Articles
Published 2021-05-05
Keywords
- microhabitat segregation,
- coexistence,
- tadpoles,
- niche,
- environmental variables
How to Cite
Sun, Z., Zhao, C., Xu, D., Zhu, W., Fan, W., Zhao, T., & Su, S. (2021). Microhabitat segregation of two coexisting tadpole species on Emei Mountain. Acta Herpetologica, 16(1), 3–9. https://doi.org/10.36253/a_h-9758
Funding data
-
National Natural Science Foundation of China
Grant numbers 31700353
Abstract
Understanding mechanisms determining the coexistence between different species is one of the key issues in community ecology and biodiversity conservation. Microhabitat segregation is a way for species to coexist, which reflects the specific habitat selection of coexisting species in a finer spatial scale. Despite quantitative studies have been conducted to investigate the microhabitat segregation of coexisting species, this type of studies was not often performed on tadpoles. In this study, we assessed the habitat selection of two coexisting tadpoles (Quasipaa boulengeri and Leptobrachium boringii) in a stream on Emei Mountain, China. Our results demonstrated that L. boringii and Q. boulengeri tadpoles occupied different microhabitats. Specifically, Q. boulengeri tadpoles preferred deep, narrow, and weak acid stream segments with slow current velocity and low value of conductivity, while L. boringii tadpoles tended to occur in a wide, shallow water bodies with relatively higher pH, conductivity, and current velocity. Overall, our study supported the Hutchinson’s niche concept, showing that at least one dimension of niche differentiation (i.e., microhabitat) occurred between coexisting tadpole species.
References
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Baker, J. A.& Ross, S. T. (1981): Spatial temporal resource utilization by southeastern cyprinids. Copeia. 178-189.
Biesterfeldt, J. M., Petranka, J. W.& Sherbondy, S. (1993): Prevalence of chemical interference competition in natural populations of wood frogs, Rana sylvtica. Copeia. 1993: 688-695.
Caceres, N.& Machado, A. (2013): Spatial, dietary and temporal niche dimensions in ecological segregation of two sympatric, congeneric marsupial species. The Open Ecology Joural 6: 10–23.
Ceneviva-Bastos, M., Casatti, L.& Rossa-Feres, D. C. (2010): Meso and microhabitat analysis and feeding habits of small nektonic characins (Teleostei: Characiformes) in Neotropical streams. Zoologia. 27: 191-200.
Dammhahn, M.& Goodman, S. M. (2014): Trophic niche differentiation and microhabitat utilization revealed by stable isotope analyses in a dry-forest bat assemblage at Ankarana, northern Madagascar. J Trop Ecol. 30: 97-109.
Dammhahn, M., Soarimalala, V.& Goodman, S. M. (2013): Trophic niche differentiation and microhabitat utilization in a species-rich montane forest small mammal community of Eastern Madagascar. Biotropica. 45: 111-118.
Escoriza, D., Pascual, G.& Sanchez-Vialas, A. (2018): Habitat use in south-west European skinks (genus Chalcides). PeerJ. 6: e4274.
Fatorelli, P., Pereira, E. G., Almeida-Gomes, M.& Rocha, C. F. D. (2015): Population dynamics of Hylodes uai tadpoles (Anura, Hylodidae) in a tropical forest stream, southeastern Brazil. J Herpetol. 49: 23-27.
Fei, L., Ye, C.& Jiang, J. P. (2012): Colored Atlas of Chinese Amphibians and Their Distributions. Sichuan Publishing House of Science & Technology, Chengdu (In Chinese with English Abstract).
Freitas, J. S., Girotto, L., Goulart, B. V., Goncalves, Alho L. d. O., Gebara, R. C., Montagner, C. C., Schiesari, L.& Gaeta Espindola, E. L. (2019): Effects of 2,4-D-based herbicide (DMA (R) 806) on sensitivity, respiration rates, energy reserves and behavior of tadpoles. Ecotoxicology and Environmental Safety. 182: 109446.
Glos, J., Wolter, J., Struck, U.& Rodel, M. O. (2017): Ecological shifts during larval development in two West African savanna frogs. J Trop Ecol. 33: 50-59.
Golden, D. R., Smith, G. R.& Rettig, J. E. (2001): Effects of age and group size on habitat selection and activity level in Rana pipiens tadpoles. Herpetolog J. 11: 69-73.
Grinnell, J. (1917): Field tests of theories concerning distributional control. Am Nat. 51: 115-128.
Grossman, G. D.& Ratajczak, R. E. (1998): Long-term patterns of microhabitat use by fish in a southern Appalachian stream from 1983 to 1992: effects of hydrologic period, season and fish length. Ecology of Freshwater Fish. 7: 108-131.
Gu, H. Y.& Li, C. H. (2008): Preliminarily Study on the Pteridophytes Flora of Emei Mountain. Acta Botanica Boreali-Occidentalia Sinica. 28: 2381-2387 (In Chinese with English Abstract).
Guo, Z. Q., Liu, J. S., Lek, S., Li Z. J., Ye, S. W., Zhu, F. Y., Tang, J. F.& Cucherousset, J. (2012): Habitat segregation between two congeneric and introduced goby species. Fundam Appl Limnol. 181: 241-251.
Hanane, S. (2015): Nest‐niche differentiation in two sympatric Streptopelia species from a North African agricultural area: the role of human presence Ecol Res. 30: 573-580.
Haramura, T. (2007): Microhabitat selection by tadpoles of Buergeria japonica inhabiting the coastal area. J Ethol. 25: 3-7.
Hocking, D. J.& Babbitt, K. J. (2014): Amphibian contributions to ecosystem services. Herpetol Conserv Bio. 9: 1-17.
Horinouchi, M. (2008): Patterns of food and microhabitat resource use by two benthic gobiid fishes. Environ Biol Fishes. 82: 187-194.
Hued, A. C.& Bistoni, M. D. (2006): Microhabitat use by two silurid species in the Anizacate River (central Argentina). Folia Zool. 55: 175-182.
Hutchinson, G. E. (1957): Population studies-Animal ecology and demography-Concluding Remarks. Cold Spring Harbor Symp Quant Biol. 22: 415-427.
IUCN. (2019): The IUCN red list of threatened species.Version 2019-3. Retrieved from https://www.iucn.org/theme/species/our-work/iucn-red-list-threatened-species. Accessed 06 Sept 2019
Johnson, D. H. (1980): The comparison of usage and availability measurements for evaluating resource preerence. Ecology. 61: 65-71.
Jordani, M. X., Mouquet, N., Casatti, L., Menin, M., Rossa-Feres, D. D.& Albert, C. H. (2019): Intraspecific and interspecific trait variability in tadpole meta-communities from the Brazilian Atlantic rainforest. Ecol Evol. 9: 4025-4037.
Jorgensen, E. E. (2004): Small mammal use of microhabitat reviewed. J Mammal. 85: 531-539.
Kessler, R. K.& Thorp, J. H. (1993): Microhabitat segregation of the threatened spotted darter (Etheostoma maculatum) and closely-related orangefin-darter (E bellum) Canadian Journal of Fisheries and Aquatic Sciences. 50: 1084-1091.
Leger, D. W., Owings, D. H.& Coss, R. G. (1983): Behavioral ecology of time allocation in California ground-squirrels (Spermophilus beecheyi) microhabitat effects. J Comp Psychol. 97: 283-291.
Ling, Z. (2005): Biodiversity monitoring and assessment report of Emei Mount. Institute of Nature Science ChengDu (In Chinese with English Abstract).
Macarthur, R.& Levins, R. (1967): The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist. 101: 377-385.
Marques, N. C. S.& Nomura, F. (2018): Environmental and spatial factors affect the composition and morphology of tadpole assemblages. Can J Zool. 96: 1130-1136.
Martin, T. E. (2001): Abiotic vs. biotic influences on habitat selection of coexisting species: climata change inpacts? Ecology of Freshwater Fish. 82: 175-188.
Melo, G. L., Miotto, B., Peres, B.& Caceres, N. C. (2013): Microhabitat of small mammals at ground and understorey levels in a deciduous, southern Atlantic Forest. An Acad Bras Cienc. 85: 727-736.
Morris, D. W. (1987): Ecological scale and habitat use. Ecology. 68: 362-369.
Nakano, S., Fausch, K. D., Furukawatanaka, T., Maekawa, K.& Kawanabe, H. (1992): Resource utilization by bull char and cutthroat trout in a mountain stream in Montana, USA. Jpn J Ichthyol. 39: 211-217.
Negovetic, S., Anholt, B. R., Semlitsch, R. D.& Reyer, H. U. (2001): Specific responses of sexual and hybridogenetic European waterfrog tadpoles to temperature. Ecology. 82: 766-774.
Nicolai, V. (1986): The bark of trees-thermal-properties, microclimate and fauna. Oecologia. 69: 148-160.
Rosenfeld, J. S. (2002): Functional redundancy in ecology and conservation. Oikos. 98: 156-162.
Salavatulin, V. (2019): Microhabitat distribution of arboreal oribatid mites (Oribatida), associated with the Siberian pine (Pinus sibirica) of Western Siberia. Exp Appl Acarol. 78: 469-483.
Schoener, T. W. (1974): Resource partitioning in ecological communities. Science. 185: 27-39.
Seale, D. B. (1980): Influence of amphibian larvae on primamary production, nutrient flux, and competition in a pond ecosystem. Ecology. 61: 1531-1550.
Segurado, P.& Figueiredo, D. (2007): Coexistence of two freshwater turtle species along a Mediterranean stream: The role of spatial and temporal heterogeneity. Acta Oecologica-international Joural of Ecology. 32: 134-144.
Strauss, A., Reeve, E., Randrianiaina, R.-D., Vences, M.& Glos, J. (2010): The world's richest tadpole communities show functional redundancy and low functional diversity: ecological data on Madagascar's stream-dwelling amphibian larvae. BMC ecology. 10: 12.
R development core team. (2019): R: a language and environment for statistical computing. Retrieved from http://www.R-proje ct.org/. Accessed 15 Oct 2019
Tubay, J. M., Suzuki, K., Uehara, T., Kakishima, S., Ito, H., Ishida, A., Yoshida, K., Mori, S., Rabajante, J. F., Morita, S., Yokozawa, M.& Yoshimura, J. (2015): Microhabitat locality allows multi-species coexistence in terrestrial plant communities. Sci Rep. 5: 9.
Wang, X., Chang, L., Zhao, T., Liu, L., Zhang, M., Li, C., Xie, F., Jiang, J.& Zhu, W. (2019): Metabolic switch in energy metabolism mediates the sublethal effects induced by glyphosate-based herbicide on tadpoles of a farmland frog Microhyla fissipes. Ecotoxicology and environmental safety. 186: 1-11.
Wei, F. W., Feng, Z. J., Wang, Z. W.& Hu, J. C. (2000): Habitat use and separation between the giant panda and the red panda. J Mammal. 81: 448-455.
Wei, G., Zhang, W. Y.& Guo, P. (2017): Amphibians in Fanjingshan Mount. Guizhou Science and Technology Publishing House Co.,Ltd. , GuiZhou (In Chinese with English Abstract).
Xia, S. S., Hu, D. M., Deng, Y., Zhong, X., Bai, W. K., Zhang, J. D., Wang, B.& Zhou, C. Q. (2019): Habitat partitioning between sympatric Golden Pheasant and Temminck' s Tragopan at different spatial scales. Acta Ecologica Sinica. 39: 1627-1638 (In Chinese with English Abstract).
Xu, D., WU, X. Q., Zhao, C. L., Zhu, W. B., Zhao, T.& Su, S. Q. (2020): Functional approach reveals niche differentiation between two coexisting tadpoles: Leptobrachium boringii and Quasipaa boulengeri. Acta Ecologica Sinica 40: 43-50 (In Chinese with English Abstract).
Yang, S. N., Jiang, J. P., Luo, Z. H., Yang, X., Wang, X. Y., Liao, W. B.& Hu, J. H. (2019): Microhabitat Segregation of Parapatric Frogs in the Qinling Mountains. Asian Herpetological Research 10(1): 48–55.
Yen, S., Wang, Y., Yu, P., Kuan, Y., Liao, Y., Chen, K.& Weng, G. (2019): Seasonal space use and habitat selection of sambar in Taiwan. The Journal of Wildlife Management. 83: 22-31.
Zhao, T., Li, C., Wang, X., Xie, F.& Jiang, J. (2017): Unraveling the relative contribution of inter- and intrapopulation functional variability in wild populations of a tadpole species. Ecol Evol. 7: 4726-4734.
Zhao, T., Wang, X. Y., Wang, X. G., Wang, S. S., Chen, Y. H.& Jiang, J. P. (2019): Effects of urea on behavior and functional traits of Asiatic toad (Bufo gargarizans) tadpoles. Aquat Ecol. 53: 9-19.
Alford, R. A.& Wilbur, H. M. (1985): Priority effects in expermental pond communities-competition between Bufo and Rana. Ecology. 66: 1097-1105.
Almeida-Gomes, M., Hatano, F. H., Van Sluys, M.& Rocha, C. F. D. (2007): Diet and microhabitat use by two Hylodinae species (Anura, Cycloramphidae) living in sympatry and syntopy in a Brazilian Atlantic Rainforest area. Iheringia Ser Zool. 97: 27-30.
Baker, J. A.& Ross, S. T. (1981): Spatial temporal resource utilization by southeastern cyprinids. Copeia. 178-189.
Biesterfeldt, J. M., Petranka, J. W.& Sherbondy, S. (1993): Prevalence of chemical interference competition in natural populations of wood frogs, Rana sylvtica. Copeia. 1993: 688-695.
Caceres, N.& Machado, A. (2013): Spatial, dietary and temporal niche dimensions in ecological segregation of two sympatric, congeneric marsupial species. The Open Ecology Joural 6: 10–23.
Ceneviva-Bastos, M., Casatti, L.& Rossa-Feres, D. C. (2010): Meso and microhabitat analysis and feeding habits of small nektonic characins (Teleostei: Characiformes) in Neotropical streams. Zoologia. 27: 191-200.
Dammhahn, M.& Goodman, S. M. (2014): Trophic niche differentiation and microhabitat utilization revealed by stable isotope analyses in a dry-forest bat assemblage at Ankarana, northern Madagascar. J Trop Ecol. 30: 97-109.
Dammhahn, M., Soarimalala, V.& Goodman, S. M. (2013): Trophic niche differentiation and microhabitat utilization in a species-rich montane forest small mammal community of Eastern Madagascar. Biotropica. 45: 111-118.
Escoriza, D., Pascual, G.& Sanchez-Vialas, A. (2018): Habitat use in south-west European skinks (genus Chalcides). PeerJ. 6: e4274.
Fatorelli, P., Pereira, E. G., Almeida-Gomes, M.& Rocha, C. F. D. (2015): Population dynamics of Hylodes uai tadpoles (Anura, Hylodidae) in a tropical forest stream, southeastern Brazil. J Herpetol. 49: 23-27.
Fei, L., Ye, C.& Jiang, J. P. (2012): Colored Atlas of Chinese Amphibians and Their Distributions. Sichuan Publishing House of Science & Technology, Chengdu (In Chinese with English Abstract).
Freitas, J. S., Girotto, L., Goulart, B. V., Goncalves, Alho L. d. O., Gebara, R. C., Montagner, C. C., Schiesari, L.& Gaeta Espindola, E. L. (2019): Effects of 2,4-D-based herbicide (DMA (R) 806) on sensitivity, respiration rates, energy reserves and behavior of tadpoles. Ecotoxicology and Environmental Safety. 182: 109446.
Glos, J., Wolter, J., Struck, U.& Rodel, M. O. (2017): Ecological shifts during larval development in two West African savanna frogs. J Trop Ecol. 33: 50-59.
Golden, D. R., Smith, G. R.& Rettig, J. E. (2001): Effects of age and group size on habitat selection and activity level in Rana pipiens tadpoles. Herpetolog J. 11: 69-73.
Grinnell, J. (1917): Field tests of theories concerning distributional control. Am Nat. 51: 115-128.
Grossman, G. D.& Ratajczak, R. E. (1998): Long-term patterns of microhabitat use by fish in a southern Appalachian stream from 1983 to 1992: effects of hydrologic period, season and fish length. Ecology of Freshwater Fish. 7: 108-131.
Gu, H. Y.& Li, C. H. (2008): Preliminarily Study on the Pteridophytes Flora of Emei Mountain. Acta Botanica Boreali-Occidentalia Sinica. 28: 2381-2387 (In Chinese with English Abstract).
Guo, Z. Q., Liu, J. S., Lek, S., Li Z. J., Ye, S. W., Zhu, F. Y., Tang, J. F.& Cucherousset, J. (2012): Habitat segregation between two congeneric and introduced goby species. Fundam Appl Limnol. 181: 241-251.
Hanane, S. (2015): Nest‐niche differentiation in two sympatric Streptopelia species from a North African agricultural area: the role of human presence Ecol Res. 30: 573-580.
Haramura, T. (2007): Microhabitat selection by tadpoles of Buergeria japonica inhabiting the coastal area. J Ethol. 25: 3-7.
Hocking, D. J.& Babbitt, K. J. (2014): Amphibian contributions to ecosystem services. Herpetol Conserv Bio. 9: 1-17.
Horinouchi, M. (2008): Patterns of food and microhabitat resource use by two benthic gobiid fishes. Environ Biol Fishes. 82: 187-194.
Hued, A. C.& Bistoni, M. D. (2006): Microhabitat use by two silurid species in the Anizacate River (central Argentina). Folia Zool. 55: 175-182.
Hutchinson, G. E. (1957): Population studies-Animal ecology and demography-Concluding Remarks. Cold Spring Harbor Symp Quant Biol. 22: 415-427.
IUCN. (2019): The IUCN red list of threatened species.Version 2019-3. Retrieved from https://www.iucn.org/theme/species/our-work/iucn-red-list-threatened-species. Accessed 06 Sept 2019
Johnson, D. H. (1980): The comparison of usage and availability measurements for evaluating resource preerence. Ecology. 61: 65-71.
Jordani, M. X., Mouquet, N., Casatti, L., Menin, M., Rossa-Feres, D. D.& Albert, C. H. (2019): Intraspecific and interspecific trait variability in tadpole meta-communities from the Brazilian Atlantic rainforest. Ecol Evol. 9: 4025-4037.
Jorgensen, E. E. (2004): Small mammal use of microhabitat reviewed. J Mammal. 85: 531-539.
Kessler, R. K.& Thorp, J. H. (1993): Microhabitat segregation of the threatened spotted darter (Etheostoma maculatum) and closely-related orangefin-darter (E bellum) Canadian Journal of Fisheries and Aquatic Sciences. 50: 1084-1091.
Leger, D. W., Owings, D. H.& Coss, R. G. (1983): Behavioral ecology of time allocation in California ground-squirrels (Spermophilus beecheyi) microhabitat effects. J Comp Psychol. 97: 283-291.
Ling, Z. (2005): Biodiversity monitoring and assessment report of Emei Mount. Institute of Nature Science ChengDu (In Chinese with English Abstract).
Macarthur, R.& Levins, R. (1967): The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist. 101: 377-385.
Marques, N. C. S.& Nomura, F. (2018): Environmental and spatial factors affect the composition and morphology of tadpole assemblages. Can J Zool. 96: 1130-1136.
Martin, T. E. (2001): Abiotic vs. biotic influences on habitat selection of coexisting species: climata change inpacts? Ecology of Freshwater Fish. 82: 175-188.
Melo, G. L., Miotto, B., Peres, B.& Caceres, N. C. (2013): Microhabitat of small mammals at ground and understorey levels in a deciduous, southern Atlantic Forest. An Acad Bras Cienc. 85: 727-736.
Morris, D. W. (1987): Ecological scale and habitat use. Ecology. 68: 362-369.
Nakano, S., Fausch, K. D., Furukawatanaka, T., Maekawa, K.& Kawanabe, H. (1992): Resource utilization by bull char and cutthroat trout in a mountain stream in Montana, USA. Jpn J Ichthyol. 39: 211-217.
Negovetic, S., Anholt, B. R., Semlitsch, R. D.& Reyer, H. U. (2001): Specific responses of sexual and hybridogenetic European waterfrog tadpoles to temperature. Ecology. 82: 766-774.
Nicolai, V. (1986): The bark of trees-thermal-properties, microclimate and fauna. Oecologia. 69: 148-160.
Rosenfeld, J. S. (2002): Functional redundancy in ecology and conservation. Oikos. 98: 156-162.
Salavatulin, V. (2019): Microhabitat distribution of arboreal oribatid mites (Oribatida), associated with the Siberian pine (Pinus sibirica) of Western Siberia. Exp Appl Acarol. 78: 469-483.
Schoener, T. W. (1974): Resource partitioning in ecological communities. Science. 185: 27-39.
Seale, D. B. (1980): Influence of amphibian larvae on primamary production, nutrient flux, and competition in a pond ecosystem. Ecology. 61: 1531-1550.
Segurado, P.& Figueiredo, D. (2007): Coexistence of two freshwater turtle species along a Mediterranean stream: The role of spatial and temporal heterogeneity. Acta Oecologica-international Joural of Ecology. 32: 134-144.
Strauss, A., Reeve, E., Randrianiaina, R.-D., Vences, M.& Glos, J. (2010): The world's richest tadpole communities show functional redundancy and low functional diversity: ecological data on Madagascar's stream-dwelling amphibian larvae. BMC ecology. 10: 12.
R development core team. (2019): R: a language and environment for statistical computing. Retrieved from http://www.R-proje ct.org/. Accessed 15 Oct 2019
Tubay, J. M., Suzuki, K., Uehara, T., Kakishima, S., Ito, H., Ishida, A., Yoshida, K., Mori, S., Rabajante, J. F., Morita, S., Yokozawa, M.& Yoshimura, J. (2015): Microhabitat locality allows multi-species coexistence in terrestrial plant communities. Sci Rep. 5: 9.
Wang, X., Chang, L., Zhao, T., Liu, L., Zhang, M., Li, C., Xie, F., Jiang, J.& Zhu, W. (2019): Metabolic switch in energy metabolism mediates the sublethal effects induced by glyphosate-based herbicide on tadpoles of a farmland frog Microhyla fissipes. Ecotoxicology and environmental safety. 186: 1-11.
Wei, F. W., Feng, Z. J., Wang, Z. W.& Hu, J. C. (2000): Habitat use and separation between the giant panda and the red panda. J Mammal. 81: 448-455.
Wei, G., Zhang, W. Y.& Guo, P. (2017): Amphibians in Fanjingshan Mount. Guizhou Science and Technology Publishing House Co.,Ltd. , GuiZhou (In Chinese with English Abstract).
Xia, S. S., Hu, D. M., Deng, Y., Zhong, X., Bai, W. K., Zhang, J. D., Wang, B.& Zhou, C. Q. (2019): Habitat partitioning between sympatric Golden Pheasant and Temminck' s Tragopan at different spatial scales. Acta Ecologica Sinica. 39: 1627-1638 (In Chinese with English Abstract).
Xu, D., WU, X. Q., Zhao, C. L., Zhu, W. B., Zhao, T.& Su, S. Q. (2020): Functional approach reveals niche differentiation between two coexisting tadpoles: Leptobrachium boringii and Quasipaa boulengeri. Acta Ecologica Sinica 40: 43-50 (In Chinese with English Abstract).
Yang, S. N., Jiang, J. P., Luo, Z. H., Yang, X., Wang, X. Y., Liao, W. B.& Hu, J. H. (2019): Microhabitat Segregation of Parapatric Frogs in the Qinling Mountains. Asian Herpetological Research 10(1): 48–55.
Yen, S., Wang, Y., Yu, P., Kuan, Y., Liao, Y., Chen, K.& Weng, G. (2019): Seasonal space use and habitat selection of sambar in Taiwan. The Journal of Wildlife Management. 83: 22-31.
Zhao, T., Li, C., Wang, X., Xie, F.& Jiang, J. (2017): Unraveling the relative contribution of inter- and intrapopulation functional variability in wild populations of a tadpole species. Ecol Evol. 7: 4726-4734.
Zhao, T., Wang, X. Y., Wang, X. G., Wang, S. S., Chen, Y. H.& Jiang, J. P. (2019): Effects of urea on behavior and functional traits of Asiatic toad (Bufo gargarizans) tadpoles. Aquat Ecol. 53: 9-19.