NORTH-WESTERN JOURNAL OF ZOOLOGY 12 (2): 271-285 ©NwjZ, Oradea, Romania, 2016 Article No.: e151510 http://biozoojournals.ro/nwjz/index.html
Autoecology of Phyllomedusa nordestina (Anura: Hylidae) in areas of the Caatinga and Atlantic Forest in the State of Sergipe, Brazil
Francis Luiz Santos CALDAS1,*, Bruno Duarte da SILVA2, Rafael Alves dos SANTOS2, Crizanto Brito DE-CARVALHO2, Daniel Oliveira SANTANA1, Fabíola Fonseca Almeida GOMES2 and Renato Gomes FARIA2
1. Programa de Pós-Graduação em Ciências Biológicas, Universidade Federal da Paraíba, Cidade Universitária - CEP: 58051-900 - João Pessoa - PB - Brasil. 2. Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal de Sergipe, Cidade Universitária Prof. José Aloísio de Campos Av. Marechal Rondon, s/n Jardim Rosa Elze - CEP 49100-000 - São Cristóvão/SE, Brasil. *Corresponding author, F.L.S. Caldas, Tel.: +381 11 2637024; Fax: +381 11 2638500, E-mail: [email protected]
Received: 22. December 2014 / Accepted: 09. October 2015 / Available online: 09. October 2015 / Printed: December 2016
Abstract. Understanding of how environmental dynamics affect the ecological niche of populations is one of the great aims ecological research. Amphibian populations are taking part in a series of complex interactions with the environment. The aim of this study was to investigate potential differences in the use of spatial, temporal and trophic resources, and variations in size, mass, and the reproductive cycles of Phyllomedusa nordestina populations. These were studied from December 2009 to November 2010 in two different biomes, both Conservation Units: the Monumento Natural Grota do Angico (MNGA – Caatinga, a tropical semiarid climate); and the Refúgio de Vida Silvestre Mata do Junco (RVSMJ – Atlantic Forest, a tropical humid climate, in Sergipe State, Brazil). Within each area, we found the specimens in lentic environments, with grass and shrub stems as main substrates. Most specimens were calling next to water bodies, generally in open places with predominantly herbaceous vegetation. Among the consumed foods items, spiders were the most important resource in the MNGA, whereas insect larvae where the most important in the RVSMJ. Regarding the reproductive period, Caatinga specimens were present between February and July, whereas in the Atlantic Forest they were observed between January and November. This longer reproductive period may be related to the regular and evenly distributed rainfall characterizing the Atlantic Forest. The specimens in the Atlantic Forest were slightly smaller than were those from Caatinga. The reason of such differences might reside in differences in habitat types, as well as in the longer reproductive period in the Atlantic Forest area, and investments related to reproduction.
Key words: niches, ecology, biome, anurans, morphometry.
Introduction tion, not only relating to the development of tad- poles, but also because of the lack of suitable call- Trying to understand how environmental dynam- ing sites, and to oviposition (Bentley 1966, Santos ics affect the ecological niche of populations, i.e. et al. 2007a). function that associates reproductive success of The reproductive strategies adopted by am- the organism with its environment, in other words phibians consist of a combination of physiological, the ecological conditions that permit the mainte- morphological, and functional attributes, which nance of stable population rates, has always been act together and aim to produce a considerable one of the main aims of ecology (Hutchinson 1957, amount of descendants for subsistence in condi- Soberón 2007). tions provided by the environment. Additionally, Water availability is the critical component of reproductive patterns can be modified by natural most amphibian habitats (Dayton & Fitzgerald selection, which results in an increase in fitness 2006). Among the structural abiotic factors of ma- that results in physiological and morphological jor importance for amphibian populations and adaptations (Duellman & Trueb 1994, Lai et al. communities are the chemical and physical prop- 2003). Thus, the lifecycles of amphibian popula- erties of water (Moore 1939, Lima & Peixoto 2007), tions within the same species are affected in dis- the frequency of pond inundation (Babbitt et al. tinct ways, depending on the conditions that they 2006), the size of water bodies and the duration of experience (Dunham & Overall 1994, Schäuble the hydroperiod (Welborn et al. 1996, Eterovick & 2004). Varying seasonal conditions influence the Sazima 2000, Eterovick & Fernandes 2001, 2002). availability of resources and affect the frogs’ diet Thus, the water factor can directly affect reproduc- (Berazategui et al. 2007, Kovács et al. 2007), as well 272 F.L.S. Caldas et al. as reproduction (Bertoluci 1998, Arzabe 1999, San- size, mass, and the reproductive cycles of P. nord- tos et al. 2007a). Therefore, the use of microhabi- estina populations in two localities in the Caatinga tats is more related to morphological adaptations, and Atlantic Forest biomes in Sergipe State, Brazil. and as a result of local changes, tends to conserva- Few differences in the exploitation of spatial re- tism (Duellman 1967, Crump 1971, Hödl 1977). sources are expected in either biome, since the use The different water regimes found in the Caat- of specific microhabitats for calling and breeding inga and Atlantic Forest biomes provide good is essential for anuran fitness (Townsend 1989). conditions for studying the influence of environ- Therefore, late ecological factors, together with the mental characteristics on the biological strategies water conditions in each environment can affect used by distinct populations of anurans of the many food items, as well as reproduction and en- same species. The Caatinga biome is located in ergy use for growth and calling activities (Janzen northeastern Brazil, between 2º54'N to 17º21'S (an & Schoener 1968, Wolbright 1983, Arzabe 1999). estimated area of approximately 800,000 km², with a tropical semiarid climate and typically two sea- sons: a very dry one, and another with moderate, Materials and Methods irregular rains (Nimer 1972, Chiang & Koutavas Phyllomedusa nordestina populations were studied from 2004, Leal et al. 2005). The Atlantic Forest is pre- December 2009 to November 2010 in two biomes in Ser- sent throughout the coast from Rio Grande do gipe State, Brazil: the Caatinga (the Conservation Unit Norte State to Rio Grande do Sul State, and ex- Monumento Natural Grota do Angico – MNGA), and the tending into the country, and covering an area of Atlantic Forest (the Conservation Unit Refúgio de Vida nearly 15% of the total national territory Silvestre Mata do Junco – RVSMJ), (Fig. 1). Monthly col- (Steinmetz 2004, Prochnow et al. 2006). The Atlan- lections on three consecutive nights were made in each area, in an attempt to maintain the smallest possible time tic forest has a high rainfall index as a result of interval between the sampling of each Conservation unit. ocean winds that carry humidity, which are drawn towards continental regions and reach the coastal mountain chains, where rainfall occurs (Ab’Sáber 1977, Steinmetz 2004, Tonhasca-Júnior 2005). However, although the Atlantic Forest sustains one of the highest species richness and endemism rates in the world, the biome has suffered from fragmentation over time, which has resulted in large forest loss, which is directly associated with the strong impact of human activity in these envi- ronments (MMA, 2007; Ribeiro et al., 2009). Phyllomedusa nordestina belongs to the P. hypo- chondrialis species group (formed by allopatric species of small size); it is a dimorphic species, with males being slightly smaller than females and Figure 1. Delimitation of the area of the Conservation it occurs in northeastern Brazil, in Caatinga areas Units Monumento Natural Grota do Angico (MNGA) or in those that are influenced by this biome (in and Refúgio de Vida Silvestre Mata do Junco (RVSMJ) located in Sergipe/Brazil. The numbers 1-6 correspond regions that are next to the Atlantic Forest and the to water bodies sampled in MNGA and 7-12 in RVSMJ. Cerrado, for example), and is found in the States of Piauí, Ceará, Rio Grande do Norte, Paraíba, Pernambuco, Alagoas, Sergipe, Bahia and Minas The Monumento Natural Grota do Angico (MNGA; Gerais (Caramaschi 2006). Because natural history 37°40'W; 09°39'S) covers an area of 2,182 ha and is located data for the species is lacking (Angulo 2008) and it within the morphoclimatic domain of the Caatinga (Ab’Sáber, 1977), between Poço Redondo and Canidé do is present in both the Caatinga and Atlantic Forest São Francisco municipalities, in the high “Sertão” of Ser- biomes (Morato et al., 2011; Gouveia & Faria 2015), gipe, next to the São Francisco river (Ruiz-Esparza et al. P. nordestina is an interesting model to be investi- 2011). The climate is semiarid, with little and irregular gated in this study. rainfall (Nimer 1972). The mean rainfall is 500 mm per The aim of the present study was to investi- year, usually from April to August (Ruiz-Esparza et al., gate potential differences in the use of spatial, 2011). The MNGA shows basically a unique phytophysi- ognomy, which is formed by vegetation in the process of temporal, and trophic resources and variations in
Autoecology of Phyllomedusa nordestina 273 secondary succession, and denser vegetation, laid over length (SVL) was measured using a digital caliper (0.01 mountain areas with typical Caatinga species (e.g., Poin- mm precision). All individuals that exhibited calling ac- cianella pyramidalis (Tul.) L. P. Queiroz, and Jatropha mol- tivity were considered as males, and females were re- lissima (Pohl Baill), near intermittent streams, and in the corded as individuals that were observed in amplexus, in wood neighbouring the São Francisco river (Silva et al. breeding activity or clearly contained eggs in their abdo- 2013). Nowadays, the Refúgio de Vida Silvestre Mata do men. The sex of the collected specimens were also deter- Junco (RVSMJ; 37°03'30''W; 10°32'30''S) consists of 1,520 mined by observations of the gonads. ha, and is in the southern part of the Capela municipality, Clutches that were attached to plants were identified Sergipe. It represents a fragment formed by areas of vege- to the smallest possible taxonomical level. The eggs of tation with distinct arboreal extracts, forming a secondary clutches without signs of drying or plundering were wood with different levels of anthropic activity and re- counted. generation (Malta et al. 2011). The region is the second The climate variables of mean monthly temperature, largest of Sergipe State, and is inserted within the Atlantic relative air humidity and accumulated monthly rainfall Forest area. It also houses the rising of the Lagartixo were taken from the Plataforma de Coleta de Dados Cli- River, the main water resource of the protected area and a matológicos – PCD, in Poço Redondo municipality, at a tributary of the Japaratuba River (Santos et al. 2007b). The distance of 15 kilometres from the MNGA, and from precipitation is high, as is that in other Brazilian coastal PCD, in Capela municipality, at the distance of 2 km from woods (Santos et al. 2007b). the RVSMJ. Twelve water bodies were sampled; six in each area For statistical analyses, data were tested for normal- (MNGA – three ponds, one swamp, one artificial tank and ity using the Shapiro–Wilk test, to determine the type of one stream, all temporary; RVSMJ – three ponds and one test to be subsequently adopted. To analyse the influence swamp, all temporary; one small lake and one stream, of the climate parameters on the abundance of popula- both permanent). The sampling method adopted was the tions, the Spearman Correlation Coefficient or Pearson “active search” for specimens (Crump & Scott 1994), be- Linear Correlation Coefficient (Legendre & Legendre tween 18.00 and 5.00 (see Vieira et al., 2007 regarding in- 1998) were used, based on mean temperature, relative air formation about the activity pattern of P. nordestina). All humidity and the monthly rainfall. observed specimens were collected and placed into bags The niche breadth (number and volume), spatial to avoid counting them again during the same sampling, niche (substratum and perch height), and temporal niche and were subsequently replaced where they had been (periods of the year) were calculated using Simpson’s di- captured at the end of dawn. versity indicator (Simpson 1949): For each specimen, we recorded the following infor- 1 B = n mation: area (MNGA or RVSMJ), date, habitat (pond, 2 pi swamp, stream, artificial tank, temporary or permanent), i=1 the substratum used (tree stem, shrub stem, grass stalk, where p is the proportion of the resource category (tro- ground or others), perch height, distance to the nearest phic, spatial, temporal) used; i and n, are the number of water body, stratum of predominant vegetation (herba- categories of adopted resources; B varies from 1 (exclu- ceous, shrubby, arboreal or from water vegetation), en- sive use of resource type) to n (homogeneous use of all re- trance of canopy (open, intermediate or closed) and activ- sources types). Similarities in the use of resources by P. ity (calling, motionless, walking, amplexus, or others). nordestina between the two areas were investigated using We collected, if possible, five adult specimens in each a formula of symmetrical overlap (Pianka 1973): biome per month. Individuals were euthanised with 2% p p lidocaine, fixed in 10% formalin, and preserved in 70% ij ik n1 ethanol. In the laboratory, the stomachs were removed jk n n from the specimens and their contents were analysed 2 2 pij pik with a stereomicroscope. i1 i1 To determine the reproductive period of P. nordestina where j and k represent specimens from different areas. populations, the following parameters were recorded: the Values near zero indicate that there is no similarity in the presence of males calling, couples in amplexus, clutches, use of resources; values near 1 indicate that there is simi- and ovigerous females (Bertoluci 1998). The animal re- larity in the use of resources in each area. productive condition was assessed by analysing the fe- Variations in the manner of substratum use between male gonad, and the male vocal sac. Females were con- areas, and activity of specimens in the predominant stra- sidered to be reproductive when their oviducts were ex- tum of vegetation in meeting sites, were tested using a G- tremely convoluted and the ovaries were well developed, test or t-test. The potential differences in the vertical use and when males, when they possessed clear vocal sacs of microhabitat (perch height: x+1), and horizontal use (Mesquita et al. 2004). (distance from the nearest water body: x+1) between both For morphometry and mass recording, information populations were analyzed using the Mann–Whitney test that came from collected and captured specimens was (Zar 1999). considered, and measurements were made for all living The prey items eaten were identified to the lowest specimens. The masses were measured in the field using a possible taxonomical level, generally to the order level, Pesola® balance (0.1 g precision) and the snout-vent using a specialized bibliography (Buzzi 2002). After, prey 274 F.L.S. Caldas et al. items were counted, and their length and width were Results measured with a digital caliper (0.01 mm accuracy). The prey volumes were calculated using the formula for the Phyllomedusa nordestina was found mainly in lentic area of an ellipsoid (Magnusson et al. 2003): water bodies (RVSMJ – 100% and MNGA – Volume= (π.length.width2)/6 97.81%) irrespective of the sampling area. Tempo- An indicator of the importance value (IVI) was calcu- lated, to verify with how much each food item partici- rary ponds had the highest frequency of P. nordes- pated in the diet of P. nordestina using the following equa- tina (MNGA – 82.89% and RVSMJ – 82.89%). tion: Although there was a high overlap in the use
IVI = (F%+N%+V%)/3 of substratum (øjk = 0.87), differences among areas Both the numerical and volumetric composition of were found (G = 27.0181; g.l. = 7; P = 0.0001; adopted prey in the diet of P. nordestina in the area was NMNGA = 228 and NRVSMJ = 75). In the MNGA, the compared by the Kolmogorov–Smirnov test. most-used substrates were shrub stems (37.28%) The SVL and mass values were log10-transformed to fulfill assumptions of normality. The body size (SVL) of and grass stalks (37.28%) and in the RVSMJ, specimens was compared by an analysis of variance 38.67% of the substrates were grass stalks, (Fig. (ANOVA), and the masses were compared using an 2A). The estimated niche space breadth was analysis of co-variance (ANCOVA), using SVL as a co- BMNGA= 3.27 and BRVSMJ=3.48. variable and both were made by adopting two factors No differences in the predominant vegetation (sex and area). stratum used as meeting places by specimens were The analyses of variance and co-variance were per- found among areas (T = 0.9122; g.l. = 4; P = 0.41; formed in the Systat 12.0 program (Wilkinson 1990) and all other analyses in R (R Development Core Team 2009) NMNGA = 228 and NRVSMJ = 75). Phyllomedusa nordes- in Windows. The significance level used was 5%. All col- tina occupied areas with a predominance of herba- lected animals were placed in the Coleção Herpetológica ceous plants (MNGA 55.26% and RVSMJ
da Universidade Federal de Sergipe (CHUFS).
Figure 2. Relative frequencies of: A - substrate type, B – predominant vegetation stratum, C – perch height (m), D – distance from the nearest water body, E – activity of Phyllomedusa nordestina in the State Conservation Units Monu- mento Natural Grota do Angico (Caatinga), Poço Redondo – SE and Refúgio de Vida Silvestre Mata do Junco (Atlan- tic Forest), Capela – SE.
Autoecology of Phyllomedusa nordestina 275
70.67%) and shrubs (MNGA 41.67% and RVSMJ Phyllomedusa nordestina consumed 15 types of 29.33%) (Fig. 2B). Animals were common in open food items in the MNGA and 14 in the RVSMJ. In sites, irrespective of the sampling area (RVSMJ the MNGA, the most frequent prey items were 97.33% and MNGA 87.28%). Araneae (25.71%), Orthoptera (15.71%), insect lar- Phyllomedusa nordestina occupied a similar vae (14.29%) and Acarina (12.86%) (Table 1). In the roost positions in both biomes, which generally RVSMJ, the most frequent prey items were Ara- did not exceed 40 cm (Mann-Whitney, U = 1.2810; neae (28.00%), insect larvae (24.00%), Auchenor- P = 0.200; N = 303; Fig. 2C). The calculated niche ryncha (16.00%), Orthoptera (12.00%) and Acarina breadths (perchs) were BMNGA = 2.71 and BRVSMJ = (12.00%). In terms of the number of eaten prey
2.25, with a high overlap (øjk = 0.96) among areas. items, P. nordestina mainly consumed Araneae Specimens were up to 50 cm from water bodies (22.83%), Diptera (22.05%) and Acarina (19.69%) in and variations were not found in the occupied po- the MNGA and insect larvae (22.73%), Araneae sitions (Man–Whitney test, U = 1.0506; P = 0.293; (15.91%) and Acarina (13.64%) in the RVSMJ (Ta-
N = 303; Fig. 2D). The niche breadths were BMNGA= ble 1). In terms of niche volume, the most-used
1.44 and BRVSMJ = 3.48, with a high overlap øjk = prey items by species in the MNGA were Araneae 0.91. (53.64%), insect larvae (32.11%) and Orthoptera Both populations of P. nordestina did not differ (10.59%) and in the RVSMJ, these were insect lar- in the type of activity of the specimens (G = 4.6783; vae (73.31%) and Araneae (14.08%), (Table 1). The g.l. = 4; P = 0.32; NMNGA = 228 and NRVSMJ = 75; Fig. most important items (IVI) in the MNGA popula- 2E); most of the specimens were calling (MNGA – tion were Araneae (63.43%) and in the RVSMJ 82.89% and RVSMJ – 77.33%) at the meeting place. populations were insect larvae (71.16%) (Table 1). Ninety-eight stomachs of P. nordestina were In addition to invertebrates, species also swal- analysed (70 from the MNGA - 70 and 28 from the lowed mineral and plant matter (small grains such RVSMJ) (Table 1). In the MNGA, 22.86% of speci- as sand and stones) in both areas. Plant material mens had stomach contents that were in an ad- was found in 49 out of 98 stomachs analyzed vanced stage of digestion and 1.43% of stomachs (MNGA – 55.71% and RVSMJ – 40.00%) and 31 were empty, whereas in the RVSMJ, 24.00% of contained grains of sand (MNGA – 41.43% and stomachs had contents in an advanced stage of di- RVSMJ – 8.00% (Table 1). gestion and 20.00% were empty. Significant differences were found in the
Table 1./A. Summary of diet of Phyllomedusa nordestina in the Natural Monument Grota do Angico (Caatinga).
P.nordestina MNGA (Caatinga) (N = 70) Categories F F% N N% V (mm3) V% IVI Acarina 9 12.86 25 19.69 10.52 0.01 32.54 Araneae 18 25.71 29 22.83 92196.07 53.64 66.43 Coleoptera 5 7.14 5 3.94 1031.61 0.60 11.28 Diptera 6 8.57 28 22.05 532.81 0.31 30.72 Ephemeroptera 1 1.43 1 0.79 1.50 0.00 2.22 Empty stomach 1 1.43 - - - - - Formicidae 4 5.71 6 4.72 31.36 0.02 10.44 Hemiptera (Auchenorryncha) 1 1.43 1 0.79 2.75 0.00 2.22 Hemiptera (Heteroptera) 5 7.14 5 3.94 4643.93 2.70 11.98 Hymenoptera 3 4.29 3 2.36 34.32 0.02 6.65 Isoptera 2 2.86 2 1.57 0.10 0.00 4.43 Insect Larvae 10 14.29 10 7.87 55195.28 32.11 32.86 Orthoptera 11 15.71 11 8.66 18194.26 10.59 27.90 Plant Material 39 55.71 - - - - - Thysanoptera 1 1.43 1 0.79 0.13 0.00 2.22 Blattaria ------Isopoda ------Lepidoptera ------Advanced digestion 16 22.86 Mineral materials 29 41.43 Total 127 171874.64 B 6.27 2.48 276 F.L.S. Caldas et al.
Table 1./B. Summary of diet of Phyllomedusa nordestina in the Wildlife Refuge Mata do Junco (Atlantic Forest).
P.nordestina RVSMJ (Atlantic Forest) (N = 28) Categories F F% N N% V (mm3) V% IVI Acarina 3 12 6 13.64 0.11 0.00 25.64 Araneae 7 28 7 15.91 4975.53 14.08 48.60 Coleoptera 2 8 2 4.55 49.53 0.14 12.59 Diptera 1 4 1 2.27 20.40 0.06 6.29 Ephemeroptera ------Empty stomach 5 20 - - - - - Formicidae 2 8 2 4.55 - - 12.55 Hemiptera (Auchenorryncha) 4 16 5 11.36 1745.22 4.94 29.01 Hemiptera (Heteroptera) 2 8 2 4.55 30.76 0.09 12.57 Hymenoptera ------Isoptera ------Insect Larvae 6 24 10 22.73 25910.83 73.31 71.16 Orthoptera 3 12 4 9.09 2551.59 7.22 23.50 Plant Material 10 40 - - - - Thysanoptera ------Blattaria 1 4 3 6.82 54.00 0.15 10.87 Isopoda 1 4 1 2.27 2.44 0.01 6.28 Lepidoptera 1 4 1 2.27 4.48 0.01 6.28 Advanced digestion 6 24 Mineral materials 2 8 Total 44 35344.89 B 7.74 1.77
number of prey types that were consumed by both populations where there was a moderate overlap,
(Kolmogorov–Smirnov, Dmax = 0.3311, g.l. = 2, P
=0.0008; BMNGA = 6.27 and BRVSMJ = 7.74; ø = 0.70). The consumed volume for each category also var- ied between areas, also with a moderate overlap
(Kolmogorov–Smirnov, Dmax = 0.4030, g.l. = 2, P <
0.0001; BMNGA = 2.48 and BRVSMJ = 1.77; ø = 0.67). The populations differed in the periods of the year when they were observed most frequently (G = 70.1818; g.l. = 11; P < 0.0001 (Fig. 3). In the MNGA, specimens were found between February and July, and were even more frequent between March and May (Fig. 3), while in RVSMJ, indi- viduals were observed between January and No- vember, being more frequent in May and June, and were not found in October (Fig. 3). The esti- mated niche breadths were BMNGA = 4.87 and
BRVSMJ = 8.19, with an overlap of øjk = 0.87.
Among the analyzed climate parameters, the biggest correlations with the abundance of speci- Figure 3. Monthly values of climate variables, taken at the mens in the MNGA were observed with the vari- closest climate stations: (Poço Redondo/SE) for MNGA ables relative humidity (rSpearman = 0.614; P = 0.033) (Caatinga) and (Capela/SE) for RVSMJ (Atlantic Forest) and accumulated rainfall (rSpearman = 0.602; P = between December 2009 and November 2010. (-▲-) 0.038). In the RVSMJ, the major correlation ob- mean temperature MNGA (-●-) mean temperature RVSMJ, (-◊-) precipitation MNGA (-■-) precipitation served was between the abundance of specimens RVSMJ, (---) relative humidity MNGA, (-x-) relative and accumulated rainfall (rSpearman = 0.603; P = humidity RVSMJ and the bars (empty – MNGA; filled – 0.037) and also humidity (rPearson = 0.583; P = RVSMJ) represent the monthly relative frequencies of 0.046). There were no correlations between the Phyllomedusa nordestina.
Autoecology of Phyllomedusa nordestina 277
Table 2. Temporal distribution of different reproductive stages of P. nordestina in the MNGA (Caatinga) (X) and in the RVSMJ (Atlantic Forest) (●) and at both locations (▲) between December 2009 and November 2010.
DEZ JAN FEV MAR ABR MAI JUN JUL AGO SET OUT NOV Vocalization ● ▲ ▲ ▲ ▲ ▲ ▲ ● ● ● Embrace ● X X Ovigerous X ▲ ▲ ▲ ▲ females Spawning ● ● X ▲ ▲ X ●
mean monthly temperatures and the abundance of the RVSMJ – 58 males and 10 females) were ob- specimens in either area: MNGA (rSpearman = 0.127; tained. The specimens differed in size (SVL) be-
P = 0.692) and RVSMJ (rPearson = 0.270; P = 0.395). tween both locations, independent sex factor
Some factors relating to the reproduction of P. (ANOVA F1,1,267 = 5.606; P = 0.019), between sexes nordestina in each area are shown in Table 2. The independent of locality (ANOVA, F1,1,267 = 222.000; presence of males calling, couples in amplexus, P < 0.0001) but not when considering the two fac- ovigerous females and clutches was lower during tors (sex and location) were considered simultane- the rainy months in the MNGA (Table 2; Fig. 3) ously (ANOVA, F1,1,267 = 1.234; P = 0.268). For the and reproductive activities ceased in July, before specimens of the MNGA, the SVL of males and water bodies became dry and at the end of rainy females was 37.77 ± 1.89 mm and 45.14 ± 2.56 mm, period. In the MNGA, P. nordestina maintained respectively. For the RVSMJ populations, the SVL calling activity for more than three months con- of males and females was 37.23 ± 1.51 mm and tinuously, but this period was restricted to a par- 43.43 ± 2.54 mm, respectively. Phyllomedusa nordes- ticular season. tina showed sexual dimorphism with respect to In the RVSMJ, in addition to calling activities, mass, independent of registration area (ANCOVA, amplexus and breeding were correlated with the F1,1,266 = 153.470; P < 0.0001), but this variation was presence of rainfall; these were not restricted to not observed when analyzed specimens of each months of high rainfall incidence, which extended area, independent of sex (ANCOVA, F1,1,266 = until the last month of sampling (Table 2; Fig. 3). 2.866; P = 0.092) or the interaction of factors (sex
In this area, specimens were observed calling for and place) (ANCOVA, F1,1,266 = 0.794; P = 0.374). nine months. Almost all specimens were found in the buffer zone adjacent to woodland and for many months, only one of these areas showed a Discussion high number of specimens. This area was ploughed twice during the period of collection Phyllomedusa nordestina was observed in lentic wa- and all the shrubs and herbaceous plants were ter bodies, independent of the area that was removed. found. In the stream in the Caatinga area In the MNGA, 46 clutches were found. Some (MNGA), both specimens of this species were of these showed evidence of dryness, but ten were found in quiet sites. The use of lentic environ- in a good condition and had a mean of 86 ± 32 ments is known for the species in other areas of eggs (22 – 130 eggs). Plants used for breeding were the Caatinga (Vieira et al. 2007) and Atlantic Forest Jatropha mollissima (73.91% – Euphorbiaceae), Cro- (Vilaça et al. 2011), as well as for other species of ton heliotropiifolius Kunth (15.22% – Euphor- the genus: P. trinitatis, P. hypochondrialis, P. biaceae), Ipomoea nil (L.) Roth. (6.52% – Convolvu- tetraploidea, P. rohdei, P. sauvagi and P. azurea laceae) and Ludwigia sp. (4.35% – Onagraceae). In (Kenny 1966, Pyburn & Glidewell 1971, Bernarde the RVSMJ, eight clutches were found in a good & Anjos 1999, Wogel et al. 2005, Rodrigues et al. condition and contained a mean of 91 ± 12 eggs (83 2007, Freitas et al. 2008). Using this type of envi- – 100 eggs). The plants found with clutches were ronment seems to be too conservative to represen- Jatropha gossypiifolia L. (50.00% – Euphorbiaceae), tatives of the subgroup of the genus hypochondri- unidentified Malvaceae (33.33%) and Acrostichum alis (P. hypochondrialis, P. nordestina, P. azurea and sp. (16.67% – Pteridaceae). P. rohdei) and the most appropriate development For SVL and species mass, 271 records (203 for of their tadpoles, which are positioned normally in the MNGA – 191 males and 12 females, and 68 for the middle of the water column (Cruz 1982) and 278 F.L.S. Caldas et al. do not have fixation structures during this phase dependence of Phyllomedusa nordestina on habitats (Mcdiarmid & Altig 1999). close to water might explain why little variation in Grass and shrub stems were the substrates the types of selected spatial resources was ob- that were most used by animals in both areas, al- served in different environments. though some preferences existed in each locality. Generally, the diets of organisms are associ- These preferences relate to the biology of P. nordes- ated with morphological and physiological charac- tina, which has adapted to suit the arboreal habit teristics and with behaviour that facilitates the lo- (Caramaschi & Cruz 2002), confirming the hy- calization, identification and capture of their prey pothesis that the use of calling sites is mainly re- (Pough et al. 2004, Maragno & Souza, 2011). An- lated to the morphological adaptations of the spe- other factor that should be considered is the cost- cies (Crump 1971, Hödl 1977) or is limited by body benefit relationship that certain food brings in size and mass (Duellman 1967). The use of shrubs terms of the requirements of the predator (Toft and grasses by P. nordestina has already been reg- 1980, 1985). istered in the Atlantic Forest and the Caatinga The wide spectrum of prey items consumed (Santos et al. 2004, Vieira et al. 2007, Protázio et al. by P. nordestina in each area agrees with a general- 2014). This appears to be true for other representa- ist pattern of food resource use. Traditionally, an- tives of the genus in other localities and biomes urans have been shown to be generalist predators (e.g., P. rohdei, P. hypochondrialis, P. azurea and P. with an opportunistic behaviour of foraging (Du- distincta) (Pombal 1997, Rodrigues et al. 2007, ellman & Trueb 1994, Solé & Rödder 2009, Schalk Freitas et al. 2008, Barrio-Amorós 2009, Forti 2009, et al. 2014). Their diets basically consist of arthro- Lima et al. 2010, Dias et al. 2014). pods (Lima et al. 2006), which reflects their abun- Phyllomedusa nordestina was also common in dance in the environment (Hirai & Matsui, 1999, open areas and modified areas, independent of the Sugai et al. 2012). studied biomes, demonstrating a certain tolerance Among several categories of prey consumed to adverse environment conditions. Natural habi- by P. nordestina, spiders are relevant, because of tat modifications can generate passive conditions their importance in the diet of the population in of being accepted by generalist species, which re- the Caatinga, and as a second prey item in the At- ceive fewer homogeneous spatial resources, which lantic Forest. Probably, the use of this resource is do not damage their activities (Grandinetti & related to the abundance of these animals in both Jacobi 2005). The use of open areas, where there is areas and to the occurrence of several species of a greater or smaller degree of disturbance, has al- the group in locations used by P. nordestina. Such ready been registered for several species of Phyl- animals are extremely abundant in localities of the lomedusa, such as P. tarsius, P. camba, P. hypochon- Caatinga (Carvalho & Brescovit 2005, Carvalho & drialis, P. trinitatis, P. azurea and P. nordestina Avelino 2010) and the Atlantic Forest (Oliveira- (Neckel-Oliveira & Gascon 2006, Bernarde 2007, Alves et al. 2005, Peres et al. 2014), and are consid- Borges & Juliano 2007, Kenny 1966, Barrio- ered as resources. Spiders were also important in Amorós 2009, Freitas et al. 2008, Vilaça et al. 2011, the diet of P. rohdei, and P. burmeisteri (Lima et al. Dias et al. 2014). 2010), males of P. azurea (Freitas et al. 2008) and P. Habitats adjacent to water and low perches nordestina in other Caatinga areas in northeastern were adopted by P. nordestina. These locations Brazil (Protázio et al. 2015). possibly offer better conditions for the survival of In the RVSMJ, the insect larvae category was this species in both biomes. Generally, these habi- the most important in the diet of P. nordestina. tats provide more favourable microclimate condi- These prey types provide a high energetic input tions to maintain the humidity of the animal and many species are considered an important re- cover, which are necessary for breathing. Addi- source of animal protein (Hanping & Changzhen tionally, the proximity of water decreases the risk 1993). The presence of this item possibly provides of desiccation for adults and clutches (Freitas et al. a basis to extend the activity of anurans from this 2008). Since the eggs of Phyllomedusa spp. are laid area and also reflects its availability in the envi- in leaves after hatching, and their development ronment. The larvae of insects were the most im- occurs in water, the selection of places near to wa- portant items in the diet of P.rohdei and P. burmeis- ter bodies is extremely important (Cruz 1982). teri (Lima et al. 2010) also in the area of the Forest. The choice of microhabitats for calling and Plant matter was frequent in the stomachs of breeding influences fitness (Townsend 1989). The both populations of P. nordestina and grains of
Autoecology of Phyllomedusa nordestina 279 sand, and small stones were found mainly in conditions for the development of larvae exist specimens in the Caatinga. The ingestion of plants (Dayton & Fitzgerald 2005). In humid tropical re- by anurans is considered accidental by some au- gions such as the Atlantic Forest, regular rainfall thors (Brandão et al. 2003, Kovács et al. 2007). In allows motionless water bodies to remain for a this case, parts of plants might have been swal- long time, which allows specimens to begin re- lowed in trying to capture prey that were on such productive activity and means that larvae are not plants. The selection of parts of vegetables and threatened by sudden changes in water availabil- minerals can also provide volume to the stomach ity (Duellman 1978, Hödl 1990, Stebbins & Cohen and contribute to the softening of the arthropod 1995). exoskeleton (Evans & Lampo 1996). Plants can In following these characteristics, the repro- also act as a water resource (Anderson et al. 1999), ductive pattern of P. nordestina in Caatinga ap- mainly in the Caatinga, where water is scarcer, or pears to be of an explosive type, since it is re- during the drier periods in the Atlantic Forest. The stricted to a particular season or period of the year increase in the consumption of plant matters dur- (Wells 1977). This has been observed for other ing the dry season has already been registered for specimens of the same genus in areas with strong Hyla truncata (Xenohyla truncatus) in the rest of the seasonality, such as P. sauvagii (Rodrigues et al. Atlantic Forest in Rio de Janeiro State (Silva et al. 2007) and P. azurea (Rodrigues et al. 2007, Freitas 1989) and might be a way to reduce water stress in et al. 2008) in the Cerrado, and for P. nordestina in this period. Associated with this, some adapta- other areas of the Caatinga (Arzabe 1999, Vieira et tions of representatives of the genus Phyllomedusa al. 2007). Seasonal regions, with dry season, usu- can help in the water economy in localities with a ally have more species associated with the rainy pronounced dried season, by the production of season at the expense of those annual as observed uric acid and wax (Caramaschi & Cruz 2002). in other studies (Arzabe 1999, Eterovick & Sazima Some specimens were found with empty 2000, Toledo et al. 2003, Vasconcelos & Rossa- stomachs, which might be related to their repro- Feres 2005). ductive period (Van Sluys & Rocha 1998, Kovács In contrast, more humid tropical regions that et al. 2007). Additionally, anuran males can fast for are not affected by severe drought periods used to reproduction, since these individuals spend a long contain a large number of species (Crump 1974). time calling in places that might be those previ- Frequent rainfall similar to that observed in the ously chosen for foraging (Duellman & Trueb Atlantic Forest (Ab’Sáber 1977, Tonhasca-Júnior 1994). 2005) may favour a longer reproductive pattern Several factors can influence the length of the for P. nordestina in the area RVSMJ. reproductive period and the behaviour of anurans, Although these explosive and longer patterns such as climate, seasons, competition and density of reproduction are common, the reproduction of (Mesquita & Wiederhercker 2003). Variations in anurans in the Caatinga appears to respond to the availability of these resources in the environ- particularities and/or irregularities in the rainfall ment mean that a particular species can show dif- index in a flexible way. The reproductive period of ferent temporary patterns or reproductive strate- P. nordestina was recorded as being from Decem- gies in distinct environments (Pombal & Haddad ber to May in the area of Matureia, Paraíba, and 2005). occurred in February, April, and May in São José The activities of P. nordestina in biomes, were do Bomfim, Paraíba (Arzabe 1999). In the region of strongly associated with periods of high humidity, Cabaceiras, Paraíba, the species actively repro- with the arrival of specimens and the greatest duced between January and August (Protázio et abundances were found within this period. In the al. 2014). The rainfall index differs slightly be- Caatinga, the animals had been present for five tween these areas. In 2010, precipitation in the months, in contrast to in the Atlantic Forest, where MNGA occurred from January to October and was they were observed during all sampling months. reflected by a period of reproductive activity of P. The observed differences are probably related to nordestina from February to July. the permanence of the water bodies in each biome, The reaction the anurans in the Caatinga to fa- with the Caatinga offering limited resources of vourable climatic conditions can be explained by this type. Amphibian reproduction in arid envi- the “theory of resource pulses”, which states that ronments is directly associated with the period of reproductive activity responds to particular condi- rainfall, because outside this period, no favourable tions or to favourable resources (Chesson et al. 280 F.L.S. Caldas et al.
2004). Therefore, when the anuran population is completely destroyed. Modifications in the struc- low, reproduction is maintained at a low level, or ture of the habitat, mainly relating to vegetation, as in this study, is non-existent. This response has can influence the structure of the anuran commu- already been noted and discussed for amphibian nities, reducing the richness rates and species di- communities from the Mediterranean region versity (Fujioka & Lane 1997) and affects the re- (Richter-Boix et al. 2006). production of P. nordestina, since the clutches of Reproduction is a critical event for amphibi- this frog are laid on leaves that overhang water ans, because they generally do not possess mecha- (Vieira et al. 2007). nisms to conserve water within their bodies (Bent- Body size is a basic characteristic of organ- ley 1966, Arzabe 1999, Navas et al. 2004). Thus, a isms, which has direct implications on physiology, high humidity positively influences the abun- ecology, and social interactions (Schäuble 2004). dance of amphibians, preventing physiological Differences in size were observed among popula- depression level of their independent coats the tions of P. nordestina in this study. Different selec- environment where they are (Arzabe 1999, Prado tion pressures might explain these differences. & Pombal 2005, Rodrigues et al. 2012). Rainfalls Morphological variations on the geographical has a similar effect and its importance has been scale are common in some animal species, and discussed in the literature for the Caatinga (Ar- these are normally associated with local particu- zabe 1999, Navas et al. 2002, Vieira et al. 2007) and larities (Castellano & Giacoma 1998, Santiago- for other biomes with a more regular rainfall Alarcon et al. 2006, Kaliontzopoulou et al. 2010). (Conte & Machado 2005, Prado & Pombal 2005, Many processes can generate such variations, in- Bernarde 2007, Canelas & Bertoluci 2007, De- cluding peculiarities of the environment and/or of Carvalho et al. 2008, Pirani et al. 2013). the climate, which affect the growth rates (Riha & Hotter periods of the year are favourable for Berven 1991, Castellano et al. 2000), variations in anuran reproduction (Aichinger 1987, Bertoluci the level of selection and dimorphism (Endler & 1998, Bernarde & Machado 2000, Vasconcelos & Houde 1995, Wiens et al. 1999) and differences in Rossa-Feres 2005, Conte & Rossa-Feres 2006, Zina the types of consumed prey, and pressures of pre- 2007). However, this was not found for the biomes dation (Schneider et al. 1999). in this study, and might reflect a low variation in The specimens of P. nordestina in the Atlantic the monthly mean temperature (Pombal 1997, Forest are slightly smaller than those in the Caat- Ávila & Ferreira 2004) in Sergipe State. inga. Probably differences in each area, the envi- The strict relationship between amphibians ronmental change levels, and predation rates or and abiotic factors causes some authors to believe even the number of competitors may contribute to that temporal segregation is not an important the observed variations. Most of specimens ob- mechanism of reproductive isolation. This is be- served in Mata do Junco were in the most dis- cause many species are only active during the turbed site of the area. This location was a tempo- rainy season (Pombal 1997, Prado & Pombal 2005, rary pond surrounded by pasture, with herba- Borges & Juliano 2007). However, the end of re- ceous plants and shrubs in its margins, and twice productive period of P. nordestina in the area of the during the study, all vegetation surrounding the Caatinga occurred before the end of rainy season, pond where animals were most frequently found, and might indicate a mechanism to facilitator was entirely destroyed. Changes in habitat quality mechanism of habitat sharing, or represent the last can influence the life of an individual, mainly in chance for the larvae to develop. Since the envi- terms of growth, as was observed for specimens of ronments of the Caatinga receive unpredictable the same genus submitted to similar conditions, rainfall, anurans must take advantage of the peri- such as P. tarsius (Neckel-Oliveira & Gascon 2006). ods when water is available. Since adults end their Variations in morphology that result from reproductive activity before the end of rainy sea- habitat changes have also been observed in popu- son, larvae have the opportunity to develop before lations of Corythomantis greeningi in different areas the ponds dry out (Heyer 1973). of the Caatinga in Bahia State (Juncá et al. 2008): Phyllomedusa nordestina was not found in the the greatest variations were observed in adult studied area of the Atlantic Forest during October. males and tadpoles and resulted from the removal In this period, the area that hosted most specimens of native vegetation that might have affected the during the study was affected by anthropic inter- quantity and quality of shelters and the abun- ference and the stratum of grasses and shrubs was dance of microorganisms important for tadpole
Autoecology of Phyllomedusa nordestina 281 feeding. These factors favoured the survival of (Woolbright 1983). smaller specimens in this location. In both biomes, P. nordestina used leaves of In the RVSMJ, 33 species were recorded grasses and shrubs to lay their eggs, and in both (Morato et al. 2011), 17 of which were arboreal biomes, clutches were more common in shrubs, species, and two; Dendropsophus decipiens and Phyl- mainly in so-called “pinhão-bravo” (Jatropha mol- lomedusa bahiana, used similar habitats to those of lissima – Caatinga), or in “pinhão-roxo” (Jatropha P. nordestina to lay eggs (Haddad & Prado 2005). gossypiifolia L. – Atlantic Forest). Phyllomedusa The pressures exerted by predators and competi- nordestina has a modal number of 24 eggs, which tors, can help in the evolution of different sizes consists of eggs laid on leaves above water and and forms (Wilbur 1997). Disputes for oviposition exotrophic tadpoles that fell into motionless water sites might have caused P. nordesrtina to move to bodies to complete their development (Haddad & disturbed areas, i.e., to areas with a lower habitat Prado 2005). The selection of oviposition sites is quality, which negatively affects their develop- related to the choice of habitats that provide more ment. In the MNGA, throughout the year studied, optimal features for egg laying and the develop- no species was found that reproduced in the same ment of embryos (Dias et al. 2014). However, this way as P. nordestina (Gouveia & Faria 2015). De- selection might also reflect the availability of the spite knowledge concerning potentially competi- local vegetation and might relate to exotic and/or tive species, further studies are necessary to eluci- generalist plants (Brachiaria) that are established in date the role of such interactions in the selection of Degraded areas, as was observed for P. azurea in distinct sizes and forms of P. nordestina in each lo- Central Brazil (Costa et al. 2010, Dias et al. 2014). cality. The mean of number of eggs a clutch was al- Phyllomedusa nordestina is a species whose fe- most the same in both biomes, but in the Caatinga males are larger than males in the studied biomes. some clutches contained 130 eggs, and in Atlantic The presence of sexual dimorphism is common in Forest, the greatest number was 100 eggs. These anurans, with females being larger than males values are similar to those observed for the genus (Shine 1979, Vitt & Caldwell 2009). This character- Phyllomedusa, which lays between 100 and 150 istic is probably related to a differential invest- eggs per clutch (Zug et al. 2001). However, there is ment in reproduction by either sex (Katsikaros & a record in an Atlantic Forest area of southeastern Shine 1997, Monnet & Cherry 2002), which results Brazil, of clutches containing up to 190 eggs (P. in distinct selective pressures that occasionally are tetraploidea) and in the Amazon, of clutches ex- not limited to a unique aspect of phenotype ceeding 300 eggs (P. tarsius) (Neckel-Oliveira 2003, (Howard 1981). Being larger is good for females, Dias et al. 2013). A large number of eggs in the since they can produce more eggs and therefore, Caatinga population might provide a positive larger clutches (Woolbright 1983, 1989, Prado et al. benefit by increasing the probability that some 2000, Wells 2007). Larger females appear to be a tadpoles develop and complete their lifecycle. characteristic of the genus Phyllomedusa (e.g., P. Since water resources are extremely limited in nordestina, P. trinitatis, P. camba, P. oreades, P. sau- Caatinga environments, more eggs increases the vagii, P. azurea, and P. megacephala) (Kenny 1966, chances in the “fight for life”. Despite the gelati- De La Riva 1999, Brandão 2002, Caramaschi 2006, nous mass that surrounds the eggs of Phlyllome- Rodrigues et al. 2007, Freitas et al. 2008). dusa, which decreases water loss, some clutches The males of P. nordestina in the Atlantic For- are lost (Pyburn 1980, Wogel et al. 2005). The con- est were smaller than those observed in the Caat- centration of water vapour and relative air humid- inga. Different investments in each biome during ity in microhabitats are essential to maintain the reproduction might be one of the causes of such water balance, and to guarantee the success of egg variation. Phyllomedusa nordestina was active for incubation (Pyburn 1970). Thus, the choice for nine months in the area of Atlantic Forest and only suitable sites for oviposition and the development six in the Caatinga. For males with a longer repro- of larvae are extremely important to maintain the ductive pattern, the defence of territory and higher species. frequency of calling activities and foraging can re- Finally, both populations of P. nordestina are sult in considerable losses of energy, which could highly similar in terms of spatial resource use, be used for growth; however, these activities do mainly in choosing a microhabitat. The most im- not affect the production of gametes, since the cost portant factors for the species in both biomes were to males is low and does not depend on size related to the availability and duration of water 282 F.L.S. Caldas et al. bodies in the environment. The main difference Venezuela. Memoria de la Fundación La Salle de Ciencias Naturales 171: 19-46. observed among the studied populations of P. Bentley, P.J. (1966): Adaptations of amphibian to arid nordestina was related to the length of the repro- environments. Science 152: 619-623. Berazategui, M., Camargo, A., Maneyro, R. (2007): Environmental ductive period, which was longer in the Atlantic and seasonal variation in the diet of Elachistocleis bicolor (Guérin- Forest area. Few variations were observed in Méneville 1838) (Anura: Microhylidae) from Northern Uruguay. Zoological Science 24: 225-231. terms of environment use, or in diet, indicating the Bernarde, P.S. (2007): Ambientes e temporada de vocalização da possible effect of recent ecological factors (Vitt & anurofauna no município de Espigão do Oeste, Rondônia, Zani 1998). However, there was a tendency to re- Sudoeste da Amazônia - Brasil (Amphibia: Anura). Biota Neotropica 7(2): 87-92. tain basic niche aspects in both biomes, i.e., his- Bernarde, P.S., Anjos, L. (1999): Distribuição espacial e temporal da torical factors influence the pattern of resource use anurofauna no Parque Estadual Mata dos Godoy, Londrina, Paraná, Brasil (Amphibia: Anura). Comunicações do Museu de (Wiens & Graham 2005). Phylomedusa nordestina Ciências e Tecnologia Série Zoologia 12: 127-140. appears to tolerate changes in the habitat in which Bernarde, P.B., Machado, R.A. (2000): Riqueza de espécies, ambientes de reprodução e temporada de vocalização da it was found and was more abundant in one of the anurofauna em Três Barras do Paraná, Brasil (Amphibia: most anthropogenic sites in one of the sites in the Anura). Cuadernos de Herpetologia 14(2): 93-104. Bertolluci, J. (1998): Annual patterns of breeding activity in Atlantic Atlantic Forest area. Rainforest anurans. Journal of Herpetology 32: 607–611. Borges, F.J.A., Juliano, R.F. (2007): Distribuição espacial e temporal de uma comunidade de anuros do município de Morrinhos, Goiás, Brasil (Amphibia: Anura). Neotropical Biology and Conservation 2(1): 21-27. Acknowledgements. We thank Mr. Manuel Messias and Brandão, A.R. (2002): A new species of Phyllomedusa Wagler, 1830 (Anura: Hylidae) from Central Brazil. Journal of Herpetology her family for the support offered in MNGA; to Marcelo 36(4): 571-578. Guigó and family for help offered in RVSMJ. We thank to Brandão, R.A., Garda, A., Braz, V., Fonseca, B. (2003): Observations CAPES for the research grant awarded; to Secretaria do on the ecology of Pseudis bolbodactyla (Anura, Pseudidae) in Meio-ambiente e Recusrsos Hídricos de Sergipe Central Brazil. Phyllomedusa 2(1): 3-8. Buzzi, Z.J. (2002): Entomologia didática. 4rd Edition. UFPR, (SEMARH-SE) for the support of infrastructure and Curitiba. driving as regards both UCs and for collect permission Canelas, M.A.S., Bertoluci, J. (2007): Anurans of the Serra do emitted under nº2010.0405.1211/00109-007. Our thanks to Caraça, southeastern Brazil: species composition and phenological patterns of calling activity. Iheringia, Série Programa de Pesquisa em Ecologia e Conservação (PPEC) Zoologia 97(1): 21-26. of Universidade Federal de Segipe (UFS) for all support Caramaschi, U. (2006): Redefinição do grupo de Phyllomedusa given. Thanks to Ana Cecília da Cruz, Marta Vieira and hypochondrialis, com redescrição de P. megacephala (Miranda- all of the Herbarium (ASE/UFS) that assisted in the Ribeiro, 1926), revalidação de P. azurea Cope, 1862 e descrição de uma nova espécie (Amphibia, Anura, Hylidae). Arquivos do identification of plants. Special thanks to all who have Museu Nacional, Rio de Janeiro 64(2): 159-179. held management positions in the two UCs, Sidney F. Caramaschi, U., Cruz, C.A.G. 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