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Effects of Breeding Habitat on the Abundance and Body Condition of Two Pelophylax Species in Agriculture and Urban Landscapes

Hina Amin, Amaël Borzée, Kevin R. Messenger, Saad Muse Muhammad, Shoaib Ahmad, Honghua Ruan

Abstract


Amphibians play a key role in structuring biological assemblages of agricultural landscapes, but they are threatened globally by agricultural intensification. Numerous studies have considered the morphology of animals to be an indicator of the health of a population, but data about the differences in amphibian morphology in different breeding habitats in agricultural landscapes are still missing. Here, we investigated the differences in the abundance and morphology of Pelophylax plancyi and Pelophylax nigromaculatus in the three waterbody types: fields, forests, and parks in agricultural landscapes in Nanjing, China. Our results emphasize that both frog species in forests and parks had significantly higher body condition indexes than those in fields, whereas their abundance in fields habitat was higher than those of the two other habitat types. Our results demonstrated the importance of non-agricultural habitats (such as forests and parks) in agricultural landscapes to the persistence of both Pelophylax species. We recommend preserving field ecosystems by constructing diverse waterbodies other than fields in rural areas and maintaining microhabitats in parks and forests to improve amphibian biodiversity in Nanjing.

Keywords


agriculture; microhabitat; black-spotted pond frog; gold-striped pond frog; China

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References


Alvey A. A. (2006), «Promoting and preserving biodiversity in the urban forest», Urban For. Urban Green, 5(4), 195 – 201.

Anholt B. R., Werner E., and Skelly D. K. (2000), «Effect of food and predators on the activity of four larval ranid frogs», Ecology, 81(12), 3509 – 3521.

Anonimous (2018), Annual Report on Biodiversity Monitoring in China 2017, Nanjing Institute of Environmental Sciences 2018.

Babini M. S., de Lourdes Bionda C., Salinas Z. A., Salas N. E., and Martino A. L. (2018), «Reproductive endpoints of Rhinella arenarum (Anura, Bufonidae): Populations that persist in agroecosystems and their use for the environmental health assessment», Ecotoxicol. Environ. Saf., 154, 294 – 301.

Berger L. and Rybacki M. (1993), «Growth an maturity of brown frogs, Rana arvalis and Rana temporaria, in central Poland», Alytes, 11(1), 17 – 24.

Bickford D., Ng T. H., Qie L., Kudavidanage E. P., and Bradshaw C. J. A. (2010), «Forest fragment and breeding habitat characteristics explain frog diversity and abundance in Singapore», Biotropica, 42(1), 119 – 125.

Bishop P. J., Angulo A., Lewis J. P., Moore R. D., Rabb G. B., and Garcia Moreno J. (2012), «The amphibian extinction crisis – what will it take to put the action into the amphibian conservation action plan?» S.A.P.I.EN.S., 5(2), 97 – 111.

Borzée A., Heo K., and Jang Y. (2018a), «Relationship between agro-environmental variables and breeding Hylids in rice paddies», Sci. Rep., 8(1), 1 – 14.

Borzée A., Kim J. Y., Da Cunha M. A. M., Lee D., Sin E., Oh S., Yi Y., and Jang Y. (2016), «Temporal and spatial differentiation in microhabitat use: Implications for reproductive isolation and ecological niche specification», Integr. Zool., 11(5), 375 – 387.

Borzée A., Kyong C. N., Kil H. K., and Jang Y. (2018b), «Impact of water quality on the occurrence of two endangered Korean Anurans: Dryophytes suweonensis and Pelophylax chosenicus», Herpetologica, 74(1), 1 – 7.

Borzée A., Purevdorj Z., Kim Y. I., Kong S., Choe M., Yi Y., Kim K., Kim A., and Jang Y. (2019a), «Breeding preferences in the treefrogs Dryophytes japonicus (Hylidae) in Mongolia», J. Nat. Hist., 53, 2685 – 2698.

Borzée A., Ren J.-L., Li J.-T., Groffen J., Jang Y., and Yang Y. (2019b), «Microhabitat segregation between Black-spotted Pond Frogs, Pelophylax nigromaculatus, and Gold-striped Pond Frogs, P. plancyi (Anura: Ranidae)», Reptiles Amphib. Conserv. Nat. Hist., 26(2), 119 – 120.

Carrier J.-A. and Beebee T. (2003), «Recent, substantial, and unexplained declines of the common toad Bufo bufo in lowland England», Biol. Conserv., 111, 395 – 399.

Cooke R. S. C., Eigenbrod F., and Bates A. E. (2019), «Projected losses of global mammal and bird ecological strategies», Nat. Commun., 10(1), 1 – 8.

Costa R. N. and Nomura F. (2016), «Measuring the impacts of roundup original on fluctuating asymmetry and mortality in a Neotropical tadpole», Hydrobiologia, 765(1), 85 – 96.

Crump M. L. and Scott N. J. (1994), «Visual encounter surveys», in: R. W. Heyer and M. A. Donelly, Measuring and Monitoring Biological Diversity: Standard Methods for Amphibian, Smithsonian Inst. Press, Washington, DC, pp. 84 – 91.

Cushman S. (2006), «Effects of habitat loss and fragmentation on amphibians: A review and prospectus», Biol. Conserv., 128, 231 – 240.

DeMaynadier P. G. and Hunter M. L. (1999), «Forest canopy closure and juvenile emigration by pool-breeding Amphibians in Maine», J. Wildl. Manag., 63(2), 441.

Donald P. (2004), «Biodiversity impacts of some agricultural commodity production systems», Biol. Conserv., 18, 17 – 38.

Fei L., Ye C., and Jiang J. (2012), Colored Atlas of Chinese Amphibians and Their Distributions, Sichuan Publishing Press, Chengdu.

Guerra C. and Aráoz E. (2016), «Amphibian malformations and body condition across an agricultural landscape of northwest Argentina», Dis. Aquat. Organ. J., 121(2), 105 – 116.

Guzy J. C., Mccoy E. D., Deyle A. C., Gonzalez S. M., Halstead N., and Mushinsky H. R. (2012), «Urbanization interferes with the use of amphibians as indicators of ecological integrity of wetlands», J. Appl. Ecol., 49(4), 941 – 952.

Hairston N. G., Ellner S. P., Geber M. A., Yoshida T., and Fox J. A. (2005), «Rapid evolution and the convergence of ecological and evolutionary time», Ecol. Lett., 8(10), 1114 – 1127.

Halstead B. J., Ray A. M., Muths E., Grant E. H. C., Grasso R., Adams M. J., Delaney K. S., Carlson J., and Hossack B. R. (2022), «Looking ahead, guided by the past: The role of U.S. national parks in amphibian research and conservation», Ecol. Indic., 136, 108631.

Hamer A. and McDonnell M. (2008), «Amphibian ecology and conservation in the urbanising world: A review», Biol. Conserv., 141, 2432 – 2449.

Harvey C., Medina A., Sánchez D., Vilchez Mendoza S., Hernández B., Saenz J., Maes J., Casanoves F., and Sinclair F. (2006), «Patterns of animal diversity in different forms of tree cover in agricultural landscapes», Ecol. Appl., 16, 1986 – 1999.

Hayes J. P. and Shonkwiler J. S. (2001), «Morphometric indicators of body condition: worthwhile or wishful thinking», in: Body Composition Analysis of Animals: a Handbook of Non-Destructive Methods, Cambridge Univ. Press, Cambridge, UK.

Huang K., Zhiqiang M. U., Qu Y. U. E., Feng Y. U., Xiao Y., Shunqi B. O., and Zhenghuan W. (2018), «Microhabitat utilization of Anuran species in Shanghai Country Parks GoogleEarth Pro», Sich. J. Zool., 37(4), 426 – 434.

Huang M. H. (1990), Fauna of Zhejiang: Amphibians and Reptilia, Zhejiang Science and Technology Publishing House, Hangzhou [in Chinese].

IUCN (2019). The IUCN Red List of Threatened Species. https://www.iucnredlist.org (assessed 2019).

Janin A., Léna J. P., and Joly P. (2011), «Beyond occurrence: Body condition and stress hormone as integrative indicators of habitat availability and fragmentation in the common toad», Biol. Conserv., 144(3), 1008 – 1016.

Jennette M. A., Snodgrass J. W., and Forester D. C. (2019), «Variation in age, body size, and reproductive traits among urban and rural amphibian populations», Urban Ecosyst., 22(1), 137 – 147.

Johnson J. B., Saenz D., Adams C. K., and Hibbitts T. J. (2015), «Naturally occurring variation in tadpole morphology and performance linked to predator regime», Nat. Ecol. Evol., 5(15), 2991 – 3002.

Katayama N., Goto T., Narushima F., Amano T., Kobori H., and Miyashita T. (2013), «Indirect positive effects of agricultural modernization on the abundance of Japanese tree frog tadpoles in rice fields through the release from predators», Aquat. Ecol., 47(2), 225 – 234.

Kato N., Yoshio M., Kobayashi R., and Miyashita T. (2010), «Differential responses of two anuran species breeding in rice fields to landscape composition and spatial scale», Wetlands, 30(6), 1171 – 1179.

Kidera N., Kadoya T., Yamano H., Takamura N., Ogano D., Wakabayashi T., Takezawa M., and Hasegawa M. (2018), «Hydrological effects of paddy improvement and abandonment on amphibian populations; long-term trends of the Japanese brown frog, Rana japonica», Biol. Conserv., 219, 96 – 104.

Knutson M. G., Sauer J. R., Olsen D. A., Mossman M. J., Hemesath L. M., and Lannoo M. J. (1999), «Effects of landscape composition and wetland fragmentation on frog and toad abundance and species richness in Iowa and Wisconsin, U.S.A»., Conserv. Biol., 13(6), 1437 – 1446.

Koumaris A. and Fahrig L. (2016), «Different Anuran species show different relationships to agricultural intensity», Wetlands, 36(4), 731 – 744.

Kruger D. J. D., Hamer A. J., and Du Preez L. H. (2015), «Urbanization affects frog communities at multiple scales in a rapidly developing African city», Urban Ecosyst., 18(4), 1333 – 1352.

Kurali A., Pásztor K., Hettyey A., and Tóth Z. (2018), «Resource-dependent temporal changes in antipredator behavior of common toad (Bufo bufo) tadpoles», Behav. Ecol. Sociobiol., 72, 91.

Lawler S. P. (1989), «Behavioural responses to predators and predation risk in four species of larval anurans», Animal Behav., 38(6), 1039 – 1047.

Liu K., Wang F., Chen W., Tu L., Min M.-S., Bi K., and Fu J. (2010), «Rampant historical mitochondrial genome introgression between two species of green pond frogs, Pelophylax nigromaculatus and P. plancyi», BMC Evol. Biol., 10, 201.

Lowe W. H. (2003). Linking dispersal to local population dynamics: A case study using a headwater salamander system», Ecology, 84(8), 2145 – 2154.

Lowe W. H., Likens G. E., and Cosentino B. J. (2006), «Self-organisation in streams: The relationship between movement behaviour and body condition in a headwater salamander», Freshwater Biol., 51(11), 2052 – 2062.

Mann R. M., Hyne R. V., Choung C. B., and Wilson S. P. (2009), «Amphibians and agricultural chemicals: Review of the risks in a complex environment», Environ. Poll., 157(11), 2903 – 2927.

Marsh D. and Pearman P. (1997), «Effects of habitat fragmentation on the abundance of two species of Leptodactylid frogs in an Andean Montane Forest», Conserv. Biol., 11, 1323 – 1328.

Marty P., AngÉlibert S., Giani N., and Joly P. (2005), «Directionality of pre- and post-breeding migrations of a marbled newt population (Triturus marmoratus): Implications for buffer zone management», Aquat. Conserv., 15, 215 – 225.

Mazerolle M. J. and Desrochers (2005), «Landscape resistance to frog movements», Can. J. Zool., 83(3), 455 – 464.

Mazerolle Marc J., Bailey L. L., Kendall W. L., Royle J. A., Converse S. J., and Nichols J. D. (2007), «Making great leaps forward: Accounting for detectability in herpetological field studies», J. Herpetol., 41(4), 672 – 689.

Mccaffery R., Eby L., Maxell B., and Corn P. (2014), «Breeding site heterogeneity reduces variability in frog recruitment and population dynamics», Biol. Conserv., 170, 169 – 176.

Mckinney M. L. (2002), «Urbanization, biodiversity, and conservation: the impacts of urbanization on native species are poorly studied, but educating a highly urbanized human population about these impacts can greatly improve species conservation in all ecosystems», Bioscience, 52(10), 883 – 890.

Pellet J., Guisan A., and Perrin N. (2004), «A concentric analysis of the impact of urbanization on the threatened European tree frog in an agricultural landscape», Conserv. Biol., 18(6), 1599 – 1606.

Relyea R. A. (2007), «Getting out alive: How predators affect the decision to metamorphose», Oecologia, 152(3), 389 – 400.

Ribeiro J., Colli G. R., Caldwell J. P., Ferreira E., Batista R., and Soares A. (2017), «Evidence of neotropical anuran community disruption on rice crops: a multidimensional evaluation», Biodivers. Conserv., 26(14), 3363 – 3383.

Scheffers B. and Paszkowski C. (2013), «Amphibian use of urban stormwater wetlands: The role of natural habitat features», Landsc. Urban Plan., 113, 139 – 149.

Scheffers B. R. and Paszkowski C. A. (2012), «The effects of urbanization on North American amphibian species: Identifying new directions for urban conservation», Urban Ecosyst., 15(1), 133 – 147.

Schulte-Hostedde A. I., Zinner B., Millar J. S., and Hickling G. J. (2005), «Restitution of mass-size residuals: Validating body condition indices», Eco, 86(1), 155 – 163.

Scott D. E., Casey E. D., Donovan M. F., and Lynch T. K. (2007), «Amphibian lipid levels at metamorphosis correlate to post-metamorphic terrestrial survival», Oecologia, 153(3), 521 – 532.

Shu X., Zhang W., Li B., Pei E., Yuan X., Wang T., and Wang Z. (2016), «Major factors affecting the distribution of Anuran communities in the urban, suburban and rural areas of Shanghai, China», Asian Herpetol. Res., 7(4), 287 – 294.

Stuart S., Chanson J., Cox N., Young B., Rodrigues A., Fischman D., and Waller R. (2005), «Status and trends of amphibian declines and extinctions worldwide», Science, 306, 1783 – 1786.

Van Buskirk J. (2000), «The costs of an inducible defense in anuran larvae», Ecology, 81(10), 2813 – 2821.

Van Buskirk J. (2002), «A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae», Am. Naturalist, 160(1), 87 – 102.

Wang Y., Wu Z., Lu P., Zhang F., and Li Y. (2008), «Breeding ecology and oviposition site selection of black-spotted pond frogs (Rana nigromaculata) in Ningbo, China», Front Biol. China, 3(4), 530 – 535.

Yao L. X., Huang L. X., Li G. L., He Z. H., Zhou C. M., Yang B. M., and Guo B. (2010), «Pesticide residual status in litchi orchard soils in Guangdong», China Environ. Sci., 31, 2723 – 2726.

Yuan Y., Wu S., Yu Y., Tong G., Mo L., Yan D., and Li F. (2018), «Spatiotemporal interaction between ecosystem services and urbanization: Case study of Nanjing City, China», Ecol. Indic., 95, 917 – 929.




DOI: https://doi.org/10.30906/1026-2296-2024-31-5-284-292

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