Abstract
Secondary compounds leached from plant litter can negatively affect aquatic amphibian larvae. Non-native plants and their potentially distinct secondary compounds may constitute cryptic threats to native amphibians. We used the availability of both native and introduced Phragmites australis (common reed) populations in North America to assess the importance of origin, intraspecific variation, and two purified classes of compounds (tannins and saponins; gradients 0–25 mg L−1) on two common and widespread amphibians (Ambystoma maculatum, spotted salamander, and Lithobates palustris, pickerel frog). In experiments with purified compounds, high tannin concentrations reduced A. maculatum survival and developmental rate while high saponin concentrations reduced survival, developmental rate, and size of L. palustris and reduced A. maculatum developmental rate. In experiments using leaf litter extracts of 14 different P. australis populations, A. maculatum larval survival varied among populations but plant origin (native or introduced) did not explain this variation. In contrast to the lack of effects of purified saponins, increases in saponin concentrations in P. australis leachates significantly decreased A. maculatum survival. Our results suggest: (1) secondary compounds can impact larval amphibian survival and development in species-specific ways; (2) impacts of P. australis on A. maculatum vary among P. australis populations, reflecting intraspecific variation in secondary chemistry; and (3) origin (whether the plant is native or introduced) is a poor predictor of P. australis effects on A. maculatum. Scientists and managers may need to move beyond considering origin as a predictive variable when managing plant communities to benefit amphibians.
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References
Adams CK, Saenz D (2012) Leaf litter of invasive Chinese tallow (Triadica sebifera) negatively affects hatching success of an aquatic breeding anuran, the southern leopard frog (Lithobates sphenocephalus).Can J Zool 90:991–998. doi:10.1139/z2012-067
Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715
Agrawal AA, Hastings AP, Johnson MTJ, Maron JL, Salminen JP (2012) Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–116. doi:10.1126/science.1225977
Allison P (1995) Survival analysis using the SAS system. SAS Institute, Cary
Babbitt K, Jordan F (1996) Predation on Bufo terrestris tadpoles: effects of cover and predator identity. Copeia 2:485–488
Bailey JK et al (2009) From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization. Philos Trans R Soc Lond B 364:1607–1616.doi:10.1098/rstb.2008.0336
Brown CJ, Blossey B, Maerz JC, Joule SJ (2006) Invasive plant and experimental venue affect tadpole performance. Biol Inv 8:327–338
Burggren WW, Infantino RL (1994) The respiratory transition from water to air-breathing during amphibian metamorphosis. Am Zool 34:238–246
Chalcraft DR, Binckley CA, Resetarits WJ Jr (2005) Experimental venue and estimation of interaction strength: comment. Ecology 86:1061–1067
Chen JC, Chen KW, Chen JM (1996) Effects of saponin on survival, growth, molting and feeding of Penaeus japonicus juveniles. Aquaculture 144:165–175. doi:10.1016/s0044-8486(96)01301-4
Cohen JS, Maerz JC, Blossey B (2012) Traits, not origin, explain impacts of plants on larval amphibians. Ecol Appl 22:218–228
Cotten TB, Kwiatkowski MA, Saenz D, Collyer M (2012) Effects of an invasive plant, Chinese Tallow (Triadica sebifera), on development and survival of anuran larvae. J Herpetol 46:186–193. doi:10.1670/10-311
Cox DR (1972) Regression models and life tables. J R Stat Soc 34:187–220
Davidson EW, Larsen A, Palmer CM (2012) Potential influence of plant chemicals on infectivity of Batrachochytrium dendrobatidis. Dis Aquat Org 101:87–93. doi:10.3354/dao02505
Donavan L (1980) Morphological features of the stages in the development of Ambystoma talpoideum (Holbrook) from the fertilized egg to the adult. PhD thesis, University of Southern Mississippi
Drake JM, Kramer AM (2012) Mechanistic analogy: how microcosms explain nature. Theor Ecol 5:433–444. doi:10.1007/s12080-011-0134-0
Earl JE, Semlitsch RD (2012) Reciprocal subsidies in ponds: does leaf input increase frog biomass export? Oecologia 170:1077–1087. doi:10.1007/s00442-012-2361-5
Earl JE, Cohagen KE, Semlitsch RD (2012) Effects of leachate from tree leaves and grass litter on tadpoles. Environ Tox Chem 31:1511–1517. doi:10.1002/etc.1829
Freda J, Dunson WA (1986) Effects of low pH and other chemical variables on the local distribution of amphibians. Copeia. 454–466
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190
Halverson MA, Skelly DK, Kiesecker JM, Freidenburg LK (2003) Forest mediated light regime linked to amphibian distribution and performance. Oecologia 134:360–364
Hansen DL, Lambertini C, Jampeetong A, Brix H (2007) Clone-specific differences in Phragmites australis: effects of ploidy level and geographic origin. Aquat Bot 86:269–279
Haviola S et al (2012) Genetic and environmental factors behind foliar chemistry of the mature mountain birch. J Chem Ecol 38:902–913. doi:10.1007/s10886-012-0148-0
Herlt AJ, Mander LN, Pongoh E, Rumampuk RJ, Tarigan P (2002) Two major saponins from seeds of Barringtonia asiatica: putative antifeedants toward Epilachna sp larvae. J Natural Products 65:115–120. doi:10.1021/np000600b
Hostettmann K, Marston A (1995) Saponins. University of Cambridge Press, Cambridge
Hulse A, McCoy C, Censky E (2001) Amphibians and reptiles of Pennsylvania and the Northeast. Conell University Press, Ithaca
Ishaaya I, Birk Y, Bondi A, Tencer Y (1969) Soyabean saponins. 9. Studies of their effects on birds, mammals and cold blooded organisms. J Sci Food Agric 20:433–436. doi:10.1002/jsfa.2740200716
Kattge J et al (2011) TRY—a global database of plant traits. Glob Change Biol 17:2905–2935. doi:10.1111/j.1365-2486.2011.02451.x
Kerby JL, Richards-Hrdlicka KL, Storfer A, Skelly DK (2010) An examination of amphibian sensitivity to environmental contaminants: are amphibians poor canaries? Ecol Lett 13:60–67. doi:10.1111/j.1461-0248.2009.01399.x
Kopp K, Wachlevski M, Eterovick PC (2006) Environmental complexity reduces tadpole predation by water bugs. Can J Zool 84:136–140. doi:10.1139/z05-186
Kraus TEC, Dahlgren RA, Zasoski RJ (2003) Tannins in nutrient dynamics of forest ecosystem—a review. Plant Soil 256:41–66. doi:10.1023/a:1026206511084
Leishman MR, Thomson VP, Cooke J (2010) Native and exotic invasive plants have fundamentally similar carbon capture strategies. J Ecol 98:28–42. doi:10.1111/j.1365-2745.2009.01608.x
LeRoy CJ, Whitham TG, Keim P, Marks JC (2006) Plant genes link forests and streams. Ecology 87:255–261. doi:10.1890/05-0159
Maerz JC, Brown CJ, Chapin CT, Blossey B (2005) Can secondary compounds of an invasive plant affect larval amphibians? Funct Ecol 19:970–975
Maerz JC, Cohen JS, Blossey B (2010) Does detritus quality predict the effect of native and non-native plants on the performance of larval amphibians? Freshw Biol 55:1694–1704. doi:10.1111/j.1365-2427.2010.02404.x
Martin LJ, Murray BR (2011) A predictive framework and review of the ecological impacts of exotic plant invasions on reptiles and amphibians. Biol Rev 86:407–419. doi:10.1111/j.1469-185X.2010.00152.x
Meier CL, Bowman WD (2008) Links between plant litter chemistry, species diversity, and below-ground ecosystem function. Proc Nat AcadSciUSA 105:19780–19785. doi:10.1073/pnas.0805600105
Melvin SD, Houlahan JE (2012) Tadpole mortality varies across experimental venues: do laboratory populations predict responses in nature? Oecologia 169:861–868. doi:10.1007/s00442-012-2260-9
Morrongiello JR, Bond NR, Crook DA, Wong BBM (2011) Eucalyptus leachate inhibits reproduction in a freshwater fish. Freshw Biol 56:1736–1745. doi:10.1111/j.1365-2427.2011.02605.x
Müller MS, McWilliams SR, Podlesak D, Donaldson JR, Bothwell HM, Lindroth RL (2006) Tri-trophic effects of plant defenses: chickadees consume caterpillars based on host leaf chemistry. Oikos 114:507–517
Njau KN, Renalda M (2010) Performance of horizontal subsurface flow constructed wetland in the removal of tannins. Can J Civil Eng 37:496–501. doi:10.1139/l09-161
Park MG, Blossey B (2008) Importance of plant traits and herbivory for invasiveness of Phragmites australis (Poaceae). Am J Bot 95:1557–1568
Rautio P, Bergvall UA, Karonen M, Salminen JP (2007) Bitter problems in ecological feeding experiments: Commercial tannin preparations and common methods for tannin quantifications. Biochem Syst Ecol 35:257–262. doi:10.1016/j.bse.2006.10.016
Rey D, Pautou MP, Meyran JC (1999) Histopathological effects of tannic acid on the midgut epithelium of some aquatic Diptera larvae. J Invertebr Pathol 73:173–181. doi:10.1006/jipa.1998.4810
Rittenhouse TAG (2011) Anuran larval habitat quality when reed canary grass is present in wetlands. J Herpetol 45:491–496
Rogalski MA, Skelly DK (2012) Positive effects of non-native invasive Phragmites australis on larval bullfrogs. PLoS One 7:e44420. doi:10.1371/journal.pone.0044420
Rubbo MJ, Kiesecker JM (2004) Leaf litter composition and community structure: translating regional species changes into local dynamics. Ecology 85:2519–2525. doi:10.1890/03-0653
Salminen JP, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338. doi:10.1111/j.1365-2435.2010.01826.x
Salminen JP, Roslin T, Karonen M, Sinkkonen J, Pihlaja K, Pulkkinen P (2004) Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J Chem Ecol 30:1693–1711. doi:10.1023/B:JOEC.0000042396.40756.b7
Saltonstall K (2002) Cryptic invasion by non-native genotypes of the common reed, Phragmites australis, into North America. Proc Nat Acad Sci USA 99:2445–2449
Saltonstall K, Peterson PM, Soreng RJ (2004) Recognition of Phragmites australis subsp. americanus (Poaceae: Arundinoideae) in North America: evidence from morphological and genetic analyses. SIDA 21:683–692
Schiesari L (2006) Pond canopy cover: a resource gradient for anuran larvae. Freshw Biol 51:412–423. doi:10.1111/j.1365-2427.2005.01497.x
Skelly DK (2002) Experimental venue and estimation of interaction strength. Ecology 83:2097–2101
Skelly DK, Werner EE, Cortwright SA (1999) Long-term distributional dynamics of a Michigan amphibian assemblage. Ecology 80:2326–2337. doi:10.1890/0012-9658(1999)[2326:ltddoa]2.0.co;2
Skelly DK, Freidenburg LK, Kiesecker JM (2002) Forest canopy and the performance of larval amphibians. Ecology 83:983–992
Smith DS, Bailey JK, Shuster SM, Whitham TG (2011) A geographic mosaic of trophic interactions and selection: trees, aphids and birds. J Evol Biol 24:422–429. doi:10.1111/j.1420-9101.2010.02178.x
Sparg SG, Light ME, van Staden J (2004) Biological activities and distribution of plant saponins. J Ethnopharmacol 94:219–243. doi:10.1016/j.jep.2004.05.016
Stoler AB, Relyea RA (2011) Living in the litter: the influence of tree leaf litter on wetland communities. Oikos 120:862–872. doi:10.1111/j.1600-0706.2010.18625.x
Stuart SN et al (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786
Temmink JHM, Field JA, Vanhaastrecht JC, Merkelbach RCM (1989) Acute and sub-acute toxicity of bark tannins in carp (Cyprinus carpio L). Water Res 23:341–344. doi:10.1016/0043-1354(89)90100-0
Ultsch GR, Bradford DF, Freda J (1999) Physiology: coping with the environment. In: McDiamid R, Altig R (eds) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, pp 189–214
Violle C et al (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252. doi:10.1016/j.tree.2011.11.014
Watling JI, Hickman CR, Lee E, Wang K, Orrock JL (2011a) Extracts of the invasive shrub Lonicera maackii increase mortality and alter behavior of amphibian larvae. Oecologia 165:153–159. doi:10.1007/s00442-010-1777-z
Watling JI, Hickman CR, Orrock JL (2011b) Invasive shrub alters native forest amphibian communities. Biol Conserv 144:2597–2601. doi:10.1016/j.biocon.2011.07.005
Watling JI, Hickman CR, Orrock JL (2011c) Predators and invasive plants affect performance of amphibian larvae. Oikos 120:735–739. doi:10.1111/j.1600-0706.2010.19255.x
Wegner C, Hamburger M (2002) Occurrence of stable foam in the upper Rhine River caused by plant-derived surfactants. Environ Sci Technol 36:3250–3256. doi:10.1021/es025532p
Williams BK, Rittenhouse TAG, Semlitsch RD (2008) Leaf litter input mediates tadpole performance across forest canopy treatments. Oecologia 155:377–384. doi:10.1007/s00442-007-0920-y
Yarnes CT, Boecklen WJ, Tuominen K, Salminen JP (2006) Defining phytochemical phenotypes: size and shape analysis of phenolic compounds in oaks (Fagaceae, Quercus) of the Chihuahuan Desert. Can J Bot 84:1233–1248. doi:10.1139/b06-076
Acknowledgments
We thank A. Laurila, C. Hickmann and two anonymous reviewers for their suggestions and V. Nuzzo, C. Kraft, A. Davalos, J. Maerz, J. Cohen, and E. Feldman for critical feedback. We thank F. Vermeylen for statistical advice, many land managers for collecting litter, and B. Whitmore, S. Biddlecomb, S. Rainford, C. Thurston, I. Conti-Jerpe, W. Simmons, W. Dietrich and J. Dietrich for technical assistance. L.J.M. is supported by the NSF GRFP; additional funding was provided by the NY Department of Transportation. This project was approved by Cornell University’s Institutional Animal Care and Use Committee (Protocol 00-26-03).
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Communicated by Anssi Laurila.
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Martin, L.J., Blossey, B. Intraspecific variation overrides origin effects in impacts of litter-derived secondary compounds on larval amphibians. Oecologia 173, 449–459 (2013). https://doi.org/10.1007/s00442-013-2624-9
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DOI: https://doi.org/10.1007/s00442-013-2624-9