Abstract
Amphibians are declining and fertility/fecundity are major drivers of population stability. The development of non-destructive methods to assess reproductive health are needed as destructive measures are fundamentally at odds with conservation goals for declining species. We investigated the utility of body size, nuptial pad size and forelimb width as non-destructive biomarkers of internal reproductive physiology, by analysing correlations with commonly used destructive methods in adult male toads (Bufo bufo) from a low human impact and a high human impact site. Principal component analyses revealed that size was the most important variable for explaining inter-individual differences in other measured endpoints, both non-destructive and destructive, except for hormone levels and nuptial pad, which were independent of size. Toads from the LI and the HI site differed in almost all of the measured endpoints; this was largely driven by the significantly smaller size of toads from the HI site. Correlational analyses within sites revealed that size was correlated with several reproductive endpoints in toads from the HI site but not the LI site, indicating a possible limiting effect of size on reproductive physiology. Intersex was observed in 33 % of toads from the HI site and incidence was not related to any other measured endpoint. In conclusion, we provide evidence that size is associated with reproductive physiology and that nuptial pad/hormone levels have potential as additional markers due to their independence from size. We also show that human activities can have a negative effect on reproductive physiology of the common toad.
Abbreviations
- LI:
-
Low impact
- HI:
-
High impact
- SVL:
-
Snout–vent length
- BO:
-
Bidders’ organ
References
Calisi RM (2005) Variation in Bidder’s organ volume is attributable to reproductive status in Bufo woodhousii. J Herpetol 39:656–659
Carrier JA, Beebee TJC (2003) Recent, substantial, and unexplained declines of the common toad Bufo bufo in lowland England. Biol Conserv 111:395–399
Davies NB, Halliday TR (1977) Optimal mate selection in the toad Bufo bufo. Nature 269:56–58
Emerson SB (1997) Testis size variation in frogs: testing the alternatives. Behav Ecol Sociobiol 41:227–235
Emerson SB, Hess DL (2001) Glucocorticoids, androgens, testis mass, and the energetics of vocalization in breeding male frogs. Horm Behav 39:59–69
Emerson SB, Greig A, Carroll L, Prins GS (1999) Androgen receptors in two androgen-mediated, sexually dimorphic characters of frogs. Gen Comp Endocrinol 114:173–180
Gittins SP, Parker AG, Slater FM (1980) Population characteristics of the common toad (Bufo bufo) visiting a breeding site in mid-wales. J Anim Ecol 49:161–173
Gray MJ, Smith LM (2005) Influence of land use on postmetamorphic body size of playa lake amphibians. J Wildl Manage 69:515–524
Hayes TB, Anderson LL, Beasley VR, de Solla SR, Iguchi T, Ingraham H, Kestemont P, Kniewald J, Kniewald Z, Langlois VS, Luque EH, McCoy KA, Muà ± oz-de-Toro MN, Oka T, Oliveira CA, Orton F, Ruby S, Suzawa M, Tavera-Mendoza LE, Trudeau VL, Victor-Costa AB, Willingham E (2011) Demasculinization and feminization of male gonads by atrazine: consistent effects across vertebrate classes. J Steroid Biochem Mol Biol 127:64–73
Herrel A, Gonwouo LN, Fokam EB, Ngundu WI, Bonneaud C (2012) Intersexual differences in body shape and locomotor performance in the aquatic frog, Xenopus tropicalis. J Zool 287:311–316
Hopkins WA, Mendonca MT, Congdon JD (1997) Increased circulating levels of testosterone and corticosterone in southern toads, Bufo terrestris, exposed to coal combustion waste. Gen Comp Endocrinol 108:237–246
Hyne RV, Spolyarich N, Wilson SP, Patra RW, Byrne M, Gordon G, Sanchez-Bayo F, Palmer CG (2009) Distribution of frogs in rice bays within an irrigated agricultural area: links to pesticide usage and farm practices. Environ Toxicol Chem 28:1255–1265
IUCN (2001) IUCN red list categories and criteria version 3.1 ed. Gland, Switzerland, p 32. http://www.iucnredlist.org/technical-documents/categories-and-criteria/2001-categories-criteria
Jorgensen CB, Larsen LO, Lofts B (1979) Annual cycles of fat-bodies and gonads in the toad Bufo–Bufo Bufo (L),—compared with cycles in other temperate zone anurans. Biol Skr K Dan Vidensk Selsk 22:3
Narayan EJ, Cockrem J, Hero J-M (2013) Changes in serum and urinary corticosterone and testosterone during short-term capture and handling in the cane toad (Rhinella marina). Gen Comp Endocrinol 191:225–230
Norris DO (2006) Vertebrate endocrinology, 4th edn. Academic Press, San Diego
Orton F, Routledge E (2011) Agricultural intensity in ovo affects growth, metamorphic development and sexual differentiation in the Common toad (Bufo bufo). Ecotoxicology 20:901–911
Orton F, Carr JA, Handy RD (2006) Effects of nitrate and atrazine on larval development and sexual differentiation in the northern leopard frog Rana pipiens. Environ Toxicol Chem 25:65–71
Owens IPF, Bennett PM (2000) Ecological basis of extinction risk in birds: habitat loss versus human persecution and introduced predators. Proc Natl Acad Sci 97:12144–12148
Reading CJ, Clarke RT (1995) The effects of density, rainfall and environmental temperature on body condition and fecundity in the common toad, Bufo bufo. Oecologia 102:453–459
Reeder AL, Foley GL, Nichols DK, Hansen LG, Wikoff B, Faeh S, Eisold J, Wheeler MB, Warner R, Murphy JE, Beasley VR (1998) Forms and prevalence of intersexuality and effects of environmental contaminants on sexuality in cricket frogs (Acris crepitans). Environ Health Perspect 106:261–266
Shaw PJA (2003) Multivariate statistics for environmental sciences. Hodder Headline Group, London
Storrs-Mendez SI, Semlitsch RD (2010) Intersex gonads in frogs: understanding the time course of natural development and role of endocrine disruptors. J Exp Zool B Mol Dev Evol 314B:57–66
Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786
Temple H, Cox N (2009) European red list of amphibians. In: IUCN (ed) Species programme. Office for official publications of the European communities, Luxembourg. http://www.iucnredlist.org/technical-documents/categories-and-criteria/2001-categories-criteria
Witschi E (1930) Studies on sex differentiation and sex determination in amphibians. IV. The geographical distribution of the sex races of the European grass frog (Rana temporaria, L.). A contribution to the problem of the evolution of sex. J Exp Zool 56:149–165
Acknowledgment
Funding from the Zoological Society of London gratefully received.
Conflict of interest
There are no competing financial interests.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Orton, F., Baynes, A., Clare, F. et al. Body size, nuptial pad size and hormone levels: potential non-destructive biomarkers of reproductive health in wild toads (Bufo bufo). Ecotoxicology 23, 1359–1365 (2014). https://doi.org/10.1007/s10646-014-1261-3
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-014-1261-3