colobosaura modesta (Reinhardt & Luetken, 1862) cer, mat 44 1 Teiidae Ameiva ameiva (Linnaeus, 1758) caa, mat, cer 17 12 Ameivula ocellifera (Spix, 1825) caa, cer 2 0 Salvator merianae Duméril & Bibron, 1839 caa, mat 1 1 82 S.L.d.S. Muniz et al.
Figure 3. Absolute abundance of the lizard species recorded in the sampling areas of the Environmental Protection Area of Chapada do Araripe between August/2011 and July/2012: A- total abundance; B- caatinga abundance; C- hill- side forest abundance; D- cerradão abundance.
tion method recorded a total of 20 species and the September and October (s=11) and the lowest passive collection method recorded 14 species. number recorded in March (s=3) (Fig. 4). With re- Only Diploglossus lessonae, Lygodactylus klugei, gards to abundance, the months with the highest Phyllopezus pollicaris, Gymnodactylus geckoides, and values were October (n=35) and November (n=38), Polychrus acutirostris were not captured in the whereas the month with the lowest value was traps. These species were found in the active March (n=4). High abundance and richness values search. The lizard Hemidactylus mabouia was only occurred in September and October, which corre- recorded around residences in caatinga and hill- sponds to the end of the dry period (Fig. 4). side forest areas and was not really found in the forest. Among the sample areas, caatinga contained the largest number of species (s= 14), followed by hillside forest (s= 13) and cerradão (s= 10). The most abundant species in the sample were Colo- bosaura modesta and Norops brasiliensis (Fig. 3A). Upon comparison of the abundance between the areas, the cerradão was the area with the greatest number of specimens (n=99), followed by the hill- side forest (n=75) and caatinga (n=64). Ameiva ameiva was the most abundant lizard in the caat- inga (Ar= 27%) (Fig. 3B), whereas Norops brasilien- Figure 4. Monthly variation of abundance and richness of the lizards recorded in the sampling areas of the Envi- sis was the most abundant in the hillside forest ronmental Protection Area of Chapada do Araripe be- (Ar= 36.5%) (Fig. 3C) and Colobosaura modesta was tween August/2011 and July/2012. the most abundant in the cerradão (Ar= 46.3%) (Fig. 3D). Only three species were found in all of the environments studied: Ameiva ameiva, Iguana In the dry season (August-November/2011 iguana, and Micrablepharus maximiliani. and June-July/2012), 16 species and 173 specimens The monthly richness ranged from 3 to 11, were captured. In the rainy season (Decem- with the highest number of species recorded in ber/2011-May/2012), 19 species and 65 specimens
Diversity of lizards and microhabitat use in a priority conservation area of Caatinga 83
Figure 5. Rarefaction curves of the species obtained through richness estimators from the total sampling effort and from each area studied in the Environmental Protection Area of Chapada do Araripe between August/2011 and July/2012: A- Total; B- caatinga; C- hillside forest; D- cerradão.
were captured. The chi-squared test (χ2) confirmed found in the cerradão (s= 10) was closest to the es- no significant differences in richness (χ2=0.118; timator Bootstrap (s= 11.47), and quite different p=0.7316), although abundance was significantly from ACE (s= 17.64), Chao 1 (s= 16) and Jack 1 (s= higher in the dry season (χ2=47.61; p=0.0001), par- 13.67) (Fig. 5). The rarefaction curve for this area ticularly in relation to C. modesta (n=44), which ex- came close to stabilization (Fig. 6). hibited a significant difference (χ2=41.089; Table 2 displays the values for Shannon’s di- p=0.0001) in the wet season (n=1), and N. brasilien- versity index (H’) and Pielou’s evenness index. sis (n=33), which also exhibited a significant dif- Morisita’s similarity index (absence and presence ference (χ2=9,80; p=0,0017) in the wet season method) revealed an 8.63% similarity between (n=12). caatinga and hillside forest, 21.06% similarity be- The general richness of species found (s= 20) tween caatinga and cerradão, and 36.06% similarity was very similar to the figures obtained with the between hillside forest and cerradão. The latter re- richness estimators ACE (s= 21.98), Chao 1 (s= sult was the highest in terms of similarity. 20.75), Jack 1 (s= 22.75) and Bootstrap (s= 21.62) Based on Morisita’s similarity index, the pre- (Fig. 5). Upon analysis of the rarefaction curve, it sent study was compared with other studies per- is clear that at the end of the sampling, the curve is formed in caatinga and in other biomes (Fig. 7). very close to stabilizing, reaching its asymptote The greatest similarity was found with the studies and confirming that the sample effort satisfied the of Vitt (1995) (72.72%), Loebmann & Haddad research (Fig. 6). (2010) (70.83%) and Werneck et al. (2009) (57.89%). The richness of species found for caatinga This comparative analysis indicates that the rich- (s=14) was closer to the estimators Chao 1 (s=16.5) ness of the area studied could be considered high. and Bootstrap (s=16.74) than to ACE (s= 20.15) The areas that exhibited the greatest richness were and Jack 1 (s= 20.42) (Fig. 5). The rarefaction curve the following: the Amazon rainforest (s=29) (Ma- of this area did not stabilize (Fig. 6). The richness cedo et al. 2008); caatinga with various phyto- of species found in the hillside forest (s= 13) was physiognomies (s=28) (Loebmann & Haddad closest to the estimator Bootstrap (s= 15.61) and 2010); the present study (s=20); cerrado (s=18) quite different from ACE (s= 22.6), Chao 1 (s= (Werneck et al. 2009); Atlantic forest (s=13) 20.5) and Jack 1 (s= 19.42) (Fig. 5). The rarefaction (Santana et al. 2008) and xeric caatinga (s=13) (Vitt curve for this area did not come close to reaching 1995). its asymptote (Fig. 6). The richness of species 84 S.L.d.S. Muniz et al.
Figure 6. Rarefaction curves representing the accumulative richness of the lizard species from the total sampling effort and from each area studied in the Environmental Protection Area of Chapada do Araripe between August/2011 and July/2012: A- Total; B- caatinga; C- hillside forest; D- cerradão.
Table 2. Richness and abundance values, Shannon’s diversity index (H’) and Pielou’s evenness index (J’) for the lizard communities collected in the sampling areas of the Environmental Protection Area of Chapada do Araripe between August/2011 and July/2012.
Local Richness Abundance H'(loge) J' junction of the three areas sampled 20 238 2.4339 0.8011 caatinga 14 64 2.128 0.8065 hillside forest 13 75 1.909 0.7442 cerradão 10 99 1.63 0.708
Figure 7. Similarity dendogram of the lizard communities studied in different morphoclimatic domains: xeric caatinga (Vitt 1995); Atlantic forest (Santana et al. 2007); Amazon rainforest (Macedo et al. 2008); cerrado (Wer- neck et al. 2009) and caatinga of various vegetation types (Loebmann and Haddad, 2010). Diversity of lizards and microhabitat use in a priority conservation area of Caatinga 85
Table 3. Abundance, niche breadth (Ln) and microhabitats of the lizard species found during active searches in the studied areas of the Environmental Protection Area of Chapada do Araripe between August/2011 and July/2012: A- soil; B- on leaf litter; C- under leaf litter; D- on a fallen trunk; E- under a fallen trunk; F- tree trunk; G- rock; H- tree
bark; I- wall (civil construction); J- tree branch; L- bush. Ln: species that obtained n > 5.
Microhabitats Species Ln A B C D E F G H I J L Gekkonidae Hemidactylus brasilianus - 1 Hemidactylus mabouia - 3 Lygodactylus klugei - 1 3 Phyllodactylidae Gymnodactylus geckoides 1.72 1 3 11 Phyllopezus pollicaris - 4 Sphaerodactylidae Coleodactylus meridionalis - 1 Mabuyidae Copeoglossum arajara - 1 1 1 Dactyloidae Norops brasiliensis 2.39 8 3 3 Iguanidae Iguana iguana - 3 Polychrotidae Polychrus acutirostris - 1 Tropiduridae Tropidurus hispidus - 3 1 Tropidurus semitaeniatus - 3 Diploglossidae Diploglossus lessonae - 1 Gymnophthalmidae Colobosaura modesta 1 7 Micrablepharus maximiliani 2.91 2 2 2 4 Vanzosaura multiscutata - 1 1 1 1 Teiidae Ameiva ameiva 1.8 2 4 Ameivula ocellifera - 2 Salvator merianae - 1
Use of microhabitat, niche breadth were records of species without overlapping, with and overlapping low, moderate and high levels of overlapping, as In total, 11 microhabitat categories were used by well as with complete overlapping. Species of the the lizards (Table 3): soil; above the leaf litter; un- Gekkonidae family did not exhibit any overlap- der the leaf litter; on fallen trunks; under fallen ping (0.00), whereas the species of the Phyllodac- trunks; tree trunks; rocks; tree bark; walls (civil tilydae and Tropiduridae exhibited high levels of construction); tree and bush branches. The niche overlapping. The Gymnophthalmidae exhibited breadth values, in relation to the use of microhabi- low levels of overlapping, as in the cases of C. tat, alternated between 1 and 2.91 (Table 3). modesta and M. maximiliani (0.21), moderate over- Niche overlapping ranged from 0.00 (no over- lapping for V. multiscutata and C. modesta (0.50) lapping) to 1.00 (complete overlapping) (Table 4, and high levels of overlapping for the lizards M. Fig. 8). The species that exhibited complete over- maximiliani and V. multiscutata (0.85). The Teiidae lapping, in terms of the use of microhabitat, were contained species with no overlapping, such as S. the following: C. modesta and C. meridionalis (under merianae and A. ocellifera (0.00), species with mod- leaf litter); I. iguana and P. acutirostris (tree erate overlapping, A. ameiva and S. merianae (0.45), branches); and P. pollicaris and T. semitaeniatus and high levels of overlapping for the lizards A. (rocks). ameiva and A. ocellifera (0.89) (Table 4, Fig. 8). Overlapping values recorded for species of the The mean niche overlap value was insignifi- same family varied significantly (Table 4). There cant when compared with the simulated mean
86 S.L.d.S. Muniz et al.
Table 4. Overlap matrix for the use of the microhabitat based on the Pianka overlap index for lizards in the studied ar- eas of the Environmental Protection Area of Chapada do Araripe between August/2011 and July/2012.
A. a. A. o. C. a. C. me. C. mo. D. l. G. g. H. b. H. m. I. i. L. k. M. m. N. b. P. a. P. p. S. m. T. h. T. s. V. m. A. ameiva - 0.89 0.52 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.38 0.79 0.00 0.00 0.45 0.00 0.00 0.67 A. ocellifera - - 0.58 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.21 0.88 0.00 0.00 0.00 0.00 0.00 0.50 C. arajara - - - 0.58 0.58 0.00 0.05 0.00 0.00 0.00 0.00 0.24 0.70 0.00 0.00 0.00 0.00 0.00 0.58 C. meridionalis - - - - 1.00 0.00 0.00 0.00 0.00 0.00 0.00 0.21 0.00 0.00 0.00 0.00 0.00 0.00 0.50 C. modesta - - - - - 0.00 0.00 0.00 0.00 0.00 0.00 0.21 0.00 0.00 0.00 0.00 0.00 0.00 0.50 D. lessonae ------0.26 0.00 0.00 0.00 0.00 0.85 0.00 0.00 0.00 0.00 0.00 0.00 0.50 G. geckoides ------0.00 0.00 0.00 0.00 0.22 0.03 0.00 0.96 0.00 0.91 0.96 0.13 H. brasilianus ------0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 H. mabouia ------0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.32 0.00 0.00 I. iguana ------0.95 0.00 0.00 1.00 0.00 0.00 0.00 0.00 0.00 L. klugei ------0.00 0.00 0.95 0.00 0.00 0.00 0.00 0.00 M. maximiliani ------0.19 0.00 0.00 0.43 0.00 0.00 0.85 N. brasiliensis ------0.00 0.00 0.00 0.00 0.00 0.44 P. acutirostris ------0.00 0.00 0.00 0.00 0.00 P. pollicaris ------0.00 0.95 1.00 0.00 S. merianae ------0.00 0.00 0.50 T. hispidus ------0.95 0.00 T. semitaeniatus ------0.00
Figure 8. Similarity dendogram in relation to niche overlapping of lizards collected in the studied areas of the Chapada do Araripe EPA between August/2011 and July/2012.
(observed mean = 0.15; simulated mean= 0.13; p= ready been reported in the domain of caatinga and 0.97). Therefore, it is possible to conclude that the a number are known to exist in Atlantic forest and use of microhabitat is not the factor responsable cerrado, including C. meridionalis, A. ameiva, S. for structuring the community. merianae, T. hispidus, N. brasiliensis and C. modesta (Rodrigues 2003, Faria et al. 2007, Santana et al. 2008, Werneck et al. 2009). Rodrigues (2005) listed Discussion 73 species of lizards for caatinga areas, including high altitude swamps (locally known as “Brejos de Richness, abundance and diversity Altitude”: humid forest remnants scattered The majority of species recorded herein have al- throughout Caatinga lowlands). The richness of Diversity of lizards and microhabitat use in a priority conservation area of Caatinga 87 lizards found in the sampled area of the EPA of seasonality is an important factor that can influ- Chapada do Araripe (s= 20) represents 27% of the ence the composition of lizard communities. Gald- lizard species listed by Rodrigues (2005). ino et al. (2003) found no significant differences The richness recorded herein is similar to the between the seasons for abundance and richness. values found in other studies of caatinga areas, However, according to Campbell and Christiman which found between 10 and 28 species (Vanzolini (1982), the dry and rainy seasons can in fact de- 1974, Rodrigues 1986, Vitt 1995, Rocha & Rodri- crease the abundance and richness of lizards if gues 2005, Santos et al. 2008, Loebmann & Haddad there is a period of high rainfall or intense 2010). Despite great differences in the capture ef- drought. forts employed and the variety of environments Shannon’s diversity index (H’) also indicates assessed in these studies, it is possible to compare the degree of complexity of the structure of com- them in terms of richness. The study that involved munities (Ludwig and Reynolds, 1988). Upon the greatest collection effort (two years and three comparison of the diversity of the present study months) and which assessed the greatest number with those assessing other biomes, the index of the of phytophysiognomies (relictual rainforest, high- present study was: higher than that of other stud- altitude caatinga, arboreal caatinga, low-altitude ies conducted in caatinga areas and ecosystems as- caatinga, cerrado) reported a richness of 28 species sociated with Atlantic forest (Vitt 1995, Carvalho (Loebmann & Haddad 2010). Therefore, these fac- et al. 2007); similar to studies of cerrado (Werneck tors could have led to the high levels of richness. et al. 2009) and lower than studies conducted in The values obtained by the richness estimators the Amazon rainforest (Macedo et al. 2008). These for the three areas together were very similar to data also support the idea that a greater sampling the observed richness, suggesting satisfactory effort in different phytophysiognomies (address- sampling. However, the sampling was not com- ing greater niche richness) is the principal factor pletely satisfactory in certain areas: a longer sam- involved in the detection of an elevated level of pling period for each area in isolation was re- richness and consequently, elevated diversity in quired. The estimator Chao 1 indicated that 96% of relictual islands of the forest and/or enclaves of the species were sampled, whereas ACE and Boot- other types of mesic landscape within semi-arid strap indicated that 92% of the species were sam- regions. pled. Jack 1 reported that 88% of the lizard species According to Ludwig & Reynolds (1988), were sampled using the methodology and effort of Pielou’s evenness index (J’) indicates the level of the present study. According to Walther and distribution of individuals in their habitat. Results Morand (1998), the estimator Jack 1 is considered of 0.5 and above suggest a uniform distribution to be the most precise and accurate estimator of among species within the same population. The species richness. region studied recorded a very high evenness Upon analyzing the richness and abundance value (J’=0.8011). Therefore, these species are well values obtained in relation to the seasons (drought distributed within the sample, in spite of the fact and rain), it became clear that the dry season is the that some were dominant (C. modesta, N. brasilien- period of greater abundance, revealing a statisti- sis and A. ameiva). The majority exhibited a uni- cally significant result when compared with the form distribution. rainy season. The same cannot be said for rich- With regards to the similarity between the ness. Certain species were only found during one studied areas, the Morisita index confirmed a season, such as V. multiscutata and A. ocellifera, greater similarity between the hillside forest and which were only found in the dry season, and E. the cerradão, based on the larger number of indi- bibronii, D. lessonae and P. acutirostris, which were viduals, the presence of species that were exclu- only found in the rainy season. During drought, sive to these areas (C. arajara, N. brasiliensis and C. there was a considerable increase in abundance, modesta) and the fact certain species, such as G. particularly in the C. modesta and N. brasiliensis geckoides, P. acutirostris and D. lessonae, were only species. The present study corroborates the find- found in caatinga areas. These species are typical of ings of a number of previous studies, indicating places with the characteristic features of mesic ar- that lizards have a close relationship with tem- eas of caatinga. perature and precipitation (Vitt et al. 1981, Vitt et Grouping analysis was carried out using the al. 1991, Huey et al. 2003). Morisita index for certain areas in different mor- According to Fitzgerald et al. (1999), climatic phoclimatic domains, based on lists available in 88 S.L.d.S. Muniz et al. previous studies (Vitt 1995, Santana et al. 2008, meridionalis was only found in places with more Macedo et al. 2008, Werneck et al. 2009, Loebmann humid and compact leaves, typical of forested ar- & Haddad 2010). The present study exhibited a eas (Rodrigues 2003), whereas C. modesta was greater similarity with the areas sampled in the more common in areas with drier and denser leaf caatinga domains, joining the studies of Vitt (1995) litters. Norops brasiliensis exhibited high levels of and Loebmann & Haddad (2010). However, they overlapping with species of the Teiidae famliy (A. shared common taxa, distributed from the cer- ameiva, A. ocellifera and S. merianae). However, this rado, Atlantic forest and even the Amazon forest relationship does not mean that they compete, domains, although the latter exhibited less similar- since the teiids inhabit more open areas than N. ity. brasiliensis, which prefers the interior of the forest and uses more categories of microhabitats (Vitt et Use of microhabitat, niche breadth al. 1997, Vitt et al. 2001, Werneck et al. 2009). and overlapping Similarly, I. iguana, P. acutirostris, and L. klugei Using different types of habitats and microhabitats exhibited high levels of overlapping. Lygodactylus enables the co-existence of potential competing klugei was found on the branches of trees and also species. Consequently, they can delineate the used the trunk as a microhabitat resource. Iguana structure of a community (Pianka 1973, Smith & iguana and P. acutirostris used the same microhabi- Ballinger 2001). After the competitive period, two tats but they have a different diet. The former’s or more species can share the same habitat, pro- diet is mainly based on leaves whereas the latter is vided that each one occupies the microhabitat that insectivorous (Vitt & Lacher Jr. 1981, Troyer 1984). is most suited to their adaptations or which has They may in fact compete for space, but this com- more advantages (Vanhooydonck et al. 2000). petition is softened by the diet component. Micrablepharus maximiliani was the species Our results are similar to data found in the lit- with the largest niche breadth and plasticity. This erature (Vitt & Zani 1996, Vitt & Zani 1998, Mes- species was observed using different types of mi- quita et al. 2006a) in terms of phylogenetically crohabitats, although most were found under close species using available resources in similar fallen trunks in the forest and a strong association ways. At least in terms of habitat, this pattern was with this resource was recorded. This is contrary repeated in the present study. According to Pianka to the literature, in which a number of studies in- (1973), habitat is the most shared resource, par- dicate that this species uses anthills as one of their ticularly between sympatric species. Therefore, main microhabitats in the cerrado (Vitt 1991, Vitt other factors, such as food, are the main segrega- & Caldwell 1993, Mesquita et al. 2006b). This pat- tive agent. Studies on the diet of these species tern appears to repeat itself in areas of caatinga could also provide evidence of this. The absence of (Vitt 1995). structure in terms of the use of the microhabitat A number of species exhibited high levels of suggests a lack of competitive interaction in the overlapping, such as members of the families spatial component. Thus, the use of microhabitats Phyllodactylidae (G. geckoides and P. pollicaris) and could be determined by other factors, such as his- Tropiduridae (T. hispidus and T. semitaeniatus). Al- torical factors or the selection of a microhabitat though these species exhibited high levels of over- based on diet (Mesquita et al. 2006a). lapping, P. pollicaris is nocturnal and exhibits tem- poral segregation. Therefore, it does not interact directly with the tropidurids or with G. geckoides (Vitt 1995). Tropidurid species exhibit preferences Acknowledgements. The authors would like to thank the for rocks (saxicolous habit), indicating that there is Fundação de Amparo à Ciência e Tecnologia de Pernambuco (FACEPE) for financing the PRONEM project (APQ 1264- direct competition for space, in which T. semitae- 2.05/10) and the anonymous reviewer of this manuscript. niatus possibly has an advantage as it is more adapted for these locations. Perhaps this explains why T. hispidus exhibits a larger niche breadth, in- habiting a greater range of microhabitats (Vitt References 1995). Other lizard species also exhibited high levels Amaral, A. 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