Skip to main content

Advertisement

Log in

Leaf litter input to ponds can dramatically alter amphibian morphological phenotypes

  • Population ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Phenotypic plasticity in growth and development is commonly examined, but morphology can exhibit plasticity as well. Leg length plasticity is important, because it impacts mobility, which affects predator avoidance, prey capture, and seasonal movements. Differences in relative (i.e., body size adjusted) hind leg lengths > 5% in anurans affect jumping abilities, and resource levels and predation can generate these differences. Leaf litter input can alter larval growth and development and likely morphology as well. I show that relative leg length [leg length/snout-to-vent length (SVL) × 100%] can be quite variable, ranging from 44% of SVL to 120% of SVL across the following species: Hyla versicolor, Lithobates sylvaticus, L. sphenocephalus, and Anaxyrus americanus. Within species variability was highest in L. sylvaticus and almost as great as across species. I measured relative leg length for metamorphs from aquatic mesocosm studies examining the effects of plant litter type and quality. I also examined the relative importance of different environmental variables, including water quality, predation, resource level, and temperature. Good predictors were found only for the two ranids, where leaf litter input was the only variable found to affect relative leg length. Ranid frogs had longer legs when emerging from mesocosms with grass than mesocosms with no litter input, and deciduous leaves produced metamorphs intermediate in leg length. These results suggest that habitat changes in vegetation from land use change, invasive species, and climate change may affect the mobility and fitness of individuals through changes in metamorph relative leg length.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

Most of the data is available at the Knowledge Network for Biocomplexity https://knb.ecoinformatics.org/view/urn%3Auuid%3Adddaa020-1038-4c34-a270-67a5a16e2f23. Additional data is available by request.

References

  • Alho JS, Herczeg G, Laugen AT, Räsänen K, Laurila A, Merilä J (2011) Allen’s rule revisited: quantitative genetics of extremity length in the common frog along a latitudinal gradient. J Evol Biol 24:59–70

    CAS  PubMed  Google Scholar 

  • Anderson DR, Burnham KP (2002) Avoiding pitfalls when using information-theoretic methods. J Wildl Manag 66:912–918

    Google Scholar 

  • Bernard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life cycles. Annu Rev Ecol Evol Syst 35:651–673

    Google Scholar 

  • Blouin MS, Brown ST (2000) Effects of temperature-induced variation in anuran larval growth rate on head width and leg length at metamorphosis. Oecologia 125:358–361

    PubMed  Google Scholar 

  • Blouin MS, Loeb MLG (1991) Effects of environmentally induced development-rate variation on head and limb morphology in the green tree frog, Hyla cinerea. Am Nat 138:717–728

    Google Scholar 

  • Boes MW, Benard MF (2013) Carry-over effects in nature: Effects of canopy cover and individual pond on size, shape, and locomotor performance of metamorphosing wood frogs. Copeia 2013:717–722

    Google Scholar 

  • Boone MD (2005) Juvenile frogs compensate for small metamorph size with terrestrial growth: overcoming the effects of larval density and insecticide exposure. J Herpetol 39:416–423

    Google Scholar 

  • Brown CJ, Blossey B, Maerz JC, Joule SJ (2006) Invasive plant and experimental venue affect tadpole performance. Biol Invasions 8:327–338

    Google Scholar 

  • Burnham KP, Anderson DH, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35

    Google Scholar 

  • Charbonnier JF, Vonesh JR (2015) Consequences of life history switch pointplasticity for juvenile morphology and locomotion in the Túngara frog. PeerJ 3:e1268

    PubMed  PubMed Central  Google Scholar 

  • Clesceri LS, Greenberg AE, Trussell RR (eds) (1989) Standard methods for the examination of water and wastewater, 17th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Earl JE, Semlitsch RD (2012) Reciprocal subsidies in ponds: does leaf input increase frog biomass export? Oecologia 170:1077–1087. https://doi.org/10.1007/s00442-012-2361-5

    Article  PubMed  Google Scholar 

  • Earl JE, Semlitsch RD (2013) Carryover effects in amphibians: are characteristics of the larval habitat needed to predict juvenile survival? Ecol Appl 23:1429–1442

    PubMed  Google Scholar 

  • Earl JE, Semlitsch RD (2015) Effect of tannin source and concentration from tree leaves on two species of tadpoles. Environ Toxicol Chem 34:120–126

    CAS  PubMed  Google Scholar 

  • Earl JE, Whiteman HH (2015) Are commonly used fitness predictors accurate? A meta-analysis of amphibian size and age at metamorphosis. Copeia 103:297–309

    Google Scholar 

  • Earl JE, Cohagen KE, Semlitsch RD (2012) Effects of leachate from tree leaves and grass litter on tadpoles. Environ Toxicol Chem 31:1511–1517

    CAS  PubMed  Google Scholar 

  • Earl JE, Castello PO, Cohagen KE, Semlitsch RD (2014) Effects of subsidy quality on reciprocal subsidies: how leaf litter species changes frog biomass export. Oecologia 175:209–218

    PubMed  Google Scholar 

  • Fontaine TD III, Ewel KC (1981) Metabolism of a Florida lake ecosystem. Limnol Oceanogr 26:754–763

    Google Scholar 

  • Gomez-Mestre I, Saccoccio VL, Iijima T, Collins EM, Rosenthal GG, Warkentin KM (2010) The shape fo things to come: linking developmental plasticity to post-metamorphic morphology in anurans. J Evol Biol 23:1364–1373

    CAS  PubMed  Google Scholar 

  • Hector KL, Nakagawa S (2012) Quantitative analysis of compensatory and catch-up growth in diverse taxa. J Anim Ecol 81:583–593

    PubMed  Google Scholar 

  • Maerz JC, Brown CJ, Chapin CT, Blossey B (2005) Can secondary compounds of an invasive plant affect larval amphibians? Funct Ecol 19:970–975

    Google Scholar 

  • Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692

    PubMed  Google Scholar 

  • Orizaola G, Laurila A (2009) Microgeographic variation in the effects of larval temperature environment on juvenile morphology and locomotion in the pool frog. J Zool 277:267–274

    Google Scholar 

  • Pfennig DW, Mabry A, Orange D (1991) Environmental causes of correlations between age and size at metamorphosis in Scaphiopus multiplicatus. Ecology 72:2240–2248

    Google Scholar 

  • Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803

    CAS  PubMed  Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. The John Hopkins University Press, Baltimore

    Google Scholar 

  • Richter-Boix A, Llorente GA, Montori A (2006) Effects of phenotypic plasticity on post-metamorphic traits during pre-metamorphic stages in the anuran Pelodytes punctatus. Evol Ecol Res 8:309–320

    Google Scholar 

  • Rubbo MJ, Kiesecker JM (2004a) Leaf litter composition and community structure: translating regional species changes into local dynamics. Ecology 85:2519–2525

    Google Scholar 

  • Rubbo MJ, Kiesecker JM (2004b) Leaf litter composition and community structure: translating regional species changes into local dynamics. Ecology 85:2519–2525

    Google Scholar 

  • Schiesari L (2006) Pond canopy cover: A resource gradient for anuran larvae. Freshw Biol 51:412–423

    CAS  Google Scholar 

  • Skelly DK, Freidenburg LK, Kiesecker JM (2002) Forest canopy and the performance of larval amphibians. Ecology 83:983–992

    Google Scholar 

  • Smith GR (1997) The effects of aeration on amphibian larval growth: an experiment with bullfrog tadpoles. Trans Nebr Acad Sci 24:63–66

    Google Scholar 

  • Stephens JP, Berven KA, Tiegs SD (2013) Anthropogenic changes to leaf litter input affect the fitness of a larval amphibian. Freshw Biol 58:1631–1646

    CAS  Google Scholar 

  • Stephens JP, Berven KA, Tiegs SD, Raffel TR (2015) Ecological stoichiometry quantitatively predicts responses of tadpoles to a food quality gradient. Ecology 96:2070–2076. https://doi.org/10.1890/14-2439.1

    Article  PubMed  Google Scholar 

  • Stoler AB, Relyea RA (2011) Living in the litter: the influence of tree leaf litter on wetland communities. Oikos 120:862–872

    Google Scholar 

  • Stoler AB, Stephens JP, Relyea RA, Berven KA, Tiegs SD (2015) Leaf litter resource quality induces morphological changes in wood frog (Lithobates sylvaticus) metamorphs. Oecologia 179:667–677

    PubMed  Google Scholar 

  • Tejedo M, Semlitsch RD, Hotz H (2000b) Differential morphology and jumping performance of newly metamorphosed frogs of the hybridogenetic Rana esculenta complex. J Herpetol 34:201–210

    Google Scholar 

  • Tejedo M, Semlitsch RD, Hotz H (2000a) Covariation of morphology and jumping performance in newly metamorphosed water frogs: effects of larval growth history. Copeia 2000(2):448–458

    Google Scholar 

  • Tejedo M et al (2010) Contrasting effects of environmental factors during larval stage on morphologial plasticity in post-metamorphic frogs. Clim Res 43:31–39

    Google Scholar 

  • Travis J (1981) Control of larval growth variation in a population of Pseudacris triseriata (anura: hylidae). Evolution 35:423–432

    PubMed  Google Scholar 

  • Trokovic N, Gonda A, Herczeg G, Laurila A, Merilä J (2011) Brain plasticity over the metamorphic boundary: carry-over effect of larval environment on froglet brain development. J Evol Biol 24:1380–1385

    CAS  PubMed  Google Scholar 

  • Van Buskirk J, Saxer G (2001) Delayed costs of an induced defense in tadpoles? morphology, hopping, and development rate at metamorphosis. Evolution 55:821–829

    PubMed  Google Scholar 

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425

    Google Scholar 

  • Werner EE, Glennemeier KS (1999) Influence of forest canopy cover on the breeding pond distributions of several amphibian species. Copeia 1999:1–12

    Google Scholar 

  • Wetzel RG, Likens GE (2000) Limnological analysis, 3rd edn. Springer, New York

    Google Scholar 

  • Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314

    CAS  PubMed  Google Scholar 

  • Williams BK, Rittenhouse TAG, Semlitsch RD (2008) Leaf litter input mediates tadpole performance across forest canopy treatments. Oecologia 155:377–384

    PubMed  Google Scholar 

  • Zug GR (1972) Anuran locomotion: structure and function. I. Preliminary observations on relation between jumping and osteometrics of appendicular and postaxial skeleton. Copeia 1972:613–624

    Google Scholar 

Download references

Acknowledgements

This paper is dedicated to the life and work of Raymond D. Semlitsch, who supported me personally and academically while I collected this data. This paper would not have been possible without his mentorship. I would also like to thank M. Osbourn, K. Cohagen, K. Malone, P. Castello, D. Leach, and D. Drake for help in the field.

Funding

Financial support was provided by the National Science Foundation (DEB-0239943), a University of Missouri (MU) Life Sciences Fellowship, TWA Scholarship, a MU Conservation Biology Fellowship, and an Environmental Protection Agency STAR Fellowship.

Author information

Authors and Affiliations

Authors

Contributions

JEE conceived, designed, and executed this study and wrote the manuscript. No other person is entitled to authorship.

Corresponding author

Correspondence to Julia E. Earl.

Ethics declarations

Conflict of interest

The author declares that she has no conflict of interest.

Ethical approval

Research was conducted with Missouri Department of Conservation Wildlife Collecting Permits 13759, 14119, and 14467 and under University of Missouri Animal Care Protocols 3368 and 6144.

Consent for publication

Not applicable.

Additional information

Communicated by Ross Andrew Alford .

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Earl, J.E. Leaf litter input to ponds can dramatically alter amphibian morphological phenotypes. Oecologia 195, 145–153 (2021). https://doi.org/10.1007/s00442-020-04819-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-020-04819-1

Keywords

Navigation