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Effects of the presence of litter on the composition of stream tadpoles' assemblages in an Atlantic Forest remnant of southeastern Brazil

Efeitos da presença de serapilheira na composição de assembleias de girinos de riacho em um remanescente de Mata Atlântica do sudeste do Brasil

Abstract:

Many tropical anurans use forest streams to deposit their eggs, but resource use and selection by tadpoles in tropical forests are poorly known. In the present research, we hypothesized that leaf litter and water depth affect tadpole assemblages due to adult habitat selection for oviposition and/or microhabitat selection by tadpoles. Fieldwork was carried out in the Estação Biológica de Boracéia, an Atlantic Rainforest reserve in São Paulo state, southeastern Brazil. We sampled tadpoles during a year using 40 double-entry funnel-traps distributed along four streams in the forest. Only leaf litter effects are species dependent. We discussed that habitat structure significance depends on the morphological and ecological adaptation to forage and avoid competition within the tadpole community.

Keywords:
Amphibians ; Aplastodiscus leucopygius; Bokermannohyla hylax; microhabitat selection ; Scinax obtriangulatus, Phasmahyla cochranae; southeastern Brazil ; tadpoles

Resumo:

Uma variedade de espécies de anuros tropicais usa riachos da floresta para depositar seus ovos, mas o uso e a seleção de recursos por girinos em florestas tropicais são pouco conhecidos. Na presente pesquisa, nossa hipótese era a de que a presença de serapilheira e a profundidade das poça dos riachos influenciam a presença de girinos devido à seleção de habitats de ovipostura pelos adultos e/ou seleção de micro-habitats pelos girinos. O trabalho de campo foi realizado na Estação Biológica de Boracéia, uma reserva de Mata Atlântica no estado de São Paulo, sudeste do Brasil. Amostramos girinos durante um ano usando 40 armadilhas-de-funil de dupla entrada distribuídas ao longo de quatro riachos na floresta. Apenas os efeitos da presença de serapilheira foram significativos Nós discutimos as relações entre a estrutura do habitat e características morfológicas, ecológicas e adaptações para procura de alimento e para evitar competição no interior da comunidade de girinos.

Palavras-chave:
Anfíbios ; Aplastodiscus leucopygius; Bokermannohyla hylax; girinos ; Phasmahyla cochranae; Scinax obtriangulatus; seleção de micro-habitat ; sudeste do Brasil

Introduction

Anuran amphibians exhibit a combination of particular reproductive strategies that includes selective breeding sites, clutch characteristics, rate and duration of larval development, and eventually parental care (Haddad & Prado 2005HADDAD, C.F.B. & PRADO, C.P.A. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil. BioScience 55(3):207-217.), linked to their spatial distribution and reproductive success (Haddad & Sawaya 2000HADDAD, C.F.B. & SAWAYA, R.J. 2000. Reproductive modes of Atlantic forest hylid frogs: a general overview and the description of a new mode. Biotropica 32(4b): 862-871, Wells 2007WELLS, K.D. 2007. The Ecology and Behavior of Amphibians. Chicago, USA: The University of Chicago Press.). Tadpoles are generally found in water bodies suitable for their development and success that are selected by their parents (Wells 2007WELLS, K.D. 2007. The Ecology and Behavior of Amphibians. Chicago, USA: The University of Chicago Press.). In these water bodies it is expected that local factors related to habitat structure and resource quality explain tadpole richness, diversity and development (Savage 1952SAVAGE, R.M. 1952. Ecological, physiological and anatomical observations on some species of anuran tadpoles. Proc. Zool. Soc. London 122(2):467-514., Stoler & Relyea 2013bSTOLER, A.B. & RELYEA, R.A. 2013b. Bottom-up meets top-down: leaf litter inputs influence predator-prey interactions in wetlands. Oecologia 173(1):249-257., Almeida et al. 2015ALMEIDA, A.P., RODRIGUES, D.J., GAREY, M.V. & MENIN, M. 2015. Tadpole richness in riparian areas is dby niche-based and neutral processes. Hydrobiologia 745(1):123-35.).

Generally, habitat use discerns among tadpoles of different species (Kopp & Eterovick 2006KOPP, K., WACHLEVSKI, M. & ETEROVICK, P.C. 2006. Environmental complexity reduces tadpole predation by water bugs. Can. J. Zool. 84(1):136-140.), as variation in morphology, physiology, and phenology impose restrictions on the way tadpoles explore the microhabitats (Fatorelli & Rocha 2009FATORELLI, P. & ROCHA, C.F.D. 2009. O que molda as guildas de girinos tropicais? Quarenta anos de busca de padrões. Oecol. Bras. 12(4):733-742.). When sharing the same site, tadpole assemblages are organized to avoid competition while keeping safe from predators (Heyer 1976HEYER, W.R. 1976. Studies in larval amphibian habitat partitioning. Smithson. Contr. Zool. 242:1-27.). Most tadpoles are filter-feeders, which can impose high levels of competition to species sharing the same pond (Fatorelli & Rocha 2009FATORELLI, P. & ROCHA, C.F.D. 2009. O que molda as guildas de girinos tropicais? Quarenta anos de busca de padrões. Oecol. Bras. 12(4):733-742.), unless there is a partitioning of resources in terms of space, time, or food (Heyer 1976HEYER, W.R. 1976. Studies in larval amphibian habitat partitioning. Smithson. Contr. Zool. 242:1-27.). For instance, tadpoles can differ in the foraging mode using the water surface, mid-water, or water bottom (Heyer 1973HEYER, W.R. 1973. "Ecological Interactions of Frog Larvae at a Seasonal Tropical Location in Thailand." Journal of Herpetology. https://doi.org/10.2307/1562868.
https://doi.org/10.2307/1562868...
, 1976HEYER, W.R. 1976. Studies in larval amphibian habitat partitioning. Smithson. Contr. Zool. 242:1-27.).

Resource quality also affects tadpole morphology and development, as larvae scratch the substrate and ingest nutrients directly by litter consumption or grazing microbial communities (Savage 1952SAVAGE, R.M. 1952. Ecological, physiological and anatomical observations on some species of anuran tadpoles. Proc. Zool. Soc. London 122(2):467-514., Stoler & Relyea 2013bSTOLER, A.B. & RELYEA, R.A. 2013b. Bottom-up meets top-down: leaf litter inputs influence predator-prey interactions in wetlands. Oecologia 173(1):249-257.). Leaf litter inputs are dominant energy and nutrient resources for tadpoles and yet can reduce their predation rate, acting as a refuge (Stoler & Relyea 2013aSTOLER, A.B. & RELYEA, R.A. 2013a. Leaf litter quality induces morphological and developmental changes in larval amphibians. Ecology 94(7):1594-1603.). Further, vegetation composition affects litter quality, which induces phenotypic and morphological changes on the consumers, potentially altering their fitness (Stoler & Relyea 2013bSTOLER, A.B. & RELYEA, R.A. 2013b. Bottom-up meets top-down: leaf litter inputs influence predator-prey interactions in wetlands. Oecologia 173(1):249-257.).

Many abiotic and biotic factors can influence the structure of tropical tadpole assemblages (Borges Júnior & Rocha 2013BORGES JÚNIOR, V. & ROCHA. 2013. Tropical tadpoles assemblages: which factors affect their structure and distribution? Oecol. Aust. 17(2): 217-228., Marques et al. 2019MARQUES, N.C.S., RATTIS, L. & NOMURA, F. 2019. Local environmental conditions affecting anuran tadpoles' microhabitat choice and morphological adaptation. Mar. Freshwater Res. 70(3):395-401.). A variety of tropical anurans use forest streams to deposit their eggs, and there are few reports on how changes in microhabitat influence tadpoles (Kopp & Eterovick 2006KOPP, K., WACHLEVSKI, M. & ETEROVICK, P.C. 2006. Environmental complexity reduces tadpole predation by water bugs. Can. J. Zool. 84(1):136-140., Kopp et al. 2006KOPP, K. & ETEROVICK, P.C. 2006. Factors influencing spatial and temporal structure of frog assemblages at ponds in southeastern Brazil. J. Nat. Hist. 40(29-31):1813-1830., Caldas et al. 2019CALDAS, F.L.S., SILVA, B.D., DE-CARVALHO, C.B., SANTANA, D.O., GOMES, F.F.A, CAVALCANTI, L.B.Q., SANTOS, R.A. & FARIA, R.G. 2019. Factors determining the spatial and temporal variation in the abundance of Pithecopus nordestinus tadpoles (Anura: Phyllomedusidae) in a semi-arid Brazilian environment. Salamandra 55(4):253-263.). In the Atlantic Rainforest, the composition of stream tadpoles' assemblages is influenced by abiotic and biotic factors (Eterovick & Barata 2006ETEROVICK, P.C. & BARATA, I.M. 2006. Distribution of tadpoles within and among Brazilian streams: the influence of predators, habitat size and heterogeneity. Herpetologica 62(4):365-377., Kopp & Eterovick 2006KOPP, K. & ETEROVICK, P.C. 2006. Factors influencing spatial and temporal structure of frog assemblages at ponds in southeastern Brazil. J. Nat. Hist. 40(29-31):1813-1830., Bertoluci et al. 2013BERTOLUCI, J., ROCHA, P.L. & RODRIGUES, M.T. 2013. Field evidence of coupled cycles of arthropod predator-tadpole prey abundance in six aquatic systems of an Atlantic Rainforest site in Brazil. Herpetol. J. 23(1):63-66., Jordani et al. 2017JORDANI, M.X., MELO, L.S.O., QUEIROZ, C.S., ROSSA-FERES, D.C. & GAREY, M.V. 2017. Tadpole community structure in lentic and lotic habitats: richness and diversity in the Atlantic rainforest lowland. Herpetol. J 27(3):299-306.), making species more prone to resource partitioning (Melo et al. 2018MELO, L.S.O., GAREY, M.V. & ROSSA-FERES, D.C. 2018. Looking for a place: how are tadpoles distributed within tropical ponds and streams? Herpetol. Notes 11:379-386.). Atlantic rainforest streams are often composed of interconnected shallow puddles with rocky bottom, whose depth and presence of litter vary greatly. These are the main habitats to stream tadpoles, so it is expected physical characteristics of puddles influence tadpole occurrence. In the present study, we hypothesized that water depth and/or the presence of leaf litter affect the species composition of tadpoles' assemblages in Atlantic rainforest streams.

Material and Methods

1. Study site and data collection

Fieldwork was carried out in the Estação Biológica de Boracéia (EBB), an Atlantic Rainforest reserve with 16,450 ha located at 900 m a.s.l. in one of the wettest regions of São Paulo state, southeastern Brazil (Setzer 1946SETZER, J. 1946. Atlas Climático e Ecolóico do Estado de São Paulo. São Paulo: Comissão Interestadual da Bacia Parana-Uruguai/CESP.) (Figure 1). Rainfall was irregularly distributed during the study period, with total precipitation of 1,747.3 mm and rainy season extending from September to March (Bertoluci et al. 2013BERTOLUCI, J., ROCHA, P.L. & RODRIGUES, M.T. 2013. Field evidence of coupled cycles of arthropod predator-tadpole prey abundance in six aquatic systems of an Atlantic Rainforest site in Brazil. Herpetol. J. 23(1):63-66.). The area is covered by Dense Ombrophylous Forest, with an understory relatively opened but denser along streams (Bertoluci & Rodrigues 2002BERTOLUCI, J. & RODRIGUES, M.T. 2002. Seasonal patterns of breeding activity of Atlantic Rainforest anurans at Boracéia, southeastern Brazil. Amphibia-Reptilia 23(2):161-67.).

Figure 1
Location of the study site in the Atlantic rainforest (red circle) and of streams R1 to R4 in the study site (red stars).

We selected four streams to obtain data on the association of microhabitat variables and the species composition of tadpole assemblage (sites R1 to R4 in Bertoluci & Rodrigues 2002BERTOLUCI, J. & RODRIGUES, M.T. 2002. Seasonal patterns of breeding activity of Atlantic Rainforest anurans at Boracéia, southeastern Brazil. Amphibia-Reptilia 23(2):161-67.; Figure 1). R1 corresponds to a small stream (60 m long, 1.3 m wide, 22 cm maximum depth) located in the primary forest and containing interconnected rocky or muddy puddles with organic matter in decomposition, mainly dead leaves and sticks. R2 is a small stream (50 m, 1.8 m, 27 cm) in the forest edge. R3 is a small stream (96 m, 2 m, 32 cm) in the primary forest with interconnected puddles with a rocky, sandy bottom and dead leaves. R4 is a small stream (91 m, 2.4 m, 30 cm) inside the forest; its bed is mainly rocky, but some puddles have sand and dead leaves (Table 1).

Table 1
Characteristics of the four streams used for the study of tadpoles in a remnant of the in Atlantic Forest at the Estação Biológica de Boracéia, São Paulo state, southeastern Brazil.

Tadpole sampling were carried out with 40 double-entry funnel-traps constructed with two 2-L plastic bottles, which result in approximately 1.5-L traps; traps were entirely submerged at the bottom of the stream puddles (Figure 2). We estimated the relative abundances of tadpoles in 40 traps distributed along the selected streams (10 traps in each stream). Sampling was carried out monthly with traps kept active during 72 hours per month from September 1993 to September 1994. The species abundance was calculated by summing the total of all individuals collected through the year. The microhabitat of each plot was characterized based on two variables: water depth (measured with a ruler in the deepest point of each stream puddle, where the trap was positioned; depth did not vary significantly along the year) and presence or absence of leaf litter (0 or 1). We built a matrix crossing the tadpole species and their microhabitat features to conduct an ordination or gradient analysis.

Figure 2
(A) Double-entry funnel-trap used in tadpole sampling (this photo was not taken at the study site). (B-E) Puddles in the streams R1 to R4, all of them containing leaf litter in the bottom.

2.Data analysis

In order to evaluate the effects of microhabitat variables on the tadpole composition, we used PerMANOVA (bray-curtis method), with presence/absence of litter as fixed factor and stream depth as covariate. Considering that our sampling observations are not independent (pseudo-replication) we used the stream ID (R1, R2, R3, and R4) to restrict the permutations in PerMANOVA, using the argument "strata" in the function "adonis" in R. We plotted the variables and species using NDMS. This analysis was performed using R 3.6.3 version. Significance level adopted in the study was 0.05.

Results

Four anuran tadpole species known to inhabit streams were captured in our study in EBB: Aplastodiscus leucopygius (N = 146), Bokermannohyla hylax (139), Scinax obtriangulatus (89) (Hylidae), and Phasmahyla cochranae (2) (Phyllomedusidae) (Figure 3). The analysis of microhabitat use and selection was performed with only 38 out of the 40 initial traps because two traps were empty. The number of tadpoles per trap varied from 0 to 79, and the abundance distributions for all species was very skewed (Table 2). Tadpoles of different species shared the same trap in 37% (Figure 4), mostly with B. hylax and A. leucopygius. These two species were captured together in 32% of the samplings. On the other hand, only two tadpoles of S. obtriangulatus were observed sharing the same trap with tadpoles of B. hylax. One tadpole of S. obtriangulatus was observed with 26 tadpoles of B. hylax, and in another occasion one tadpole was captured with two tadpoles of B. hylax. Phasmahyla cochranae tadpoles was observed sharing the same trap with one tadpole of B. hylax, and on another occasion, it was found in the same trap with one tadpole of A. leucopygius (Figure 4).

Figure 3
Tadpoles collected in this study. (A-B) Aplastodiscus leucopygius (cryptic form and tadpole changing to the green coloration of adults; note the red eyes), (C) Bokermannohyla hylax (note the unpigmented spiracle), (D) Scinax obtriangulatus (advanced stage of metamorphosis), (E) Phasmahyla cochranae (note the anterodorsal funnel-shaped oral disc).

Figure 4
Tadpole abundances of four anuran species in 38 traps distributed in four streams of an Atlantic rainforest remnant of southeastern Brazil.

Table 2
Captures of tadpoles of four anuran species in 38 traps in Atlantic Forest streams at the Estação Biológica de Boracéia, southeastern Brazil. Values are discriminated for sampling unities with (n = 27) and without (n = 11) litter. Values are presented as: (total number collected; number of plots where the species occurred) and mean ± standard deviation.

Using PerMANOVA we detected effect of presence/absence leaf litter on the composition of tadpole community (F3,37 = 9.3238, p = 0.030) but not of the stream depth (F3,37 = 1.4364, p = 0.677) (Figure 5).

Figure 5
Biplot showing the systematic change of tadpole community composition (relative abundance) with change in water depth and presence of leaf litter in the streams studied at Estação Biológica de Boracéia, southeastern Brazil. Blue and orange circles represent observations with and without leaf litter, respectively.

Discussion

The tadpole assemblages studied in EBB showed partitioning organization with habitat structure discerning among tadpole species. These findings corroborate other studies in the Atlantic rainforest, like those of Jordani et al. (2017)JORDANI, M.X., MELO, L.S.O., QUEIROZ, C.S., ROSSA-FERES, D.C. & GAREY, M.V. 2017. Tadpole community structure in lentic and lotic habitats: richness and diversity in the Atlantic rainforest lowland. Herpetol. J 27(3):299-306., which shows that habitat type (lentic or lotic) influences the structure of the assemblages, and of Kopp & Eterovick (2006)KOPP, K., WACHLEVSKI, M. & ETEROVICK, P.C. 2006. Environmental complexity reduces tadpole predation by water bugs. Can. J. Zool. 84(1):136-140., which demonstrates that patterns of species distributions are due to environmental and stochastic factors rather than by predation. According to Kopp et al. (2006)KOPP, K. & ETEROVICK, P.C. 2006. Factors influencing spatial and temporal structure of frog assemblages at ponds in southeastern Brazil. J. Nat. Hist. 40(29-31):1813-1830., the choice of shallow or deep areas in the water column can be a strategy to avoid predation or interspecific competition. In the present study, we did not find a correlation with puddle depth, but species were associated with the presence of litter. An early description of S. obtriangulatus in Boracéia witnessed tadpoles of this species using the bottom of the puddle in a small stream in the forest (Heyer et al. 1990HEYER, W.R., RAND, A.S., CRUZ, C.A.G, PEIXOTO, O.L. & NELSON, C.E. 1990. Frogs of Boracéia. Arq. Zool. 31(4):231-410.). Due to their anteroventral mouth tadpoles of P. cochranae forage swimming in the water surface and sometimes float motionless at mid-water (Leão-Pires et al. 2017LEÃO-PIRES, T.A., GIARETTA, A. & SAWAYA, R.J. 2017. The diurnal aggregation behavior in Phasmahyla cochranae tadpoles (Anura: Phyllomedusidae). Basic Appl. Herpetol. 31:117-123.). Puddle depth did not influence the occurrence of Phasmahyla nordestinus tadpoles, suggesting a strategy to avoid competition or a response to unpredictable temporary aquatics habitats, limiting the degree of specialization for resources in the Brazilian semi-arid, an environment subjected to water scarcity and irregularities (Caldas et al. 2019CALDAS, F.L.S., SILVA, B.D., DE-CARVALHO, C.B., SANTANA, D.O., GOMES, F.F.A, CAVALCANTI, L.B.Q., SANTOS, R.A. & FARIA, R.G. 2019. Factors determining the spatial and temporal variation in the abundance of Pithecopus nordestinus tadpoles (Anura: Phyllomedusidae) in a semi-arid Brazilian environment. Salamandra 55(4):253-263.). Phasmahyla cochranae tadpoles present schooling and aggregation behavior associated with daylight (Leão-Pires et al. 2017LEÃO-PIRES, T.A., GIARETTA, A. & SAWAYA, R.J. 2017. The diurnal aggregation behavior in Phasmahyla cochranae tadpoles (Anura: Phyllomedusidae). Basic Appl. Herpetol. 31:117-123.). In the present study, only two tadpoles of P. cochranae were captured and on different occasions, which is easily explained by the fact that the traps were set at the bottom of the stream, reducing the probability of capturing non-benthic tadpoles. Apart from daylight, tadpole aggregation behavior is linked to water transparency, temperature, and other characteristics not investigated in the present study (Branch 1983BRANCH, L.C. 1983. Social behavior of the tadpoles of Phyllomedusa vaillanti Copeia 1983(2):420-428., Spieler 2003SPIELER, M. 2003. Risk of predation affects aggregation size: a study with tadpoles of Phrynomantis microps (Anura: Microhylidae). Anim. Behav. 65(1):179-184.). However, it is known that tadpoles of P. cochranae and S. obtriangulatus are more active during the day (Carvalho-e-Silva 1986CARVALHO-E-SILVA, S.P. 1986. Girinos de espécies do gênero Ololygon pertencentes ao grupo 'catharinae', no Estado do Rio de Janeiro. M.Sc. Dissertation. Universidade Federal do Rio de Janeiro, Brazil. 77 p., Leão-Pires et al. 2017LEÃO-PIRES, T.A., GIARETTA, A. & SAWAYA, R.J. 2017. The diurnal aggregation behavior in Phasmahyla cochranae tadpoles (Anura: Phyllomedusidae). Basic Appl. Herpetol. 31:117-123.). Behavior shift can also be a strategy to avoid overlapping and interspecific competition as well to assure protection against predators (Carlson & Langkilde 2013CARLSON, B.E. & LANGKILDE. T. 2013. A common marking technique affects tadpole behavior and risk of predation. Ethology 119(1):167-177.).

Diel activity behavior can be a sign of tadpole assemblage organization and partitioning (Heyer 1976HEYER, W.R. 1976. Studies in larval amphibian habitat partitioning. Smithson. Contr. Zool. 242:1-27.). Bokermannohyla hylax and A. leucopygius tadpoles are also more active at night presumably to avoid predators (Bertoluci 2002BERTOLUCI, J. 2002. Diel activity of the tadpoles of Hyla hylax (Anura: Hylidae) at Boracéia, southeastern Brazil. Phyllomedusa 1(1):41-43., Gomes and Peixoto 2002GOMES, M.R., & PEIXOTO, O.L. 2002. O girino de Hyla leucopygia Cruz & Peixoto, 1987 (Amphibia, Anura, Hylidae). Bol. Mus. Biol. Mello Leitão 13:17-25.). These two species show specialized reproductive modes associated with forest streams (Haddad & Prado 2005HADDAD, C.F.B. & PRADO, C.P.A. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil. BioScience 55(3):207-217., Gomes & Peixoto 2002GOMES, M.R., & PEIXOTO, O.L. 2002. O girino de Hyla leucopygia Cruz & Peixoto, 1987 (Amphibia, Anura, Hylidae). Bol. Mus. Biol. Mello Leitão 13:17-25.). Together they were the most abundant tadpoles in our sampling and often shared the same trap. The dark chocolate-brown coloration of B. hylax tadpoles shows an advantage when seeking cover among the leaf litter, rocks, and mud in the streambed (Bertoluci et al. 2003BERTOLUCI, J., XAVIER, V. & CASSIMIRO, J. 2003. Description of the tadpole of Hyla hylax Heyer, 1985 (Anura, Hylidae) with notes on its ecology. Amphibia-Reptilia 24(4):509-514.). This could likewise represent an advantage for A. leucopygius with a cryptic coloration that hides under litter and rocks (Gomes & Peixoto 2002GOMES, M.R., & PEIXOTO, O.L. 2002. O girino de Hyla leucopygia Cruz & Peixoto, 1987 (Amphibia, Anura, Hylidae). Bol. Mus. Biol. Mello Leitão 13:17-25.), except in the advanced stages of metamorphosis, when tadpoles turn to green (Figure 3A-B).

Differences in the habitat structure used by tadpoles is perhaps a combination between oviposition site selection by adults and microhabitat selection by tadpoles, owing to evidences that each life-history stage evolves independently (Sherratt et al. 2017SHERRATT, E., VIDAL-GARCÍA, M., ANSTIS, M. & KEOGH, J.S. 2017. Adult frogs and tadpoles have different macroevolutionary patterns across the Australian continent. Nat. Ecol. Evol. 1:1385-1391.). Habitat structure, such as leaf litter cover and depth, humidity, vegetation, and canopy cover, offer insights into amphibian richness and abundance (Jongsma et al. 2014JONGSMA, G.F.M., HEDLEY, R.W., DURÃES, R. & KARUBIAN, J. 2014. Amphibian diversity and species composition in relation to habitat type and alteration in the Mache-Chindul Reserve, northwest Ecuador. Herpetologica 70(1):34-46., Marques et al. 2019MARQUES, N.C.S., RATTIS, L. & NOMURA, F. 2019. Local environmental conditions affecting anuran tadpoles' microhabitat choice and morphological adaptation. Mar. Freshwater Res. 70(3):395-401.). Generally, oviposition sites will be near habitats suitable for mating by the adults, yet adult anuran and tadpoles may use distinct spatial resources during their complex life cycle (Haddad & Sawaya 2000HADDAD, C.F.B. & SAWAYA, R.J. 2000. Reproductive modes of Atlantic forest hylid frogs: a general overview and the description of a new mode. Biotropica 32(4b): 862-871, Rudolf & Rödel 2005RUDOLF, V.H.W. & RÖDEL, M.O. 2005. Oviposition site selection in a complex and variable environment: the role of habitat quality and conspecific cues. Oecologia 142:316-325., Wells 2007WELLS, K.D. 2007. The Ecology and Behavior of Amphibians. Chicago, USA: The University of Chicago Press.). Aplastodiscus leucopygius has a long breeding season, benefiting from the rain for reproduction (Bertoluci & Rodrigues 2002BERTOLUCI, J. & RODRIGUES, M.T. 2002. Seasonal patterns of breeding activity of Atlantic Rainforest anurans at Boracéia, southeastern Brazil. Amphibia-Reptilia 23(2):161-67.). This species shows a complex courtship with males guiding females to subterranean nests previously constructed by them (Haddad & Sawaya 2000HADDAD, C.F.B. & SAWAYA, R.J. 2000. Reproductive modes of Atlantic forest hylid frogs: a general overview and the description of a new mode. Biotropica 32(4b): 862-871). Tadpoles then scape from the nests chambers when it floods by the rise in the pond's water level caused by heavy rains and reach the water bodies in either streams or temporary ponds (Haddad & Prado 2005HADDAD, C.F.B. & PRADO, C.P.A. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil. BioScience 55(3):207-217.). This adaptation suggests some tolerance and flexibility of tadpoles to cope with external unpredictable factors influenced by hydrological cycles, water depth, or litter availability. In any case, high specializations to habitat structure represent disadvantageous to the species survivorship in unpredictable environments (Ultsch et al. 1999ULTSCH, G.R., BRADFORD, D.F. & FREDA, J. 1999. Physiology coping with the environment. In Tadpoles: The Biology of Anuran Larvae (R.W. McDiarmid & R. Altig, eds.). University of Chicago Press, Berkeley, p. 189-214.).

Tadpoles of different species show different habitat exploration strategies associated with their physiology, morphology, and phenology (Zimmerman & Simberloff 1996ZIMMERMAN, B.L. & SIMBERLOFF, D. 1996. An historical interpretation of habitat use by frogs in a Central Amazonian forest. J. Biogeogr. 23(1):27-46.). A combination of evolutionary processes is involved either in the choice of oviposition sites by adults or in the resource use by tadpoles, being survival their end goal. Yet anuran mortality is highest during the larvae stage (Heyer 1973HEYER, W.R. 1973. Ecological interactions of frog larvae at a seasonal tropical location in Thailand. J. Herpetol. 7(4):337-361.). Anurans in the Atlantic Rainforest are known for their specialized reproductive modes (Haddad & Prado 2005HADDAD, C.F.B. & PRADO, C.P.A. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil. BioScience 55(3):207-217.). The four species studied here showed various adaptations to their microhabitats, represented by distinct evolutionary processes that guarantee their safe development. In other words, each species has its own evolutionary strategy to ensure larval phase and adult recruitment success, a combination of adult selection for breeding and oviposition sites and tadpole strategies to forage, hide, and escape from predators and avoid competitors. Habitat use will then depend on the resources available when larvae emerge from eggs, as they have limited locomotor ability at this stage (Heyer 1976HEYER, W.R. 1976. Studies in larval amphibian habitat partitioning. Smithson. Contr. Zool. 242:1-27.).

Tadpoles play essential roles in tropical streams not only as prey but also producing substantial amounts of egested particles (still understudied) that are critical nutrient sources in streams (Ramamonjisoa & Natuhara 2018RAMAMONJISOA, N. & NATUHARA, Y. 2018. Contrasting effects of functionally distinct tadpole species on nutrient cycling and litter breakdown in a tropical rainforest stream. Freshw. Biol. 63(2):202-213., Iwai et al. 2009IWAI, N., PEARSON, R.G. & ALFORD, R.A. 2009. Shredder-tadpole facilitation of leaf litter decomposition in a tropical stream. Freshw. Biol. 54(12):2573-2580.), and so they act as abiotic and biotic elements of aquatic communities (Stoler et al. 2016STOLER, A.B., BURKE, D.J. & RELYEA, R.A. 2016. Litter chemistry and chemical diversity drive ecosystem processes in forest ponds. Ecology 97(7):1783-95.). Additional comparison between lentic and lotic habitats could show distinct outcomes as consumers may have different responses to litter in ponds and wetlands that retain litter for extended periods compared to streams (Melo et al. 2017MELO, L.S.O., GONÇALVES-SOUZA, T., GAREY, M.V. & CERQUEIRA, D. 2017. Tadpole species richness within lentic and lotic microhabitats: an interactive influence of environmental and spatial factors. Herpetol. J. 27 (4):339-345., Stoler et al. 2016STOLER, A.B., BURKE, D.J. & RELYEA, R.A. 2016. Litter chemistry and chemical diversity drive ecosystem processes in forest ponds. Ecology 97(7):1783-95., Stoler & Relyea 2016STOLER, A.B. & RELYEA, R.A. 2016. Leaf litter species identity alters the structure of pond communities. Oikos 125(2):179-91.).

We concluded that presence/absence of leaf litter has an effect on the composition of stream tadpoles' assemblages. Anyhow, the presence of vegetation can be an important variable influencing tadpole richness of both ponds and streams (Kopp et al. 2006KOPP, K., WACHLEVSKI, M. & ETEROVICK, P.C. 2006. Environmental complexity reduces tadpole predation by water bugs. Can. J. Zool. 84(1):136-140.). Vegetation type and presence were not investigated in the present study, but their influence could be an important component in the species composition (Kopp & Eterovick 2006KOPP, K. & ETEROVICK, P.C. 2006. Factors influencing spatial and temporal structure of frog assemblages at ponds in southeastern Brazil. J. Nat. Hist. 40(29-31):1813-1830., Melo et al. 2018MELO, L.S.O., GAREY, M.V. & ROSSA-FERES, D.C. 2018. Looking for a place: how are tadpoles distributed within tropical ponds and streams? Herpetol. Notes 11:379-386.). Future studies are recommended to comprehend each species' response to different types of resources, such as vegetation, water rate, streambed, daylight, and in lentic habitats, considering the species morphology and phylogeny.

Acknowledgments

We thank FAPESP for a grant to JB (process number 96/6701-3). This study was supported in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. CNPq provided productivity grants to JB, PLBR, and MTR. PLBR was supported by a scholarship from Fundação de Amparo à Pesquisa do Estado da Bahia during his association with the project. Thanks are due to Gabriel Skuk (in memorian), for suggesting the design of the funnel traps, and to Cybele Araújo, for de drawing of the trap.

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Publication Dates

  • Publication in this collection
    23 Aug 2021
  • Date of issue
    2021

History

  • Received
    13 Oct 2020
  • Reviewed
    02 July 2021
  • Accepted
    05 July 2021
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