While deforestation is one of the greatest drivers of biodiversity loss, our understanding of the effects of habitat modification on species is limited. We investigated the diet of a forest-dwelling frog species, Morafka’s frog (Odorrana morafkai), in a highland forest in Vietnam in relation to habitat disturbance, sex and season. We surveyed the species at 45 sites in forest of varying disturbance and examined its diet using stomach flushing, estimating prey availability via trapping. We detected significantly fewer O. morafkai in highly disturbed habitats compared to moderately disturbed or non-disturbed habitats. We revealed that O. morafkai is a dietary generalist, identifying 28 prey types, primarily invertebrates. Prey composition, the number of prey items per stomach and prey volume per stomach did not vary between disturbance levels. Diet did not vary significantly between sexes, except that females had a higher prey volume. Prey composition in the species varied between seasons, with Coleoptera and Orthoptera dominating the diet in the rainy season and Lepidoptera in the dry season. The number of prey items per stomach and prey volume were significantly higher in the rainy season. There was a significant correlation between prey availability and diet composition. The low number of O. morafkai detected in highly disturbed habitats suggests that this habitat may not be optimal for the species, despite having a generalist feeding strategy and presumed high mobility. This study provides a window into the impact of an increasing threat, habitat disturbance, on forest-dependent amphibian species.
Deforestation, mostly driven by cash-crop plantations and logging (FAO, 2010), is occurring at a remarkable rate, with 11% of natural forests lost in tropical countries between 1990 and 2015 (FAO, 2015; Keenan et al., 2015). This worldwide reduction and degradation of natural forests is one of the major drivers of global biodiversity declines. Most forest-dependent species are unable to persist in highly modified environments (Hamer and McDonnell, 2008; Metzger et al., 2009). Despite this, there is very little specific information on what drives these declines and what characteristics render some species more susceptible to habitat modification than others.
Amphibians are amongst the most threatened taxa on earth, with 40% of all species threatened with extinction (IUCN, 2019). One of the biggest threats facing amphibians is deforestation. In 86% of threatened species, deforestation, caused by annual and perennial non-timber crops, wood and pulp plantations, livestock farming and ranching, and logging and wood harvesting, is understood as a threat (IUCN, 2019). Deforestation results in the creation of large canopy gaps, fewer large trees, less flowing water and edge effects that may lead to a reduced number of microhabitats available for amphibians (Inger and Colwell, 1977; Saunders, Hobbs and Margules, 1991; Donnelly and Crump, 1998; Vallan, 2002).
The global decline of amphibians has serious ecosystem-level consequences (Ranvestel et al., 2004; Whiles et al., 2006). Amphibians are a critical component of most ecosystems, in part because of their complex life cycle, with a typically aquatic larval life stage and terrestrial adult (Gascon et al., 2005). As a result of this biphasic life-cycle, amphibians provide an energetic link between terrestrial and aquatic habitats, helping ensure that energy flows from primary consumers to higher trophic levels (Burton and Likens, 1975; Duellman and Trueb, 1994; Wells, 2007). Despite this, basic information about the requirements of amphibians, including their microhabitat use and diet, is lacking for most species.
In order to further understand the role of amphibians in ecosystems, predict impacts of amphibian population declines and inform conservation management of this highly threatened group of animals, a better understanding of the dietary patterns of amphibian species is needed (Toft, 1980; Hirai and Matsui, 1999; Ranvestel et al., 2004). From the limited amount of information we have, we know that amphibians are typically opportunistic, generalist predators of invertebrates (Duellman and Trueb, 1994). However, some species in families Bufonidae, Leptodactylidae and Microhylidae were determined to be ant specialists (Toft, 1980; Hirai and Matsui, 2000b; Santos, Almeida and Vasconcelos, 2004). The origin of their food may be terrestrial (Hirai and Matsui, 2000a; Aszalós et al., 2006; Szeibel et al., 2008; Caldart et al., 2012) or aquatic habitats (Measey, 1998; Covaciu-Marcov et al., 2005; Tomescu et al., 2010; Ngo, Lee and Ngo, 2014), and depends on the life history and habitat use of each amphibian species (Duellman and Trueb, 1994). Different species of amphibians vary in their feeding intensity, average prey number and dominant prey type, due primarily to differences in their microhabitat use, mobility, foraging mode and body size (Duellman and Trueb, 1994; Aszalós et al., 2006; Wells, 2007).
Despite the increasing number of publications on amphibian diets, dietary information is not available for the vast majority of amphibian taxa (Solé and Rödder, 2010). There is almost no data on how the diet of amphibian species changes with habitat disturbance. This is particularly true in some of the most diverse and poorly-known amphibian communities.
Vietnam is home to a highly diverse and endemic amphibian fauna that is under great threat mostly due to habitat loss (Nguyen, Ho and Nguyen, 2009; Rowley et al., 2010). However, the dietary habits of amphibian species in the country have received very little attention (but see Ngo, Lee and Ngo, 2014; Ngo, Hoang and Ngo, 2014; Le et al., 2018). Of the 264 species of frog known from Vietnam (Frost, 2018), more than 75% are considered to be forest-dependent (IUCN, 2019) and are therefore under great threat from rapid deforestation (Rowley et al., 2010). A better understanding of the diet of such species may shed light on the reasons behind their dependence on forest, and how their declines may affect ecosystems.
Morafka’s frog, Odorrana morafkai (Bain et al., 2003), is a stream-breeding, forest-dwelling species known from Cambodia, Laos and Vietnam (Bain et al., 2003; Bain and Stuart, 2006; Stuart, Sok and Neang, 2006; Nguyen, Ho and Nguyen, 2009). The species is highly sexually dimorphic, with males up to 4.6 cm and females to 10.3 cm body size (Bain et al., 2003; Bain and Stuart, 2006). Although currently widespread and relatively abundant at specific, forested sites, habitat loss and harvesting for food are likely to be resulting in population declines in the species (IUCN, 2018).
Odorrana morafkai is an easily detectable frog species that occurs in both primary forests and adjacent disturbed areas in the central highlands of Vietnam (Teynié et al., 2004; IUCN, 2018). Forests in this region have diverse and highly endemic amphibian communities (Nguyen and Kuznetsov, 2009; Bain and Hurley, 2011) that are under increasing threat from human activities including the expansion of cash crops, and the construction of roads, houses and associated infrastructure. In this study, we investigate the dietary patterns of O. morafkai in a montane forest in southern Vietnam undergoing habitat modification and analyze the effect of habitat disturbance on the dietary patterns of the species over two seasons.
Materials and methods
Bidoup-Nui Ba National Park (NP), established in 2004, is in the southern Truong Son mountain range in Lam Dong Province, Vietnam (fig. 1). The NP has a total area of 64 800 ha and ranges in altitude from 700 m to 2200 m above sea level. Bidoup-Nui Ba NP has a subtropical climate, with an average annual temperature of 18°C and average annual rainfall of 1870 mm per year (Nguyen and Kuznetsov, 2009). There are two seasons: the rainy season from April to October and the dry season from November to March (Nguyen and Kuznetsov, 2009). The average daily relative humidity is high (84%) and varies little throughout the year (Nguyen and Kuznetsov, 2009).
We sampled amphibians in both the dry (January 2015 and 2016) and rainy (June 2015 and 2016) seasons at a total of 45 stream sites (fig. 1). These sites belonged to one of three habitat categories: relatively non-disturbed sites, moderately disturbed sites and highly disturbed sites (15 per category). Stream sites were considered non-disturbed if their banks (from the stream edge to 50 m from the stream) had native forest with canopy cover of >75%, the distance to the nearest agricultural land use (e.g., fish farms and coffee plantations) was more than 500 m, there was no evidence of other human activities (e.g. bathing and washing) within 200 m from the stream, no obvious upstream hydrologic alterations (e.g., dredging or diversions) and there was a low frequency of human visitation (no obvious trails). Stream sites were considered moderately disturbed if their banks had a native forest canopy cover of 50-75%, the distance to the nearest agricultural land use was 200 to 500 m, obvious upstream hydrologic alterations and there was a high frequency of human visitation (visible trails). Stream sites were considered highly disturbed if their banks (from the stream edge to 50 m from the stream) had native forest with <50% canopy cover, agricultural or urban land use within 200 m, and had obvious upstream hydrologic alterations (e.g., dredging or diversions) and evidence of human activity (i.e., trails, houses). Study sites were at 1000-1555 m elevation. All streams were part of the Da Nhim and Krong No river systems, were about 2-4 m wide, had a permanent flow and a substrate of sand, gravel, boulders and bed rock. The distance between each study site was at least 500 m.
At each site, we conducted nocturnal visual encounter surveys along 200 m of stream and along two 50 m-long forest transects perpendicular to the stream body, for a total of 45 stream transects and 90 forest transects. For all O. morafkai encountered (except individuals with a snout-vent length (SVL) < 30 mm), we recorded sex, SVL and body mass. Sex was determined by the presence or absence of nuptial pads or/and vocal sacs and by body size (as adult females are much larger than adult males). We recorded SVL to 0.1 mm using digital calipers and measured weight using Pesola scales to the nearest 0.1 g. We used stomach flushing to obtain the stomach contents of frogs without sacrificing frogs (Griffiths, 1986; Leclerc and Courtois, 1993; Solé et al., 2005). For small frogs (<60 mm SVL), we used 2 mm inner diameter, soft catheter tubes and a 60 ml syringe, and for large frogs (⩾60 mm), we used 3 mm inner diameter, soft catheter tubes and a 120 ml syringe. After flushing, we released frogs at the place of capture and transferred stomach contents to 80% ethanol. We estimated prey availability using light traps (for flying insects) and pitfall traps (for cursorial invertebrates). Each light trap consisted a strip of 100 12 V light-emitting diodes glued around a 0.5 × 0.3 × 0.1 m plastic tray. Pitfall traps were 15 cm high plastic buckets with a diameter at the mouth of 9 cm which we set up along each forest transect (see detail in Le et al., 2018).
We preserved all prey specimens collected via both stomach flushing and environmental trapping in 80% ethanol and identified them to order level except for Hymenoptera, which were classified into Formicidae and others. We used a stereomicroscope (Olympus SZ61) and reference keys to identify specimens (Ross, Ross and Ross, 1982; Borror, Triplehorn and Johnson, 1989) and measured the maximum length (L) and width (W) of each prey item to the nearest 0.1 mm using calipers.
To determine if there was a difference in the number of captured O. morafkai individuals between habitat disturbance categories, we used a general linear model with a post-hoc Tukey test, with sex and season as cofactors. To determine whether the prey composition of O. morafkai was reliably assessed, we used a Jackknife formula to estimate the prey richness (Krebs, 1999) and Primer v6 software to create the species cumulative curve of number of prey taxa from individuals sampled.
We calculated the frequency of occurrence and the numerical proportion of each prey category. We determined the frequency of occurrence (F) of each prey category by dividing the number of stomachs with prey belonging to taxonomic group X by the total number of stomachs with food. We estimated the numeric proportion (N) of each prey taxon as the number of preys belonging to taxon X divided by the total number of all prey taxa.
We estimated the volume of each prey item using a formula for an ellipsoid:and calculated the relative percent volume of each prey taxon. We used the relative importance index to determine the overall importance of each prey taxon in the diet (Biavati, Wiederhecker and Guarino, 2004), where I = (F + N + V)/3.
We used the Shannon-Wiener index to estimate the diversity of the diet of O. morafkai for each season and each sex category with the formula:
Since the number of frogs captured in highly disturbed sites was low (
To compare the overall diet composition between season, sex and level of habitat disturbance, we used PRIMER v 6 (Clarke and Gorley, 2006). We used the Bray-Curtis similarity measure to calculate association matrices before ordination using Nonmetric multi-dimensional scaling (NMDS). Following NMDS, we used ANOSIM to detect differences between groups, then SIMPER analysis to identify taxa contributing to average dissimilarity in diet between season, sex and habitat.
There was a significant effect of habitat disturbance on the number of frogs detected (General linear model,
Females had a larger snout vent length (
Of the 255 O. morafkai detected during the study, 239 (94%) had food in their stomachs. In total, we identified 654 prey items in the stomachs of O. morafkai and classified them into 27 prey taxonomic groups (table 1). Jackknife estimates suggested that more than 90% of prey composition was assessed (supplementary figure S1), indicating that a representative sample of the diet had been obtained. Insects dominated in the diet, both in terms of frequency of occurrence (90.2%) and in terms of number of items (90.7%) (table 1). The most important prey taxon was Coleoptera (beetles). According to the method of Amundsen, Gabler and Staldvik (1996), Odorana morafkai showed a generalized feeding strategy, as no prey type had both a frequency of occurrence and numeric proportion greater than 50%. Both aquatic and terrestrial prey were consumed by the species (table 1).
Diet: seasonal variation
The number of prey items per stomach and the prey volume per stomach differed significantly between seasons (table 2, figs. 3C, E). There was no season-habitat disturbance or season-sex interaction (table 2).
The dietary composition of O. morafkai in the rainy season was more diverse (178 frogs, with 28 prey types, Shannon-Wiener index:
Diet: differences between sex
The number of prey items per stomach in female O. morafkai was significantly higher than in males (table 2, fig. 3D). Prey length was an average of 15.6 ± 1.49 mm SD and 11.2 ± 1.48 mm SD in females and males respectively. There was a significant difference in the volume of prey in the stomachs of males and females (table 2, fig. 3F); there was no sex-season interaction (table 2). There was no difference in the diet composition between sexes (ANOSIM,
Diet: effect of habitat disturbance
There was an interaction between the effect of habitat disturbance and sex on the number of prey items per stomach (table 2). The number of prey items per stomach in females at non-disturbed sites was significantly less than at disturbed sites (Mann-Whitney U test,
There was no difference in the dietary composition of O. morafkai between non-disturbed sites and disturbed sites (ANOSIM,
In total, we collected 22 invertebrate taxa in the light and pitfall traps (supplementary table S2). Seven prey taxa (Chilopoda, Decapoda, Mantodae, Odonata, Phasmatodea, Squamata, and Thysanoptera) were identified from stomachs but were not detected in surrounding habitats. The prey diversity in the environment in the rainy season was similar to that in the dry season (Shannon-Wiener index:
There was no difference in the overall prey abundance (ANOVA,
The diet of O. morafkai is one of the most diverse diets reported to date for a tropical frog species (e.g., Stewart and Woolbright, 1996; Hirai and Matsui, 2000a; Biavati, Wiederhecker and Guarino, 2004; Wachlevski et al., 2008; Leavitt and Fitzgerald, 2009; Quiroga, Sanabria and Acosta, 2009; Caldart et al., 2012; Brito et al., 2013; Ngo, Lee and Ngo, 2014; Pamintuan and Starr, 2016). The variety of prey consumed by O. morafkai is likely related to the broad habitat use of the species (Inger, Orlov and Darevsky, 1999; Bain et al., 2003; Stuart, Sok and Neang, 2006; Bain, Nguyen and Doan, 2007), as it forages in both aquatic and terrestrial microhabitats. Among the 28 groups of prey identified, a single group, Coleoptera provided the greatest contribution to the diet. This pattern is not surprising since tropical frog species have often been identified consuming Coleoptera (Stewart and Woolbright, 1996; Hirai and Matsui, 2000a; Biavati, Wiederhecker and Guarino, 2004; Wachlevski et al., 2008; Leavitt and Fitzgerald, 2009; Quiroga, Sanabria and Acosta, 2009; Caldart et al., 2012; Brito et al., 2013; Ngo, Lee and Ngo, 2014; Pamintuan and Starr, 2016). A single vertebrate prey (a lizard), found in the stomach of a female O. morafkai could be considered as a rare prey group in this species. Vertebrate prey has been reported in only a few frog species in Southeast Asia (e.g., Inger and Greenberg, 1966; Kueh et al., 2010).
The dietary pattern of O. morafkai varied significantly with season, with a higher diversity of prey taxa consumed in the rainy season. As we did not detect any differences in prey abundance or diversity in the environment between seasons, the higher diversity of prey taxa consumed by O. morafkai in the rainy season is likely due to frogs being able to access more habitat types in the rainy season. In contrast, in the dry season, frogs are likely to concentrate around water bodies (Duellman and Trueb, 1994; Rowley and Alford, 2007; Wells, 2007). Indeed, in this study we often observed O. morafkai on forest transects, far away from streams in the rainy season (Le, pers. obs.). The seasonal variation in their diet composition could be explained through the significant correlation between prey availability and prey composition detected. This seasonal relationship between prey availability and diet composition has been also reported in previous studies (e.g., Stewart and Sandison, 1972; Forstner, Forstner and Dixon, 1998; Hirai and Matsui, 1999).
We detected a significant difference between sexes in the volume of prey, with female O. morafkai having greater prey volume. This is consistent with the size-efficiency hypothesis (Forsman, 1996), as females have a higher body size and higher stomach capacity, thereby are able to consume larger prey items than males. We found no difference in the dietary composition of male versus female O. morafkai. This pattern has been reported in other frog species with generalized feeding strategies (Measey, 1998; Hirai and Matsui, 2001; Biavati, Wiederhecker and Guarino, 2004; Yu et al., 2009; Pamintuan and Starr, 2016). The similarity in prey numbers and prey composition between sexes in this species may also be due to both sexes using the same microhabitats, as they were frequently detected in the same microhabitats during our surveys, unlike many species which have sexual dimorphism in microhabitat use (Regosin, Windmiller and Reed, 2003; Fellers and Kleeman, 2007; Rowley and Alford, 2007).
In this study, we did not detect an impact of habitat disturbance on the diet of O. morafkai. This is likely because prey availability did not differ significantly between non-disturbed sites and disturbed sites. Moreover, generalist species may be less susceptible to fluctuation in trophic resources compared to specialist species (William et al., 2006). However, we suggest caution when interpreting these results for two reasons: (1) the number of frogs detected in highly disturbed sites was too low to be included in statistical analysis, and data from these frogs were merged with that from detected in moderately disturbed habitats, and (2) environmental sampling at disturbed sites is likely to have been more successful as they were more open, increasing the likelihood of trapping invertebrates (Bowden, 1982; Muierhead-Thompson, 2012).
Despite the lack of a detectable impact of habitat disturbance on the diet of O. morafkai, the number of O. morafkai detected in highly disturbed sites was significantly smaller than in non-disturbed sites. Forest disturbance frequently results in changing microhabitats and microclimates (Vallan, 2002; Riley et al., 2005; Urbina-Cardona, Olivares-Pérez and Reynoso, 2006; Hillers, Veith and Rödel, 2008). Further studies on changes in habitat parameters under habitat disturbance, as well as the effects of habitat disturbance on breeding success, and the growth and survival of larval, juvenile and adult O. morafkai need to be conducted to understand the impact of habitat disturbance on this and other species.
In addition to providing a greater understanding of how an amphibian species responds to habitat disturbance, our findings provide the first information on the diet of O. morafkai, and amongst the first for any amphibian species in Vietnam. Trophic studies of frogs in disturbed areas are still scarce and in the context of global amphibian declines, research on the effects of habitat changes on feeding and life history of amphibian species should be considered a priority in developing conservation strategies.
Field work was supported by grants from the University of Science, Ho Chi Minh City; the Partnerships for Enhanced Engagement in Research (PEER) Science program (PGA-2000003583), a partnership between the U.S. Agency for International Development (USAID) and the National Science Foundation. Our research followed the Guidelines for the use of Amphibians and Reptiles in Field and Laboratory Research. Staff at Bidoup-Nui Ba National Park kindly facilitated surveys (permit number 807/KHTN-KH). Ta, V.T., Tran, T.C.L., Dang, H.S., Nguyen, P.T., Phan, X.T., Vo, N.T., and Huynh, K.T assisted in the field and Cutajar, T created the map.
Supplementary material is available online at: https://doi.org/10.6084/m9.figshare.9414917
Amundsen, P.A., Gabler, H.M., Staldvik, F.J. (1996): A new approach to graphical analysis of feeding strategy from stomach contents data-modification of the Costello (1990) method. J. Fish. Biol. 48: 607-614.
Aszalós, L., Bogdan, H., Kovács, E.H., Peter, V.I. (2006): Food composition of two Rana species on a forest habitat (Livada Plain, Romania). North-West. J. Zool. 1: 25-30.
Bain, R.H., Lathrop, A., Murphy, R.W., Orlov, N.L., Ho, C.T. (2003): Cryptic species of a cascade frog from Southeast Asia: taxonomic revisions and descriptions of six new species. Am. Mus. Novit. 3417: 1-60.
Bain, R.H., Stuart, B.L. (2006): A new species of cascade frog (Amphibia: Ranidae) from Thailand, with new data on Rana banaorum and Rana morafkai. Nat. Hist. Bull. Siam. Soc. 53: 3-16.
Bain, R.H., Hurley, M.M. (2011): A biogeographic synthesis of the amphibians and reptiles of Indochina. Bull. Am. Mus. Nat. Hist. 360: 1-138.
Biavati, G.M., Wiederhecker, H.C., Guarino, R.C. (2004): Diet of Epipedobates flavopictus (Anura:Dendrobatidae) in a neotropical savanna. J. Herpetol. 38: 510-518.
Brito, L., Aguiar, F., Moura-Neto, C., Zuco, A., Cascon, P. (2013): Diet, activity patterns, microhabitat use and defensive strategies of Rhinella hoogmoedi Caramaschi & Pombal, 2006 from a humid forest in northeast Brazil. Br. J. Herpetol. 23: 29-37.
Burton, T.M., Likens, G.E. (1975): Energy flow and nutrient cycling in salamander populations in the Hubbard Brook Experimental Forest, New Hampshire. Ecology. 56: 1068-1080.
Caldart, V.M., Iop, S., Bertaso, T.R.N., Cechin, S.Z. (2012): Feeding ecology of Crossodactylus schmidti (Anura: Hylodidae) in southern Brazil. Zool. Stud. 51: 484-493.
Covaciu-Marcov, S.D., Sas, I., Cupşa, D., Bogdan, H., Lukács, J. (2005): The seasonal variation of the food of a non-hibernated Rana ridibunda Pallas 1771 population from the thermal lake from 1 Mai Spa, Romania. An. Univ. Oradea. Fasc. Biol. 12: 77-85.
Donnelly, M.A., Crump, M.L. (1998): Potential effects of climate change on two Neotropical amphibian assemblages. Clim. Change. 2 (39): 541-561.
Fellers, G.M., Kleeman, P.M. (2007): California red-legged frog (Rana draytonii) movement and habitat use: implications for conservation. J. Herpetol. 41 (2): 276-287.
Forstner, J.M., Forstner, M.R.J., Dixon, J.R. (1998): Ontogenetic effects on prey selection and food habits of two sympatric east Texas ranids: the southern leopard frog, Rana sphenocephala, and the bronze frog, Rana clamitans clamitans. Herpetol. Rev. 29 (4): 208.
Frost, D.R. (2018): Amphibian Species of the World: an Online Reference. Version 6.0 (30 April 2018). Electronic Database accessible at: http://research.amnh.org/herpetology/amphibia/index.html. American Museum of Natural History, New York, USA.
Gascon, C., Collins, J.P., Moore, R.D., Church, D.R., McKay, J.R., Mendelson III (2005): Amphibian Conservation Action Plan: Proceedings IUCN/SSC Amphibian Conservation Summit 2005. IUCN, Gland.
Griffiths, R.A. (1986): Feeding niche overlap and food selection in smooth and palmate newts, Triturus vulgaris and T. helveticus, at a pond in mid-Wales. J. Animal. Ecol. 55 (1): 201-214.
Hamer, A.J., McDonnell, M.J. (2008): Amphibian ecology and conservation in the urbanising world: a review. Biol. Conserv. 141 (10): 2432-2449.
Hillers, A., Veith, M., Rödel, M.O. (2008): Effects of forest fragmentation and habitat degradation on West African leaf litter frogs. Conserv. Biol. 22 (3): 762-772.
Hirai, T., Matsui, M. (1999): Feeding habits of the pond frog, Rana nigromaculata, inhabiting rice fields in Kyoto, Japan. Copeia. 1999 (4): 940-947.
Hirai, T., Matsui, M. (2000a): Feeding habits of the Japanese tree frog, Hyla japonica, in the reproductive season. Zool. Sci. 17: 977-982.
Hirai, T., Matsui, M. (2000b): Ant specialization in diet of the narrow-mouthed toad, Microhyla ornata, from Amamioshima Island of the Ryukyu Archipelago. Curr. Herpetol. 19 (1): 27-34.
Hirai, T., Matsui, M. (2001): Diet composition of the Indian rice frog, Rana limnocharis, in rice fields of central Japan. Curr. Herpetol. 20 (2): 97-103.
Inger, R.F., Greenberg, B. (1966): Ecological and competitive relations among three species of frogs (genus Rana). Ecology. 47: 746-759.
Inger, R.F., Colwell, R.K. (1977): Organization of contiguous communities of amphibians and reptiles in Thailand. Ecol. Monogr. 47 (3): 229-253.
IUCN (2018): The IUCN Red List of Threatened Species. Version 2017-3. www.iucnredlist.org. Downloaded on 14 May 2018.
IUCN (2019): The IUCN Red List of Threatened Species. Version 2018-2. http://www.iucnredlist.org. Downloaded on 14 March 2019.
Keenan, R.J., Reams, G.A., Achard, F., de Freitas, J.V., Grainger, A., Lindquist, E. (2015): Dynamics of global forest area: results from the FAO global forest resources assessment 2015. Forest. Ecol. Manag. 352: 9-20.
Kueh, B.H., Albert, J., Ismail, N., Siwan, E.S., Lau, C.E., Ngidang, V.B., Koh, J.S. (2010): Limnonectec kuhlii (Kuhl’s Creek Frog): diet. Herpetol. Rev. 41: 338.
Le, T.T.D., Rowley, J.J.L., Tran, T.A.D., Vo, N.T., Hoang, D.H. (2018): Diet composition and overlap in a montane frog community in Vietnam. Herpetol. Conserv. Biol. 13 (1): 205-215.
Metzger, J.P., Martensen, A.C., Dixo, M., Bernacci, L.C., Ribeiro, M.C., Teixeira, A.M.G., Pardini, R. (2009): Time-lag in biological responses to landscape changes in a highly dynamic Atlantic forest region. Biol. Conserv. 142 (6): 1166-1177.
Ngo, V.B., Lee, Y.F., Ngo, C.D. (2014): Variation in dietary composition of granular spiny frogs (Quasipaa verrucospinosa) in central Vietnam. Br. J. Herpetol. 24: 245-253.
Ngo, V.B., Hoang, T.N., Ngo, C.D. (2014): Diet of the banna caecilian Ichthyophis bannanicus (Amphibia: Gymnophiona: Ichthyophiidae) in the Mekong Delta, Vietnam. J. Herpetol. 48 (4): 506-513.
Pamintuan, P.E., Starr, C.K. (2016): Diet of the giant toad, Bufo marinus (Amphibia: Salientia), in a coastal habitat of the Philippines. Trop. Agric. (Trinidad) 93: 323-327.
Quiroga, L., Sanabria, E.A., Acosta, J.C. (2009): Size- and sexdependent variation in diet of Rhinella arenarum (Anura: Bufonidae) in a wetland of San Juan, Argentina. J. Herpetol. 43: 311-317.
Ranvestel, A.W., Lips, K.R., Pringle, C.M., Whiles, M.R., Bixby, R.J. (2004): Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations. Freshwater. Biol. 49: 274-285.
Regosin, J.V., Windmiller, B.S., Reed, J.M. (2003): Terrestrial habitat use and winter densities of the wood frog (Rana sylvatica). J. Herpetol. 37 (2): 390-395.
Riley, S.P.D., Busteed, G.T., Kats, L.B., Vandergon, T.L., Lee, L.F.S., Dagit, R.G., Kerby, J.L., Fisher, R.N., Sauvajot, R.M. (2005): Effects of urbanization on the distribution and abundance of amphibians and invasive species in Southern California streams. Conserv. Biol. 9: 1894-1907.
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)| false ( , Riley, S.P.D. , Busteed, G.T. , Kats, L.B. , Vandergon, T.L. , Lee, L.F.S. , Dagit, R.G. , Kerby, J.L. , Fisher, R.N. Sauvajot, R.M. ): 2005 Effects of urbanization on the distribution and abundance of amphibians and invasive species in Southern California streams. 9: 1894- 1907.
Rowley, J.J., Alford, R.A. (2007): Movement patterns and habitat use of rainforest stream frogs in northern Queensland, Australia: implications for extinction vulnerability. Wildl. Res. 34 (5): 371-378.
Rowley, J.J.L., Brown, R., Bain, R., Kusrini, M., Inger, R., Stuart, B.L., Phimmachak, S. (2010): Impending conservation crisis for Southeast Asian amphibians. Biol. Lett. 6: 336-338.
Santos, E.M., Almeida, A.V., Vasconcelos, S.D. (2004): Feeding habits of six anuran (Amphibia: Anura) species in a rainforest fragment in Northeastern Brazil. Iheringia. Ser. Zoo. 94 (4): 433-438.
Saunders, D.A., Hobbs, R.J., Margules, C.R. (1991): Biological consequences of ecosystem fragmentation: a review. Conserv. Biol. 5 (1): 18-32.
Solé, M., Beckmann, O., Pelz, B., Kwet, A. (2005): Stomach-flushing for diet analysis in anurans: an improved protocol evaluated in a case study in Araucaria forests, southern Brazil. Stud. Neotrop. Fauna. E. 40: 23-28.
Solé, M., Rödder, D. (2010): Dietary assessments of adult amphibians. In: Amphibian Ecology and Conservation, p. 167-184. Kenneth Dood, C., Ed., Oxford University Press Inc., New York.
Stewart, M.M., Sandison, P. (1972): Comparative food habits of sympatric mink frogs, bullfrogs, and green frogs. J. Herpetol. 6 (3/4): 241-244.
Stewart, M.M., Woolbright, L.L. (1996): Amphibians. In: The Food web of a Tropical Rain Forest, p. 273-320. Reagan, D.P., Waide, R.B., Eds, The University of Chicago Press, Chicago.
Stuart, B.L., Sok, K., Neang, T. (2006): A collection of amphibians and reptiles from hilly eastern Cambodia. Raffles. B. Zool. 54 (1): 129-155.
Szeibel, B., Citrea, L., Jurj, N., Condure, N. (2008): Feeding ecology of the Pelophylax ridibundus (Anura, Ranidae) in Dobromir, Romania. Biharean. Biol. 2: 27-37.
Teynié, A., David, P., Ohler, A., Luanglath, K. (2004): Notes on a collection of amphibians and reptiles from southern Laos, with a discussion of the occurrence of Indo-Malayan species. Hamadryad. 29: 33-62.
Toft, C.A. (1980): Seasonal variation in populations of Panamanian litter frogs and their prey: a comparison of wetter and drier sites. Oecologia. 47 (1): 34-38.
Tomescu, N., Ferenti, S., Covaciu-Marcov, S.D., Sas, I., David, A. (2010): What do the terrestrial isopods eaten by some frogs from north-western Romania have to say?. North-West. J. Zool. 6 (2): 268-274.
Urbina-Cardona, J.N., Olivares-Pérez, M., Reynoso, V.H. (2006): Herpetofauna diversity and microenvironment correlates across a pasture–edge–interior ecotone in tropical rainforest fragments in the Los Tuxtlas Biosphere Reserve of Veracruz, Mexico. Biol. Conserv. 132 (1): 61-75.
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)| false ( , Urbina-Cardona, J.N. , Olivares-Pérez, M. Reynoso, V.H. ): 2006 Herpetofauna diversity and microenvironment correlates across a pasture–edge–interior ecotone in tropical rainforest fragments in the Los Tuxtlas Biosphere Reserve of Veracruz, Mexico. 132( 1): 61- 75.
Vallan, D. (2002): Effects of anthropogenic environmental changes on amphibian diversity in the rain forests of eastern Madagascar. J. Trop. Ecol. 18 (5): 725-742.
Wachlevski, M., De Souza, P.H.C., Kopp, K., Eterovick, P.C. (2008): Microhabitat use and feeding habits of Crossodactylus bokermanni Caramaschi and Sazima, 1985 (Anura: Hylodidae) at a site in south-eastern Brazil. J. Nat. Hist. 42: 1421-1434.
Whiles, M.R., Lips, K.R., Pringle, C.M., Kilham, S.S., Bixby, R.J., Brenes, R., Scott, C., Jose, C.C., Meshagae, H., Alexander, D.H., Chad, M., Scot, P. (2006): The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Front. Ecol. Environ. 4 (1): 27-34.
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)| false ( , Whiles, M.R. , Lips, K.R. , Pringle, C.M. , Kilham, S.S. , Bixby, R.J. , Brenes, R. , Scott, C. , Jose, C.C. , Meshagae, H. , Alexander, D.H. , Chad, M. Scot, P. ): 2006 The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. 4( 1): 27- 34.
Williams, Y.M., Williams, S.E., Alford, R.A., Waycott, M., Johnson, C.N. (2006): Niche breadth and geographical range: ecological compensation for geographical rarity in rainforest frogs. Biol. Lett. 2 (4): 532-535.
Yu, T.L., Gu, Y.S., Du, J., Lu, X. (2009): Seasonal variation and ontogenetic change in the diet of a population of Bufo gargarizans from the farmland, Sichuan, China. Biharean. Biol. 3 (2): 99-104.
Associate Editor: Raffael Ernst.