Abstracts
In this study we analyzed diet composition, niche breadth and overlap of the two leaf-litter frogs Ischnocnema henselii and Adenomera marmorata. Frogs were collected in an Atlantic Rainforest area in the Reserva Natural Salto Morato, in Paraná State, Southern Brazil, using plots of 16 m2 established on forest floor. Ischnocnema henselii consumed 18 different types of prey and the diet of this species was composed predominantly by Hymenoptera (Formicidae) (15.4%), Araneae (13.83%), Orthoptera (6.15%) and Opiliones (6.15%), whereas Adenomera marmorata consumed 15 different types of prey and its diet was composed mainly by Hymenoptera (Formicidae) (45.7%), Acari (31.8%) and Blattodea (14.8%). The niche breadth of I. henselii was BA = 0.43 and that of A. marmorata was BA = 0.19. The diet of the two sympatric species of leaf-litter frogs was basically composed by arthropods and the trophic niche overlap among them did not differ from expected at random. The differences in prey consumption should potentially facilitate the coexistence of two sympatric frogs on the forest floor. Possibly, this difference of prey consumption partly reflects differences in jaw width, species-specific body size of the two species and the period of activity of these two species.
Anura; syntopy; species coexistence; Atlantic Rainforest
Neste estudo analisamos a composição da dieta e a amplitude e sobreposição do nicho trófico dos anuros de folhiço Ischnocnema henselii e Adenomera marmorata. Os anuros foram coletados em uma área de Mata Atlântica na Reserva Natural Salto Morato, no Estado do Paraná, Sul do Brasil, utilizando o método de parcelas de 16 m2 estabelecidas no chão da floresta. Ischnocnema henselii consumiu 18 diferentes tipos de presa e a dieta desta espécie foi composta predominantemente por Hymenoptera (Formicidae) (15,4%), Araneae (13,83%), Orthoptera (6,15%) e Opiliones (6,15%), enquanto Adenomera marmorata consumiu 15 diferentes tipos de presas e sua dieta foi composta principalmente por Hymenoptera (Formicidae) (45,7%), Acari (31,8%) e Blattodea (14,8%). A amplitude de nicho de I. henselii foi BA = 0,43 e de A.marmorata foi BA = 0,19. A dieta das duas espécies de anuros simpátricos do folhiço por nós estudadas foi composta basicamente de artrópodes e a sobreposição de nicho trófico entre elas não diferiu do esperado para ocorrer ao acaso. As diferenças no consumo de presas potencialmente devem facilitar a coexistência desses dois anuros simpátricos no chão da floresta. Possivelmente, esta diferença no consumo de presas em parte reflete diferenças na largura da mandíbula, no tamanho do corpo e no período de atividade dessas duas espécies.
Anura; sintopia; coexistência de espécies; Mata Atlântica
1 Introduction
The coexistence of similar species within a community implies in temporal and spatial
overlap between these species. This coexistence could not occur if two or more
species compete for a single limiting resource (“Competitive Exclusion Principle”;
Hardin, 1960Hardin, G., 1960. The competitive exclusion principle. Science, vol.
131, no. 3409, p. 1292-1297. http://dx.doi.org/10.1126/science.131.3409.1292.
PMid:14399717
http://dx.doi.org/10.1126/science.131.34...
). Therefore, ecological
differences, or niche differences, are necessary to allow coexistence among species.
Despite niche are known to contain several dimensions, its main dimensions are daily
activity (time), microhabitat use (space) and food resources (diet) (Pianka, 1994Pianka, ER., 1994. Evolutionary ecology. 5th ed.
New York: Harper Collins College Publishers. 486 p.).
Food is a crucial resource for animals and its partitioning among sympatric and
syntopic species is an important tool to understand interactions among locally
coexisting species (Schoener, 1974Schoener, TW., 1974. Resource partitioning in ecological
communities. Science, vol. 185, no. 4145, p. 27-39.
http://dx.doi.org/10.1126/science.185.4145.27. PMid:17779277
http://dx.doi.org/10.1126/science.185.41...
; Taper and Marquet, 1996Taper, ML. and Marquet, PA., 1996. How do species really divide
resources? American Naturalist, vol. 147, no. 6, p. 1072-1082.
http://dx.doi.org/10.1086/285893.
http://dx.doi.org/10.1086/285893...
; Sih and Christensen, 2001SIh, A. and Christensen, B., 2001. Optimal diet theory: when does it
work, and when and why does it fail? Animal Behaviour, vol. 61, no. 2, p.
379-390. http://dx.doi.org/10.1006/anbe.2000.1592.
http://dx.doi.org/10.1006/anbe.2000.1592...
). Trophic niche overlap occurs when
two species share similar food resource when exploiting the habitat. However, in
nature, usually only a partial overlap tend to occur where some resources are shared
and other are used exclusively by each one of the species (Pianka, 1994Pianka, ER., 1994. Evolutionary ecology. 5th ed.
New York: Harper Collins College Publishers. 486 p.). Therefore, sympatric species do not necessarily
feed on the same items due to the differences in their evolutionary history
(phylogenetic affinities), patterns of microhabitat use (Van Sluys and Rocha, 1998Van Sluys, M. and Rocha, CFD., 1998. Feeding habitats and
microhabitat utilization by two syntopic Brazilian Amazonian frogs (Hyla
minuta and (gr. . Pseudo paludicula
spfalcipes). Revista Brasileira de
Biologia =Brazilian Journal of Biology, vol. 58, no. 4, p.
559-562.), intrinsic ecological aspects (e.g.
ecophysiology), body size (Sabagh et
al.,2010Sabagh, LT., Ferreira, VL. and Rocha, CFD., 2010. Living together,
sometimes feeding in a similar way: the case of the syntopic hylid frogs
Hypsiboas raniceps and Scinax acuminatus (Anura: Hylidae) in the Pantanal of
Miranda, Mato Grosso do Sul State, Brazil. Brazilian journal of biology =
Revista brasileira de biologia, vol. 70, no. 4, p. 955-959.
http://dx.doi.org/10.1590/S1519-69842010000500006.
PMid:21180899
http://dx.doi.org/10.1590/S1519-69842010...
) which, as result, may lead to the consumption of prey of
different sizes, types and also to forage at different periods (Menin et al., 2005Menin, M., ROSSA-FERES, DC. and GIARETTA, AA., 2005. Resource use
and coexistence of two syntopic hylid frogs (Anura, Hylidae). Revista Brasileira
de Zoologia, vol. 22, no. 1, p. 61-72.
http://dx.doi.org/10.1590/S0101-81752005000100008.
http://dx.doi.org/10.1590/S0101-81752005...
).
Ischnocnema henselii (Peters, 1870) (Brachycephalidae) and
Adenomera marmorata (Steindachner, 1867) (Leptodactylidae) are
endemic to the Brazilian Atlantic Rainforest biome, occurring in sympatry in various
parts of this biome (Frost, 2013Frost, DR., 2013. Amphibian Species of the World: an Online
Reference. New York: American Museum of Natural History.
Available from:
<http://research.amnh.org/herpetology/amphibia/index.html>. Access in: 9
Jan. 2013.). The two
species sharing nocturnal activity (whilst A. marmorata is also
active in daylight period), being I. henselii slightly larger than
A. marmorata in body size (Haddad et al., 2013Haddad, CFB., Toledo, LF., Prado, CPA., Loebmann, D., Gasparini, JL.
and Sazima, I., 2013. Guia dos Anfíbios da Mata Atlântica: diversidade e
biologia = Guide to the amphibians of the Atlantic Forest: diversity and
biology. São Paulo: Anolisbooks. 544 p.). In Paraná State, Southern Brazil, these two leaf
litter frogs are usually the most abundant species and occur syntopically on the
forest floor of the Atlantic Rainforest of Reserva Natural Salto Morato (Santos-Pereira et al., 2011Santos-Pereira, M., Candaten, A., Milani, D., Oliveira, FB.,
Gardelin, J. and Rocha, CFD., 2011. Seasonal Variation in the Leaf-Litter Frog
Community (Amphibia: Anura) from an Atlantic Forest Area in Salto Morato Natural
Reserve, Southern Brazil. Zoologia, vol. 28, no. 6, p. 755-761.
http://dx.doi.org/10.1590/S1984-46702011000600008.
http://dx.doi.org/10.1590/S1984-46702011...
).
In this study, we analyzed the diet aspects, niche breadth, and niche overlap of Ischnocnema henselii and Adenomera marmorata, specifically aiming to answer the following questions: 1) What is the composition of the diet and food niche breadth of the two studied species? 2) To what extent does the width of the frog jaw explain the size of prey ingested? 3) How the sympatric frogs species differ in body size? 4) In which extent do the syntopic frogs overlap in their trophic niche?
2 Material and Methods
Frogs were collected between January and April 2010 in an Atlantic Rainforest area in the Reserva Natural Salto Morato (25° 09’ S; 48° 16’ to 48° 20’ W), in Paraná State, Southern Brazil. The reserve has an area of 2,252 ha, located in the Área de Preservação Ambiental de Guaraqueçaba, and it is part of the largest and continuous remnant of the Atlantic Rainforest in Brazil (Câmara, 2005Câmara, IG., 2005. Breve história da conservação da Mata Atlântica. In GALINDO-LEAL, C. and CÂMARA, IG. (Eds.). Mata Atlântica: Biodiversidade, ameaças e perspectivas. São Paulo: Fundação SOS Mata Atlântica; Belo Horizonte: Conservação Internacional. p. 31-42.). The mean annual temperature is 21°C and the mean annual relative humidity is 85%. The altitude varies between 25-930 m.a.s.l., and the rainfall is about 2,000 mm per year (FBPN, 2011Fundação Grupo Boticário de Proteção à Natureza – FBPN2011Plano de Manejo da Reserva Natural Salto Morato – Guaraqueçaba - PRCuritibaFundação Grupo Boticário de Proteção à Natureza222p. vol1).
To sample the anurans species, we used Large-Plot sampling method (Jaeger and Inger, 1994Jaeger, RG. and Inger, RF., 1994. Quadrat sampling. In: HEYER, WR., DONNELLY, MA., MCDIARMID, RW., HAYEK, LC. and FOSTER, MS. (Eds.). Measuring and monitoring biological diversity: standard methods for amphibians. Washington: Smithsonian Institution Press. p. 97-102.). We established 88 plots of 16 m2 (4 × 4 m) on the forest floor, totaling 1,408 m2 of sampled area. Plots were arbitrarily established scattered along the forest floor at altitudes from 200 to 300 m.a.s.l. in an area of primary Atlantic Rainforest. We marked the corners of each plot with plastic stakes, and the area inside the plot was enclosed with a 50 cm high soft plastic fence. At night, each plot was carefully searched for about half an hour by a team of four persons using headlamps. The plots were established at least 100 meters away from each other, in order to avoid spatial pseudoreplication of data. Frogs were anesthetized with lidocaine, killed in 50% ethanol, fixed in 10% formalin and preserved in 70% ethanol.
Voucher specimens from this study were deposited at the scientific collection of the Museu Nacional do Rio de Janeiro under the following numbers (I. henselii: MNRJ 75394-75400 and MNRJ 75418-75438 and A. marmorata: MNRJ 75439-75460).
In the laboratory, individuals had the snout-vent length (SVL) and the jaw size (LM)
measured (both in mm) with a digital caliper (to the nearest 0.1 mm). Frogs were
dissected and their stomach contents were qualitatively and quantitatively analyzed.
Animal prey was identified under a dissecting stereoscopic microscope to the
taxonomic level of order, except in the case of ants (identified to Family),
molluscs, millipedes and centipedes, which were identified to Class (Triplehorn and Johnson, 2005Triplehorn, CA. and Johnson, NF., 2005. Borror and DeLong's
introduction to the study of insects. 7th ed. Belmont: Thomson
Brooks/Cole. 864 p.). For each food
item, we measured the length and the width using calipers (0.1 mm precision) and
prey volume (mm3) was estimated using the formula for an ovoid spheroid:
V = 4/3π (length/2) (width/2)2 (Dunham,
1983Dunham, AE., 1983. Realized niche overlap, resource abundance, and
intensity of interspecific competition. In HUEY, RB., PIANKA, ER. and SCHOENER,
TW. (Eds.). Lizard ecology: studies of a model organism.
Cambridge: Harvard University Press. p. 261-280.
http://dx.doi.org/10.4159/harvard.9780674183384.c15.
http://dx.doi.org/10.4159/harvard.978067...
). Unidentified remains of arthropods were grouped as ‘‘remains of
arthropods’’ and this category was considered only for volumetric analysis. The
frequency for each category of prey was expressed by the number of stomachs that
contained that category. An index of relative importance (Ix) was
calculated for each prey category, with the sum of the numeric, volumetric and
frequency of occurrence proportions divided by three (Powell et al., 1990Powell, R., Parmerlee, JS., Rice, MA. and Smith, DD., 1990.
Ecological observations on Hemidactylus brookihaitianus
Meerwarth (Sauria: Gekkonidae) from Hispaniola. Caribbean Journal of Science,
vol. 26, p. 67-70.).
We estimated the trophic niche breadth (based on the number of food items) using the
formula proposed by Levins (1968)Levins, R., 1968. Evolution in changing
environments. Princeton: Princeton University Press. 120
p.. The
values of niche breadth were standardized (BA) to the range of 0 to 1
using the appropriated formula. We calculated the niche overlap between the two
species (Ojk, based on the Ix) using the formula of
MacArthur and Levins (1967)Macarthur, R. and Levins, R., 1967. The limiting similarity,
convergence, and divergence of coexisting species. American Naturalist, vol.
101, no. 921, p. 377-385. http://dx.doi.org/10.1086/282505.
http://dx.doi.org/10.1086/282505...
modified by
Pianka (1973)Pianka, ER., 1973. The structure of lizard communities. Annual
Review of Ecology and Systematics, vol. 4, no. 1, p. 53-74.
http://dx.doi.org/10.1146/annurev.es.04.110173.000413.
http://dx.doi.org/10.1146/annurev.es.04....
. This index value varies
from 0 (total partitioning) to 1 (total overlap). We tested if the probability of
trophic niche overlap would be the same if data would be randomly distributed using
null models (with 10.000 iterations or pseudo-communities), with the software EcoSim
(Gotelli and Entsminger, 2006Gotelli, NJ. and Entsminger, GL., 2006. EcoSim: null models software
for ecology. Jericho: Acquired Intelligence Inc. and
Kesey-Bear.). For the
analysis we utilized a matrix containing the importance index (Ix)
of each category of species's prey. We used the algorithm of randomization number
three (RA3), that consider each species resource, effectively retaining the niche
breadth of species (Gotelli and Graves,
1996Gotelli, NJ. and Graves, GR., 1996. Null models in
Ecology. Washington: Smithsonian Institute. 368
p.). Differences among frog species in body size (SVL) were evaluated using
a T-test (Zar, 1999Zar, JH., 1999. Biostatistical Analysis. 4th ed.
Upper Saddle River: Prentice Hall. 663 p.). We performed a simple
linear regression between prey size (based on the volume of the largest prey) and
jaw width to evaluate in which extent jaw width of individuals influenced the size
of consumed prey.
3 Results
From the 88 plots sampled, Ischnocnema henselii and Adenomera marmorata occurred in 36 of them, but they co-occurred in only five plots (14%). In the summer the two frog species occurred in 28 plots whereas in the autumn they occurred in eight plots. All of the plots that the two species occurred together were sampled in the summer.
Ischnocnema henselii (n = 28) consumed 18 different prey types and 7.1% of sampled individuals had empty stomachs (n = 2). Formicidae (Hymenoptera) (15.4%) was the dominant item in the diet of I. henselii in terms of number, followed by Araneae (13.8%) and Opiliones and Orthoptera (both with 6.2%). In terms of volume, Orthoptera (14.3%) dominated, followed by Blattodea (6.5%) and Formicidae (3.0%). Araneae was the most frequent item (25%), followed by Formicidae (21.4%), and Orthoptera and Opiliones (both with 14.3%). Based on the index of importance (Ix), Araneae (12.3%), Formicidae (12.1%) and Orthoptera (11.1%) were the most representative items in the diet of I. henselii (Table 1).
Number (N), Volume (V, in mm3), Frequency (F) and Importance index (Ix) of the different prey types in the diet of Ischnocnema henselii (n = 28) and Adenomera marmorata (n = 22) at RPPN Salto Morato, Southern Brazil. (URA) Unidentified remains of arthropods.
Adenomera marmorata (n = 22) consumed 15 different types of prey items and all frogs had some content in their stomach. Formicidae (45.7%) was the dominant item by number, followed by Acari (31.5%) and Diplopoda (5.4%). Blattodea represented 19.1% of total volume intake, followed by Formicidae (8.7%) and Isopoda (4.6%). Formicidae was also the more frequent item (86.4%), followed by Acari (59.1%) and Hymenoptera and Blattodea, both with 22.7%. According to the index of importance (Ix), Formicidae (45.7%), Acari (31.08%) and Blattodea (14.8%) were the most representative preys with the other items being less frequent in the diet of A. marmorata (Table 1).
The prey items shared the two frog species were: Amphipoda, Araneae, Blattodea, Colembola, Coleoptera (adults), Diptera (adults), Formicidae, Isopoda, Mollusca and Opiliones. Items exclusively consumed by I. henselii were Chilopoda, Coleoptera (larvae), Diptera (larvae), Hemiptera (nymphs), Lepidoptera (adults and larvae) and Orthoptera. Acari, Diplopoda, Hymenoptera and Isoptera were prey items consumed exclusively by A. marmorata (Table 1). Arthropod preys with large body size were crickets and Araneae whereas those with small size were Acari and Collembola.
The niche breadth of I. henselii was BA = 0.43 and that of A. marmorat was BA = 0.19. The mean SVL of I. henselii (27.4 ± 4.5 mm; range: 8.55 – 39.93 mm) was significantly larger than that of A. marmorata (16.9 ± 3.5 mm; range: 8.78 – 21.08) (t-test, tsvl= 3.528; df = 48; p = 0.001). In both species the jaw size significantly influenced the maximum volume of prey ingested (I. henselii: mean = 7.6 ± 2.7 mm; range: 2.58 – 14.06 mm; F1.21 = 9.487, R2 = 0.558, p = 0.006 and A.marmorata: mean = 3.97 ± 1.24 mm; range: 2.19 – 5.71 mm; F1.20 = 10.563, R2 = 0.588, p = 0.004) (Figure 1). Niche overlap among species was Ojk 0.52.The mean observed was higher than expected (Фobs= 0.52; Фexp= 0.32; pobs≤pexp= 0.90; pobs≥pexp= 0.09), and did not differ from expected by random.
Relationship between jaw width (mm) and largest prey volume in log 10 (mm3) of food items ingested by Adenomera marmorata (gray symbol) and Ischnocnema henselii (black symbol) in Reserva Natural Salto Morato, Paraná State.
4 Discussion
Our results suggested that even living in syntopy in forest floor, and possibly being
exposed to a similar set of prey, Ischnocnema henselii and
Adenomera marmorata differed in some aspects of their diet.
Although the two species fed on a similar number of prey types
(I. henselii = 18 and
A. marmorata = 15 different prey types),
differences in the types of the consumed items may have contributed to the observed
differences in their diets. Although for many frog species, the diet tend to simply
reflect the availability of prey in the environment (Duellman and Trueb, 1994DUELLMAN, WE. and TRUEB, L., 1994. Biology of
Amphibians. Baltimore: The Johns Hopkins University Press.
670 p.), other factors may also influence
the consumption of preys by frogs. Sabagh et
al. (2010)Sabagh, LT., Ferreira, VL. and Rocha, CFD., 2010. Living together,
sometimes feeding in a similar way: the case of the syntopic hylid frogs
Hypsiboas raniceps and Scinax acuminatus (Anura: Hylidae) in the Pantanal of
Miranda, Mato Grosso do Sul State, Brazil. Brazilian journal of biology =
Revista brasileira de biologia, vol. 70, no. 4, p. 955-959.
http://dx.doi.org/10.1590/S1519-69842010000500006.
PMid:21180899
http://dx.doi.org/10.1590/S1519-69842010...
studied food consumption by two syntopic
hylid species in Central Brazil and suggested that some intrinsic ecological aspects
(e.g. ecophysiology), tended to result in differences in the types of prey eaten and
in their consumption frequencies. Differences in body size may also explain
differences in the rate and type of preys consumed by syntopic frogs (Van Sluys and Rocha, 1998Van Sluys, M. and Rocha, CFD., 1998. Feeding habitats and
microhabitat utilization by two syntopic Brazilian Amazonian frogs (Hyla
minuta and (gr. . Pseudo paludicula
spfalcipes). Revista Brasileira de
Biologia =Brazilian Journal of Biology, vol. 58, no. 4, p.
559-562.).
In the present study, Araneae, Formicidae and Orthoptera were the most important preys to I. henselii, whereas Formicidae, Acari and Blattodea were the most important prey items for A. marmorata. This result can be partially explained by the larger size of I. henselii, which allow the consumption of preys of comparatively larger sizes, as spiders and crickets. On the other hand, the importance of Acari consumed by A. marmorata may reflect the comparatively smaller body size of this frog, which may favor the consumption of small preys. Only Ischnocnema henselii consumed Orthoptera (large prey), while solely A. marmorata ate Acari (small prey). These preys consumed exclusively for each species possibly contributed to the coexistence of these species of leaf-litter frogs.
Although leptodactylids are not considered important predators of mites species in
the leaf-litter (Simon and Toft, 1991Simon, MP. and Toft, CA., 1991. Diet specialization in small
vertebrates: mite-eating in frogs. Oikos, vol. 61, no. 2, p. 263-278.
http://dx.doi.org/10.2307/3545344.
http://dx.doi.org/10.2307/3545344...
), this
item can be an important food resource to smaller species, as recorded for
Adenomera andreae in the Central Amazon (Lima, 1998Lima, AP., 1998. The effects of size on the diets of six sympatric
species of post metamorphic litter anurans in central Amazonia. Journal of
Herpetology, vol. 32, no. 3, p. 392-399.
http://dx.doi.org/10.2307/1565453.
http://dx.doi.org/10.2307/1565453...
), for Zachaenus parvulus in the
Atlantic Forest (Van Sluys et al., 2001Van Sluys, M., ROCHA, CFD. and SOUZA, MB., 2001. Diet, reproduction
and density of the leptodactylid litter frog in an Atlantic Rain Forest of
southeastern Brazil. Zachaenus parvulusJournal of Herpetology,
vol. 35, no. 2, p. 322-325. http://dx.doi.org/10.2307/1566124.
http://dx.doi.org/10.2307/1566124...
),
also for miniaturized frog species such as Brachycephalus
didactylus (Almeida-Santos et al.,
2011Almeida-Santos, M., Siqueira, CC., Van Sluys, M. and Rocha, CFD.,
2011. Ecology of the Brazilian Flea Frog . Brachycephalus
didactylus (Terrarana: Brachycephalidae)Journal of Herpetology,
vol. 45, no. 2, p. 251-255. http://dx.doi.org/10.1670/10-015.1.
http://dx.doi.org/10.1670/10-015.1...
) and for Ischnochnema parva (Martins et al., 2010Martins, ACJS., Kiefer, MC., Siqueira, CC., Van Sluys, M., Menezes,
VA. and Rocha, CFD., 2010. Ecology of . Ischnocnema parva
(Anura: Brachycephalidae) at the Atlantic rainforest of Serra da Concórdia,
state of Rio de Janeiro, BrazilZoologia, vol. 27, no. 2, p. 201-208.
http://dx.doi.org/10.1590/S1984-46702010000200007.
http://dx.doi.org/10.1590/S1984-46702010...
), another frog species that inhabit the
leaf-litter. We demonstrated that A. marmorata had a higher
consumption of ants in terms of number (42.2%), frequency (86.4%) and importance
(45.7%), compared to I. henselii (N = 15.4; F = 21.4; Ix = 13.3),
what was not expected for a leptodactylid considered as non-ant-specialist guild
(sensu Toft, 1980Toft, CA., 1980. Feeding ecology of thirteen syntopic species of
anurans in a seasonal tropical environment. Oecologia, vol. 45, no. 1, p.
131-141. http://dx.doi.org/10.1007/BF00346717.
http://dx.doi.org/10.1007/BF00346717...
). However, our results
reinforce the idea that this generalization may not apply to A.
marmorata species group, since ants form a substantial part of its
diet, as was also reported by Almeida-Gomes et al.
(2007)Almeida-Gomes, M., Van Sluys, M. and Rocha, CFD., 2007. Ecological
observations on the leaf-litter frog in an Atlantic rainforest area of
southeastern Brazil. Adenomera marmorataThe Herpetological
Journal, vol. 17, p. 81-85.. In the Amazon, the consumption of ants by Adenomera
andreae by adult individuals was also higher (Sabagh et al., 2012Sabagh, LT., Mello, RS. and Rocha, CFD., 2012. Food niche overlap
between two sympatric leaf-litter frog species from Central Amazonia. Zoologia,
vol. 29, no. 1, p. 95-98.
http://dx.doi.org/10.1590/S1984-46702012000100013.
http://dx.doi.org/10.1590/S1984-46702012...
), whereas for small individuals the
proportion of mites dominated (Pimentel Lima and
Magnusson, 1998PIMENTEL Lima, A. and Magnusson, WE., 1998. Partitioning seasonal
time: interactions among size, foraging activity and diet in leaf litter frogs.
Oecologia, vol. 116, no. 1-2, p. 259-266.
http://dx.doi.org/10.1007/s004420050587.
http://dx.doi.org/10.1007/s004420050587...
). As argued by Toft
(1980)Toft, CA., 1980. Feeding ecology of thirteen syntopic species of
anurans in a seasonal tropical environment. Oecologia, vol. 45, no. 1, p.
131-141. http://dx.doi.org/10.1007/BF00346717.
http://dx.doi.org/10.1007/BF00346717...
, ant-specialist species tend to eat slower and chitinous prey,
whereas those who are non-ant-specialists tend to eat faster-moving prey such as
cockroaches, crickets and spiders. Ischnocnema henselii showed a
comparatively lower consumption of ants and may be considered a non-ant-specialist
(sensu Toft, 1980Toft, CA., 1980. Feeding ecology of thirteen syntopic species of
anurans in a seasonal tropical environment. Oecologia, vol. 45, no. 1, p.
131-141. http://dx.doi.org/10.1007/BF00346717.
http://dx.doi.org/10.1007/BF00346717...
). It consumed higher
amount of fast-moving prey, compared to A. marmorata. On the other
hand, it has been shown that ants have a high biomass in tropical rainforests (Hölldobler and Wilson, 1990Hölldobler, B. and Wilson, EO., 1990. The Ants.
Cambridge: Belknap Press of Harvard University Press. 732 p..
http://dx.doi.org/10.1007/978-3-662-10306-7.
http://dx.doi.org/10.1007/978-3-662-1030...
), which also may
explain the importance of the consumption of these arthropods.
We conclude that the diet of the two syntopic species of leaf-litter frogs studied were composed basically of arthropod preys and that the observed niche overlap did not differ from expected at random. Concurrently, the distinct size of preys ingested (larger in Ischnocnema henselii), the differences in trophic niche breadth (greater in I. henselii) and the occurrence of exclusive prey categories (Orthoptera by I. henselii and Acari by A. marmorata) among the three more important items consumed, all these factors might explain the coexistence of these two frogs on the forest floor at Reserva Natural Salto Morato. These differences in prey consumption may be due to differences in jaw and body size of these species, as well, differences in activity period (broader in A. marmorata). Thus, even living in the same habitat and sharing a specific microhabitat, leaf-litter frogs from Atlantic Rainforest can feed on different things.
Acknowledgments
This study was supported by research grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (#304791/2010-5 and 470265/2010-8) and from the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) through “Cientistas do Nosso Estado” Program (E-26/102.765/2012) to CFDR. Graduate fellowships were granted to MSP from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). Financial support for the realization of the project was granted by Fundação Grupo Boticário de Proteção à Natureza (FBPN), through the Reserva Natural Salto Morato (Term Partnership nº 0165_2012_PR). Authorization (No. 20703-3) to collect the frogs was granted by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). We thank DC. Passos and LT. Sabagh, which kindly reviewed a draft version offering valuable suggestions.
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References
- Almeida-Gomes, M., Van Sluys, M. and Rocha, CFD., 2007. Ecological observations on the leaf-litter frog in an Atlantic rainforest area of southeastern Brazil. Adenomera marmorataThe Herpetological Journal, vol. 17, p. 81-85.
- Almeida-Santos, M., Siqueira, CC., Van Sluys, M. and Rocha, CFD., 2011. Ecology of the Brazilian Flea Frog . Brachycephalus didactylus (Terrarana: Brachycephalidae)Journal of Herpetology, vol. 45, no. 2, p. 251-255. http://dx.doi.org/10.1670/10-015.1.
» http://dx.doi.org/10.1670/10-015.1 - SIh, A. and Christensen, B., 2001. Optimal diet theory: when does it work, and when and why does it fail? Animal Behaviour, vol. 61, no. 2, p. 379-390. http://dx.doi.org/10.1006/anbe.2000.1592.
» http://dx.doi.org/10.1006/anbe.2000.1592 - Câmara, IG., 2005. Breve história da conservação da Mata Atlântica. In GALINDO-LEAL, C. and CÂMARA, IG. (Eds.). Mata Atlântica: Biodiversidade, ameaças e perspectivas. São Paulo: Fundação SOS Mata Atlântica; Belo Horizonte: Conservação Internacional. p. 31-42.
- DUELLMAN, WE. and TRUEB, L., 1994. Biology of Amphibians. Baltimore: The Johns Hopkins University Press. 670 p.
- Dunham, AE., 1983. Realized niche overlap, resource abundance, and intensity of interspecific competition. In HUEY, RB., PIANKA, ER. and SCHOENER, TW. (Eds.). Lizard ecology: studies of a model organism. Cambridge: Harvard University Press. p. 261-280. http://dx.doi.org/10.4159/harvard.9780674183384.c15.
» http://dx.doi.org/10.4159/harvard.9780674183384.c15 - Fundação Grupo Boticário de Proteção à Natureza – FBPN2011Plano de Manejo da Reserva Natural Salto Morato – Guaraqueçaba - PRCuritibaFundação Grupo Boticário de Proteção à Natureza222p. vol1
- Frost, DR., 2013. Amphibian Species of the World: an Online Reference. New York: American Museum of Natural History. Available from: <http://research.amnh.org/herpetology/amphibia/index.html>. Access in: 9 Jan. 2013.
- Gotelli, NJ. and Entsminger, GL., 2006. EcoSim: null models software for ecology. Jericho: Acquired Intelligence Inc. and Kesey-Bear.
- Gotelli, NJ. and Graves, GR., 1996. Null models in Ecology. Washington: Smithsonian Institute. 368 p.
- Haddad, CFB., Toledo, LF., Prado, CPA., Loebmann, D., Gasparini, JL. and Sazima, I., 2013. Guia dos Anfíbios da Mata Atlântica: diversidade e biologia = Guide to the amphibians of the Atlantic Forest: diversity and biology. São Paulo: Anolisbooks. 544 p.
- Hardin, G., 1960. The competitive exclusion principle. Science, vol. 131, no. 3409, p. 1292-1297. http://dx.doi.org/10.1126/science.131.3409.1292. PMid:14399717
» http://dx.doi.org/10.1126/science.131.3409.1292» PMid:14399717 - Hölldobler, B. and Wilson, EO., 1990. The Ants. Cambridge: Belknap Press of Harvard University Press. 732 p.. http://dx.doi.org/10.1007/978-3-662-10306-7.
» http://dx.doi.org/10.1007/978-3-662-10306-7 - Jaeger, RG. and Inger, RF., 1994. Quadrat sampling. In: HEYER, WR., DONNELLY, MA., MCDIARMID, RW., HAYEK, LC. and FOSTER, MS. (Eds.). Measuring and monitoring biological diversity: standard methods for amphibians. Washington: Smithsonian Institution Press. p. 97-102.
- Levins, R., 1968. Evolution in changing environments. Princeton: Princeton University Press. 120 p.
- Lima, AP., 1998. The effects of size on the diets of six sympatric species of post metamorphic litter anurans in central Amazonia. Journal of Herpetology, vol. 32, no. 3, p. 392-399. http://dx.doi.org/10.2307/1565453.
» http://dx.doi.org/10.2307/1565453 - PIMENTEL Lima, A. and Magnusson, WE., 1998. Partitioning seasonal time: interactions among size, foraging activity and diet in leaf litter frogs. Oecologia, vol. 116, no. 1-2, p. 259-266. http://dx.doi.org/10.1007/s004420050587.
» http://dx.doi.org/10.1007/s004420050587 - Macarthur, R. and Levins, R., 1967. The limiting similarity, convergence, and divergence of coexisting species. American Naturalist, vol. 101, no. 921, p. 377-385. http://dx.doi.org/10.1086/282505.
» http://dx.doi.org/10.1086/282505 - Martins, ACJS., Kiefer, MC., Siqueira, CC., Van Sluys, M., Menezes, VA. and Rocha, CFD., 2010. Ecology of . Ischnocnema parva (Anura: Brachycephalidae) at the Atlantic rainforest of Serra da Concórdia, state of Rio de Janeiro, BrazilZoologia, vol. 27, no. 2, p. 201-208. http://dx.doi.org/10.1590/S1984-46702010000200007.
» http://dx.doi.org/10.1590/S1984-46702010000200007 - Menin, M., ROSSA-FERES, DC. and GIARETTA, AA., 2005. Resource use and coexistence of two syntopic hylid frogs (Anura, Hylidae). Revista Brasileira de Zoologia, vol. 22, no. 1, p. 61-72. http://dx.doi.org/10.1590/S0101-81752005000100008.
» http://dx.doi.org/10.1590/S0101-81752005000100008 - Pianka, ER., 1973. The structure of lizard communities. Annual Review of Ecology and Systematics, vol. 4, no. 1, p. 53-74. http://dx.doi.org/10.1146/annurev.es.04.110173.000413.
» http://dx.doi.org/10.1146/annurev.es.04.110173.000413 - Pianka, ER., 1994. Evolutionary ecology. 5th ed. New York: Harper Collins College Publishers. 486 p.
- Powell, R., Parmerlee, JS., Rice, MA. and Smith, DD., 1990. Ecological observations on Hemidactylus brookihaitianus Meerwarth (Sauria: Gekkonidae) from Hispaniola. Caribbean Journal of Science, vol. 26, p. 67-70.
- Sabagh, LT., Ferreira, VL. and Rocha, CFD., 2010. Living together, sometimes feeding in a similar way: the case of the syntopic hylid frogs Hypsiboas raniceps and Scinax acuminatus (Anura: Hylidae) in the Pantanal of Miranda, Mato Grosso do Sul State, Brazil. Brazilian journal of biology = Revista brasileira de biologia, vol. 70, no. 4, p. 955-959. http://dx.doi.org/10.1590/S1519-69842010000500006. PMid:21180899
» http://dx.doi.org/10.1590/S1519-69842010000500006 - Sabagh, LT., Mello, RS. and Rocha, CFD., 2012. Food niche overlap between two sympatric leaf-litter frog species from Central Amazonia. Zoologia, vol. 29, no. 1, p. 95-98. http://dx.doi.org/10.1590/S1984-46702012000100013.
» http://dx.doi.org/10.1590/S1984-46702012000100013 - Santos-Pereira, M., Candaten, A., Milani, D., Oliveira, FB., Gardelin, J. and Rocha, CFD., 2011. Seasonal Variation in the Leaf-Litter Frog Community (Amphibia: Anura) from an Atlantic Forest Area in Salto Morato Natural Reserve, Southern Brazil. Zoologia, vol. 28, no. 6, p. 755-761. http://dx.doi.org/10.1590/S1984-46702011000600008.
» http://dx.doi.org/10.1590/S1984-46702011000600008 - Schoener, TW., 1974. Resource partitioning in ecological communities. Science, vol. 185, no. 4145, p. 27-39. http://dx.doi.org/10.1126/science.185.4145.27. PMid:17779277
» http://dx.doi.org/10.1126/science.185.4145.27 - Simon, MP. and Toft, CA., 1991. Diet specialization in small vertebrates: mite-eating in frogs. Oikos, vol. 61, no. 2, p. 263-278. http://dx.doi.org/10.2307/3545344.
» http://dx.doi.org/10.2307/3545344 - Taper, ML. and Marquet, PA., 1996. How do species really divide resources? American Naturalist, vol. 147, no. 6, p. 1072-1082. http://dx.doi.org/10.1086/285893.
» http://dx.doi.org/10.1086/285893 - Toft, CA., 1980. Feeding ecology of thirteen syntopic species of anurans in a seasonal tropical environment. Oecologia, vol. 45, no. 1, p. 131-141. http://dx.doi.org/10.1007/BF00346717.
» http://dx.doi.org/10.1007/BF00346717 - Triplehorn, CA. and Johnson, NF., 2005. Borror and DeLong's introduction to the study of insects. 7th ed. Belmont: Thomson Brooks/Cole. 864 p.
- Van Sluys, M. and Rocha, CFD., 1998. Feeding habitats and microhabitat utilization by two syntopic Brazilian Amazonian frogs (Hyla minuta and (gr. . Pseudo paludicula spfalcipes). Revista Brasileira de Biologia =Brazilian Journal of Biology, vol. 58, no. 4, p. 559-562.
- Van Sluys, M., ROCHA, CFD. and SOUZA, MB., 2001. Diet, reproduction and density of the leptodactylid litter frog in an Atlantic Rain Forest of southeastern Brazil. Zachaenus parvulusJournal of Herpetology, vol. 35, no. 2, p. 322-325. http://dx.doi.org/10.2307/1566124.
» http://dx.doi.org/10.2307/1566124 - Zar, JH., 1999. Biostatistical Analysis. 4th ed. Upper Saddle River: Prentice Hall. 663 p.
Publication Dates
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Publication in this collection
Jan-Mar 2015
History
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Received
04 Sept 2013 -
Accepted
06 Jan 2014