North-Western Journal of Zoology Vol. 6, No. 1, 2010, pp.13-24 P-ISSN: 1584-9074, E-ISSN: 1843-5629 Article No.: 061102

Diet of two sympatric (Anura: ) species from a cacao plantation in southern Bahia,

Jonatha Edson de Paula LIMA1, Dennis RÖDDER2 and Mirco SOLÉ1,*

1. Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Rodovia Ilhéus Itabuna, km 16, CEP 45650-000, Ilhéus, Bahia, Brazil 2. Department of Biogeography, Trier University, Am Wissenschaftspark 25-27, D-54296 Germany * Corresponding author: M. Sole, E-mail:: [email protected]

Abstact. We studied the diet of two sympatric species of leaf-, Phyllomedusa rohdei and P. burmeisteri, captured in a cacao plantation in the Atlantic forest domain of southern Bahia, using stomach-flushing. The most important prey categories for P. rohdei were Araneae, larval Lepidoptera and Orthoptera, while for P. burmeisteri: Araneae, Coleoptera and larval Lepidoptera. Other items frequently flushed out of the frogs were plant remains, mites and skin. The snout-vent-length of the frogs was not correlated with the length and number of prey items. Our results suggest that both leaf species studied are opportunistic sit-and-wait predators with a high overlap in prey categories.

Key words: Amphibia; Anura; Hylidae; diet; Phyllomedusa burmeisteri, Phyllomedusa rohdei

Introduction Causes for declines and extinctions are manifold, but habitat loss and emerging The Brazilian Atlantic Rain Forest is one of the infectious diseases such as Chytridiomycosis world’s most diverse biodiversity hot spots play a major role (e.g. Stuart et al. 2004, Rödder (Myers et al. 2000) harboring a very rich an- et al. 2009). First reports of amphibian declines uran fauna. More than 400 amphibian species in the Atlantic Rainforest were published by have been reported from this biome and many Weygoldt (1989). Subsequently, Batrachochyt- new species are described every year, rium dendrobatidis, the biological agent of Chyt- especially from southern Bahia (Haddad et al. ridiomycosis, was detected in many amphibian 2008). This area has recently been identified as populations and has most likely caused amphi- a climatic refugium for neotropical species in bian declines on local levels (Weygoldt 1989, the late Pleistocene (Carnaval & Moritz 2008, Carnaval et al. 2005). The Amphibian Conser- Carnaval et al. 2009). Due to its heterogeneity vation Action Plan was developed by IUCN in and the large amount of niches, a high percent- order to identify knowledge gaps and to age of the species inhabiting the Atlantic Rain coordinate conservation efforts (Gascon et al. Forest are tree frogs belonging to the family 2007). Captive breeding programs for highly Hylidae (Haddad et al. 2008). threatened species have been advocated as a Nowadays, are among the pivotal short term emergency response (Lötters most threatened vertebrates globally declining et al. 2005), but, to be successful, detailed at an alarming rate (Stuart et al. 2004) and knowledge on their natural history is crucial researchers have raised the question whether (e.g. Rödder et al. 2009). mankind is witnessing the midst of the sixth Only a few studies on feeding ecology of mass extinction (Wake & Vredenburg 2008). anurans have been undertaken in the Atlantic

©NwjZ, Oradea, Romania, 2010 North-West J Zool, 6, 2010 www.herp-or.uv.ro/nwjz Oradea, Romania 14 Lima, J.E.P. et al.

Rain Forest, most of them focusing on leaf litter Despite the fact that Phyllomedusa species species from southern and southeastern Brazil have been identified as possessing highly belonging to the families Leptodactylidae (e.g. active skin substances (e. g. Phyllomedusa bicolor van Sluys et al. 2001, Teixeira & Vrcibradic (Erspamer et al. 1993); P. hypochondrialis (Brand 2003, Solé et al. 2009). Most of the few studies et al. 2006)), few efforts to study their diet have dealing with the diet of Atlantic Forest tree been undertaken. More detailed information is frog species have been undertaken in the only available for P. azurea (Freitas et al. 2008), middle and southern extension of this biome P. hypochondrialis (Dure 1999, Peltzer et al. (Solé & Pelz 2007). The lack of studies on 2000), P. rohdei (Teixeira & Vrcibradic 2007) feeding ecology of hylid frogs may be explain- and for larvae of P. tetraploidea (Lajmanovich & ed by the difficulty of capturing these frogs in Faivovich 1998). The main goal of our study their habitats outside their often short repro- was to assess the diet composition, trophic ductive periods, during which many species do niche breadth and the degree of trophic niche not feed (Solé & Pelz 2007). During the rest of overlap of Phyllomedusa rohdei and Phyllome- the year most Hylids live and feed in the dusa burmeisteri (Fig.1) from a cacao plantation canopy and are therefore difficult to collect. in southern Bahia, Brazil. In the remnants of the Atlantic Forest of southern Bahia, two species belonging to genus Phyllomedusa can be found in syntopy: Phyllo- Material and Methods medusa burmeisteri Boulenger, 1882 and Phyllo- Study site medusa rohdei Mertens, 1926. Phyllomedusa bur- meisteri is a large species of the P. burmeisteri The study area is located behind the campus of group (Faivovich et al. 2005), distributed Universidade Estadual de Santa Cruz (UESC) through Eastern Brazil. Phyllomedusa rohdei is a (14°47’45’’S, 39°10’20’’W) (Fig.2), municipality of Ilhéus, southern Bahia, Brazil, the primary cacao growing region medium sized species belonging to the P. in Brazil. With an annual mean temperature of 24°C and hypochondrialis group described from Rio de 1500 mm of rainfall per year it shows no significant Janeiro who had its distribution recently differences between the seasons (Mori et al. 1983). The extended to southern Bahia (Vrcibradic et al. vegetation is classified as tropical lowland rain forest (Oliveira Filho & Fontes 2000). In the traditional cacao 2006, Araujo et al. 2007). Both species tolerate a plantations called cabrucas, the cacao trees (Theobroma certain anthropogenic habitat disturbance. cacao) grow in the shadow of large trees belonging to the Both can be often found in cabrucas, typical original flora of the Atlantic rainforest or to introduced cacao plantations of southern Bahia where the species as rubber trees (Hevea brasiliensis), coral trees shelter of old-growth trees of the original (Erythrina sp.) or jackfruit (Artocarpus heterophyllus). Recent studies estimate the total area of cabrucas in Atlantic vegetation matrix is used to shade the southern Bahia to occupy an area of 650.000 ha (Araújo et cacao trees. The genus Phyllomedusa Wagler, al. 1998). Losses due to witches’ broom disease, triggered 1830 comprises 31 species, 14 of which can be by the fungus Moniliophthora perniciosa, and low market found in the Atlantic Rain Forest (Caramaschi prices are causing a rapid change in land-use in the & Cruz 2002, Frost 2009). Only two other region. The cabrucas are being cut down to open space for extensive cattle farming. Nevertheless, Faria et al. (2007) species, P. bahiana and P. nordestina, can be found cabrucas that harbor over 81% of the amphibian found in the adjacent biome Caatinga. The diversity detected in not anthropized forests. A total latter occurs sympatrically with P. rohdei and P. number of 41 Amphibian anurans have been reported for burmeisteri in some breeding ponds on forest the studied cabruca so far (Marciano-Jr, Ilhéus, pers. comm. 2008, Solé et al. 2009). edges (Solé, pers. obs.). Herein, we focus on the Frogs were sampled in the 5 ha cabruca from June trophic niches of both of them. 2008 to October 2008. During 41 nights, frogs of the genus Phyllomedusa were captured manually between

North-West J Zool, 6, 2010 Diet of two sympatric Phyllomedusa 15

19:00 and 21:00 at two ponds and transferred to the with an accuracy of 0.1 g and had its snout-vent length nearby laboratory within a maximum of two hours after (SVL) and mouth width (MW) measured with a digital capture. Every frog was weighted using a digital balance caliper.

Figure 1. Phyllomedusa burmeisteri (A) and Phyllomedusa rohdei (B) from a cacao plantation behind the campus of Universidade Estadual de Santa Cruz, Ilhéus, Bahia, Brazil.

Figure 2. Study site: Pond inside a cacao plantation behind the campus of Universidade Estadual de Santa Cruz, Ilhéus, Bahia, Brazil.

North-West J Zool, 6, 2010 16 Lima, J.E.P. et al.

Stomach flushing and statistics percentage of volume (100 x total volume of individuals of t in all stomachs/total volume of all taxa in all After being collected, stomach flushing as described by stomachs). Overlap in trophic niches between the two Solé et al. (2005) and Solé & Rödder (2009) was applied to species was assessed with an index proposed by May all frogs in order to assess stomach contents. A voucher and MacArthur (1972) as modified by Pianka (1974): for each of both sampled species was deposited in the n pp Museum of Zoology of Universidade Estadual de Santa B ij ik O  i Cruz. All other frogs were released at the original jk nn 22 capture site during the same night, in a maximum of four BBppij ik hours after having been captured. Flushed stomach ii contents were fixed in 70% ethanol, preserved in small Ojk = niche overlap, pij and pik represent the numeric vials and later spread on a Petri dish and analyzed under proportions of the ith resource used by the jth and kth a stereomicroscope. Prey items were classified in species. Ojk varies between 0 indicating no overlap to 1 categories representing, whenever possible, taxonomic suggesting complete overlap. orders, except for Hymenoptera, which were separated into Formicidae and non-Formicidae. Taxonomic categories follow the Tree of Life (Maddison & Schulz Results 2007). The volume of prey items was calculated for each completely preserved item using the formula 2 A total number of 76 Phyllomedusa rohdei were 4 LWCS V  DT EU captured. Most frogs were recorded in low 32 2 proposed by Dunham (1983), where V = volume, L = shrubs near ponds (n = 74) and only in a few length, and W = width of prey item. For partially cases (n = 2) perching on the forest floor. SVL digested invertebrates, the regression formulae proposed varied from 41.12 mm to 55.00 mm (mean = by Hirai and Matsui (2001) were used in order to 44.72 mm; SD = 2.31 mm). MW ranged from estimate the approximate original prey size, thus allowing the volumetric assessment using the above 13.00 mm and 17.43 mm (mean= 14.45 mm, SD mentioned formula for an ellipsoid. Prey items in an = 0.62 mm) and weight varied between 3.50 g advanced digestion stage that did not allow measuring and 9.97 g (mean = 5.24 g; SD = 1.30 g). A total the original length were also identified to order level, but number of 60 of the 76 captured and stomach not used for the volume calculation as suggested by flushed frogs revealed stomach contents. A Miranda et al. (2006). In order to compare the niche breath between the total of 14 unregimented items, 34 prey two species, the Shannon-Weaver diversity index H’ fragments and 37 remains of plants were (Weaver & Shannon 1949) was used: recovered by stomach flushing. The highest Hpp'  B iiln number of prey items flushed out of a frog was i whereby pi is the relative abundance of each prey four (mean = 1.613; SD = 0.803). The MW of the category, calculated as the proportion of prey items of a frogs and the number of prey items ingested given category to the total number of prey items. For were only slightly correlated (R2 = 0.120; p = comparison purposes, the Shannon-Weaver diversity 0.057), as were MW and length of prey items index was standardised according to H (R2 = 0.028; p = 0.242). The mean length of the J  ' n prey items ingested by P. rohdei was 5.37 mm, log( ) where n is the total number of prey categories of whereby the prey item with the minimum both species. The index of relative importance (IRI) was length (0.43 mm) belonged to the order used as a measure that reduces bias in description of Collembola and the prey item with the animal dietary data (Pianka et al. 1971, Pianka 1973): maximum length (24.26 mm) was an IRI ()( PO PI PV ) tttt Orthopteran. The mean volume of ingested where POt is the percentage of occurrence (100 x prey items was 28.82 mm3. The smallest number of stomachs contained t item / total number of volume of prey items was observed in the stomachs), PIt is the percentage of individuals (100 x total number of individuals of t in all stomachs/total number order Collembola (0.0087 mm3) and the lowest of individuals of all taxa in all stomachs), and PVt is the percentages (above 1 %) by volume in Isopoda

North-West J Zool, 6, 2010 Diet of two sympatric Phyllomedusa 17

(1.31 %) and Formicidae (1.46 %). The largest ptera, adult Diptera, Dermaptera, Collembola, volumes were observed in Lepidoptera larvae Blattaria and Ixodida. As in P. rohdei, mites and (360.29 mm3) and Orthoptera (452.45 mm3) plant remains were also quite frequent in contributing to total volume with 25.59 % and stomach contents of P. burmeisteri. The lower 32.14 %, respectively. The most frequent prey volume was observed in prey items belonging items consumed were Araneae (n = 15, n% = to the order Collembola (0.023 mm3), the 17.85%), followed by Formicidae (n = 11, n% = largest volumes were contributed by adult 13.09) and Diptera (n = 7, n% = 8.33). Mites and Coleoptera (736.54 mm3) and Lepidoptera lar- plant material were also quite frequent in the vae (1077.97 mm3). These orders also contri- stomach contents. The less frequent prey found buted to the largest percentages 21.1 % and in stomachs of P. rohdei were Blattaria, 30.9 %, respectively. The IRI values calculated Collembola, Coleoptera larvae, adult Lepido- for P. bumeisteri showed the highest value for ptera, Orthoptera larvae, and Trichoptera spiders and Lepidoptera larvae as in P. rohdei, (Table 1). As shown in Table 1, relative but the results also showed high value of IRI importance of prey items was highest for for Coleoptera. Aranea, Lepidoptera larvae and Orthopterans. There was no significant difference in the Almost all individuals of P. burmeisteri length of prey ingested by P. rohdei and were caught in high branches or on top of P. burmeisteri (F = 2.9268, p = 0.0861). bushes, and rarely observed in the soil. Of the Meanwhile the volume of prey was signi- 99 sub-adult and adult specimens of P. ficantly different (F = 4.2343, p < 0.05) between burmeisteri captured, SVL ranged from 63.80 the two species. The trophic niche breadth was mm to 89.64 mm (mean = 71.98 mm; SD = 4.89 higher in P. rohdei (H' = 2.59; J = 1.83) than in P. mm). The width of the mouth ranged from burmeisteri (H' = 1.94; J = 1.37), but in general 21.76 mm to 30.01 mm (mean = 23.67 mm; SD = the overlap in the trophic niches of both 1.36 mm) The weight of the specimens ranged species was high (O = 0.82). between 11.77 g and 42.70 g (mean = 17.79 g; SD = 5.16 g). Of the 99 analyzed specimens, 77 had prey in their stomachs. The total number Discussion of prey items found in a stomach was nine and the average 1.6. Of stomachs with contents, 28 Only one study has been previously performed complete prey items were retrieved, 38 to assess the diet of P. rohdei. Teixeira & fragments of prey and 50 items of Vrcibradic (2007) analyzing the diet of 17 males remnant vegetation. The length of prey items and three females and found as most frequent ranged from 0.55 mm (Collembola) to 29.86 prey items Plecoptera together with of a high mm (Orthoptera) (mean = 7.478 mm; SD = variety of frequently consumed arthropods 7.078). The MW of the frogs and the number of characterized by large and soft bodies (Ortho- prey items ingested were not correlated (R2 = ptera, Araneae, Blattaria and several larvae). 0.027; p = 0.977), as was not MW and length of However, since Plecoptera were not detected prey items (R2 = 0.002; p = 0.742). The most in other diet studies of Atlantic Rainforest frequent prey items were Araneae (n = 16, n% hylids and several Odonata were found in diet, = 18.39), followed by Formicidae (n = 15, n% = the authors believed that P. rohdei is an 17.24) and adult Coleopterans (n = 10, n% = opportunistic feeder frequently foraging near 11.49). The prey categories with the minimum bodies of water. The results of Teixeira & frequencies of occurrence were Orthoptera Vrcibradic (2007) are quite similar to ours, but, larvae, Mantodea, adult Lepidoptera, Hemi- although the species in our study were cap-

North-West J Zool, 6, 2010

Table 1. Prey types consumed by Phyllomedusa rhodei and Phyllomedusa burmeisteri from a cacao plantation in southern Bahia, Brazil. N = number of prey items; N% = percentage of total number; F = frequency of occurrence; F% = relative frequency of occurrence; V = volume in mm3; V% = relative volume in mm3; IRI = index of relative importance.

Phyllomedusa rohdei Phyllomedusa burmeisteri Prey category N N% F F % V V % IRI N N % F F % V V % IRI

Arachnida Acariformes 14 16.66 1311.02 - - - 13 14.94 138.78 - - - Araneae 15 17.85 1411.86 24.19 1.7 10.47 16 18.39 1510.13 284.37 8.1 12.22 Ixodida 2 2.38 21.69 1.22 0.1 1.39 1 1.15 10.68 0.34 0.0 0.61 Opiliones 2 2.38 21.69 9.61 0.7 1.58 ------

Crustacea Isopoda 2 2.38 21.69 18.57 1.3 1.79 2 2.3 21.35 - - -

Hexapoda Anoplura 3 3.57 32.54 1.12 0.1 2.06 5 5.75 5 3.38 0.11 0.0 3.04 Blattaria 1 1.19 10.85 51.24 3.6 1.89 1 1.15 10.68 147.51 4.2 2.02 Collembola 1 1.19 10.85 0.0087 0.0 0.68 1 1.15 1 0.68 0.023 0.0 0.61 Coleoptera (Ad.) 3 3.57 3 2.54 59.86 4.3 3.45 10 11.49 6 4.05 736.54 21.1 12.21 Coleoptera (Lv.) 1 1.19 1 0.85 51.64 3.7 1.9 ------Dermaptera ------1 1.15 10.68 0.16 0.0 0.61 Diptera (Ad.) 7 8.33 7 5.93 4.54 0.3 4.86 1 1.15 1 0.68 0.53 0.0 0.62 Diptera (Lv.) ------2 2.3 2 1.35 0.52 0.0 1.22



Table 1. (Continued)

Phyllomedusa rohdei Phyllomedusa burmeisteri Prey category N N% F F % V V % IRI N N % F F % V V % IRI

Hemiptera 2 2.38 21.69 61.46 4.4 2.81 1 1.15 10.68 0.2 0.0 0.61 Hymenoptera - Formicidae 11 13.09 11 9.32 20.68 1.5 7.96 15 17.24 14 9.46 9.44 0.3 8.99 Hymenoptera - other 5 5.95 5 4.24 1.17 0.1 3.42 4 4.6 4 2.7 12.04 0.3 2.55 Isoptera 3 3.57 32.54 2.98 0.2 2.11 ------Lepidoptera (Ad.) 1 1.19 1 0.85 87.54 6.2 2.75 1 1.15 1 0.68 352.11 10.1 3.97 Lepidoptera (Lv.) 5 5.95 5 4.24 360.29 25.6 11.93 7 8.05 7 4.73 1077.97 30.9 14.55 Mantodea ------1 1.15 10.68 140.17 4.0 1.95 Orthoptera (Ad.) 4 4.76 3 2.54 198.85 14.1 7.14 4 4.6 4 2.7 618.3 17.7 8.33 Orthoptera (Lv.) 1 1.19 1 0.85 452.45 32.1 11.39 1 1.15 1 0.68 112.97 3.2 1.69 Trichoptera 1 1.19 10.85 ------

Cycloneuralia Nematoda ------15 - 10 6.76 - - -

Others Plant remains - - 37 31.35 - - - - - 50 33.78 - - - Mineral remains ------7 4.73 - - -

Total 84 118 1407.42 87 148 3493.3

 20 Lima, J.E.P. et al.

tured in low shrubs near ponds, Odonata were Plants can also constitute a significant part of not detected in a single case. the diet of adults of Rana hexadactyla (Das Bertoluci (2002) reported pedal luring for P. 1996). In the present study, plants were a burmeisteri from a captive individual that constant food group for most specimens, with readily fed on Orthoptera and Blattaria, but a moderate degree of preference compared to ignored beetle larvae (Tenebrio sp.). Duré other food items. We do not know if the (1999), studying the diet of a population of ingestion of plant material was accidental Phyllomedusa hypochondrialis from Corrientes, while preying on the arthropods or intentional. Argentina, found Diptera to make up 76.3 % of Amphibians may choose to ingest vegetation total stomach contents and 58.1 % of total or mineral material because these can speed up volume. The second category in importance the removal of intestinal parasites such as the was Homoptera with 10.5 % of all dietary nematodes detected herein, may provide items ingested. Note that according to roughness facilitating crushing the exoskeleton Caramaschi (2006) the Argentinean popu- of arthropods (Evans & Lampo 1996), provide lations of Phyllomedusa belonging to the P. nutrients, and may even serve as an additional hypochondrialis group should be assigned to resource of water to prevent desiccation Phyllomedusa azurea. (Anderson et al. 1999). The presence of struc- Terrestrial invertebrates usually dominate tures of plants in the stomachs indicates that the diet of most anurans, even in those species vegetation is not only used as a breeding site, which are aquatic or semiaquatic (e.g. Hirai & but also as foraging territory (Santos et al. Matsui 2001, Stewart & Sandison 1972, Sas et 2004). Information on the consumption of al. 2009). It is well known that most adult plants by amphibians may therefore contribute anurans are able to prey on a broad spectrum to the understanding of behavioral patterns. of invertebrates, ranging from small Collem- It might be reasonable to assume that diet bola and mites to large Odonata and Lepido- composition of species may vary according to ptera, from soft tissue animals as Annelida to the prey items available in a specific habitat animals with strongly keratinized or calcified (Hirai & Matsui 1999; Lizana et al. 1986; for bodies as Coleoptera and Crustaceae (Solé & Hylid frogs see Maneyro & da Rosa, 2004). Rödder 2009). Small vertebrates are also con- Hence, variations in diet composition between sumed by larger anuran species (e.g. Teixeira & natural and anthropogenized habitats should Vrcibradic 2003, Çiçek & Mermer 2006, Sas et be expected (Solé et al. 2009). However, al. 2009), but were not detected during our comparisons of our results with those pre- investigation. The ingestion of plants and sented by Teixeira & Vrcibradic (2007) revealed mineral material is often considered accidental no major differences despite two prey types in anurans (Brandão et al. 2003, Aszalós et al. not detected in our samples. These were 2005, Solé & Pelz 2007, Kovács et al. 2007), but Plecoptera, numerically dominant and most folivory (Das 1996) or frugivory (Silva & Britto- frequently consumed prey item in Teixeira & Pereira 2006, Solé et al. 2009) has been reported Vrcibradic´s samples and Odonata, ingested in for a few species. Reports on herbivory in Nova Venécia, Espirito Santo, Brazil. A lack of tropical frogs have become more frequent in obvious differences in the diet composition the past years. Silva et al. (1989) demonstrated was also detected in comparisons among that Xenohyla truncata includes bromeliad fruit Leptodactylus ocellatus specimens inhabiting and seeds in its diet, especially during the dry cacao plantations and natural habitats made by season, when invertebrates are less abundant. Solé et al. (2009). This apparent lack of diffe-

North-West J Zool, 6, 2010 Diet of two sympatric Phyllomedusa 21 rences may be explained by the opportunistic tinguished. Toft (1980) described two main diet feeding behavior of the species studied. patterns in anurans: The “ant specialists” that Several studies reported that SVL and MW feed on strongly chitinized, slow-moving were significantly correlated with prey size arthropods such as mites and ants and the and volume in other species (Franca et al. 2004, “non-ant-specialists” that feed on a greater Maneyro et al. 2004). However, simple linear variety of less chitinous arthropods and avoid regression analyses in our study revealed no ingesting ants. According to our results, both significant relationships between SVL and MW P. burmeisteri and P. rohdei can be classified as of both P. burmeisteri and P. rohdei and prey non-ant-specialists sensu Toft (1980). Feeding volume, minimum lengths of prey items and specialization is often associated with a type of maximum length of prey items. Since variation foraging mode, whereby active feeders prey on in size was low in our sample (Figure 3), it is a larger number of smaller preys that often live likely that the failure to detect significant in aggregations as ants and termites (Toft 1980, relationships between SVL (and mouth width) 1981). On the other hand, sit-and-wait foragers and prey size was caused by the high pro- commonly prey on large, mobile and solitary portion of adult specimens included. Maneyro invertebrates as beetles and spiders with only a et al. (2004) and Franca et al. (2004) sampled few items consumed per time unit what is frogs in different habitats including a higher apparently the case in both species analyzed proportion of juveniles enhancing size varia- herein. Additionally, “sit-and-wait” feeders tion. use to be predated by active predators (like Anurans are able to distinguish between snakes), and are not aposematic, but mymetic. different prey types, thus allowing different This seems to be the case of frogs in the Genus feeding specialization degrees, whereby com- Phyllomedusa, reinforcing the interpretation monly two main feeding strategies are dis- discussed above.

80

70

60

50 SVL [mm] SVL

40

30 P burmeisteri P rohdei

Figure 3. Variation in Snout-Vent Length (SVL) in Phyllomedusa burmeisteri and Phyllomedusa rohdei from a cacao plantation in Northeastern Brazil. Short horizontal bars indicate minimum and maximum values; broad horizontal bars indicate first quartiles, medians and third quartile; averages are indicated by red crosses.

North-West J Zool, 6, 2010 22 Lima, J.E.P. et al.

Acknowledgements. We would like to thank Instituto Chico Carnaval, A.C., Hickerson, M.J., Haddad, C.F.B., Rodrigues, Mendes de Conservação da Biodiversidade (ICMBio) for M.T., Moritz, C. (2009): Stability predicts genetic issuing the permanent research license no. 13708-1 (ICMBio). diversity in the Brazilian Atlantic Forest. Science 323: For suggestions on the manuscript we thank Anibal Ramadan 785-789. Oliveira, Éva-Hajnalka Kovács, Lucimeire de Souza Ramos Çiçek, K., Mermer, A. (2006): Feeding biology of the Marsh Lacau, Raúl Maneyro, Tibor Hartel and Yvonnick Le Pendu. Frog, Rana ridibunda Pallas 1771, (Anura, Ranidae) in DR is grateful to the research initiative of the Ministry of Turkey’s Lake District. North-Western Journal of Education, Science, Youth and Culture of the Rhineland- Zoology 2: 57-72. Palatinate state of Germany (‘Die Folgen des Global Change Das, I. 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