Oecologia

, Volume 165, Issue 1, pp 153–159 | Cite as

Extracts of the invasive shrub Lonicera maackii increase mortality and alter behavior of amphibian larvae

  • J. I. Watling
  • C. R. Hickman
  • E. Lee
  • K. Wang
  • J. L. Orrock
Plant-Animal interactions - Original Paper

Abstract

Water-soluble phytochemicals produced by invasive plants may represent novel elements of invaded ecosystems that can precipitate a variety of direct and indirect effects on native organisms. Phenolic compounds in particular are a common plant defense, and these compounds may have disproportionate impacts on amphibians compared to other taxa. We coupled an exploration of invasive plant extract effects on larvae of four amphibian species (the salamander Ambystoma maculatum, the toad Anaxyrus americanus, and the frogs Hyla sp. and Lithobates blairi) with behavioral observations designed to determine whether behavior can ameliorate the negative effects of exposure to invasive plant extracts. Larvae were reared in extracts of the widespread invasive Amur honeysuckle (Lonicera maackii), mixed native leaf litter, and a water control. Anaxyrus americanus tadpoles reared in L. maackii extracts were more likely to die than tadpoles reared in native extracts, but differences in mortality following rearing in native and exotic extracts were not significant for the other three species. Anaxyrus americanus and L. blairi tadpoles made more trips to the surface in L. maackii extracts than in native extracts, consistent with the hypothesis that exotic extracts may interfere with respiratory physiology and suggesting that L. blairi can behaviorally ameliorate the negative effects of L. maackii extracts. Our study highlights both a direct and indirect pathway by which invasive plant extracts may alter the ecological dynamics of native fauna.

Keywords

Allelopathy Invasive species Missouri Respiration Tadpoles 

References

  1. Bartuszevige AB, Gorchov DL, Raab L (2006) The relative importance of landscape and community features in the invasion of an exotic shrub in a fragmented landscape. Ecography 29:213–222. doi:10.1111/j.2006.0906-7590.04359.x CrossRefGoogle Scholar
  2. Brooks RT, Hayashi M (2002) Depth-area-volume and hydroperiod relationships of ephemeral (vernal) forest pools in southern New England. Wetlands 22:247–255. doi:10.1672/0277-5212 CrossRefGoogle Scholar
  3. Brooks ML, D’ Antonio CM, Richardson DM, Grace JB, Kelley JE, DiTomaso JM, Hobbs RJ, Pellant M, Pyke D (2004) Effects of invasive alien plants on fire regimes. Bioscience 54:677–688. doi:10.1641/0006-3568 CrossRefGoogle Scholar
  4. Brown CJ, Blossey B, Maerz JC, Joule SJ (2006) Invasive plant and experimental venue affect tadpole performance. Biol Invasions 8:327–338. doi:10.1007/s10530-004-8244-x CrossRefGoogle Scholar
  5. Canhoto C, Laranjeira C (2007) Leachates of Eucalyptus globulus in intermittent streams affect water parameters and invertebrates. Int Rev Hydrobiol 92:173–182. doi:10.1002/iroh.200510956 CrossRefGoogle Scholar
  6. Cipollini D, Stevenson R, Enright S, Eyles A, Bonello P (2008) Phenolic metabolites in leaves of the invasive shrub, Lonicera maackii, and their potential phytotoxic and anti-herbivore effects. J Chem Ecol 34:144–152. doi:10.1007/s10886-008-9426-2 CrossRefPubMedGoogle Scholar
  7. Clesceri LS, Greenberg AE, Eaton AD (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, Washington D.C.Google Scholar
  8. Cooke AS (1971) Selective predation by newts on frog tadpoles treated with DDT. Nature 229:275–276CrossRefPubMedGoogle Scholar
  9. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166. doi:10.1034/j.1600-0706.2002.970201.x CrossRefGoogle Scholar
  10. Cutway HB, Ehrenfeld JG (2009) Exotic plant invasions in forested wetlands: effects of adjacent urban land use type. Urban Ecosyst 12:371–390. doi:10.1007/s11252-009-0088-9 CrossRefGoogle Scholar
  11. Dorning M, Cipollini D (2006) Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecol 184:287–296. doi:10.1007/s11258-005-9073-4 CrossRefGoogle Scholar
  12. Harkey GA, Semlitsch RD (1988) Effects of temperature on growth, development, and color polymorphism in the Ornate Chorus Frog, Pseudacris ornata. Copeia 1988:1001–1007CrossRefGoogle Scholar
  13. Hickman CR, Stone MD, Mathis A (2004) Priority use of chemical over visual cues for detection of predators by Graybelly Salamanders, Eurycea multiplicata griseogaster. Herpetologica 60:203–210CrossRefGoogle Scholar
  14. Hutchinson TF, Vankat JL (1997) Invasibility and effects of Amur Honeysuckle in southwestern Ohio forests. Conserv Biol 11:1117–1124CrossRefGoogle Scholar
  15. Kerby JL, Richards-Hrdlicka K, Storfer A, Skelly D (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 CrossRefPubMedGoogle Scholar
  16. Kimbro DL, Grosholz ED, Baukus AJ, Nesbitt NJ, Travis NM, Attoe S, Coleman-Hulbert C (2009) Invasive species cause large-scale loss of native California oyster habitat by disrupting trophic cascades. Oecologia 160:563–575. doi:10.1007/s00442-009-1322-0 CrossRefPubMedGoogle Scholar
  17. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989. doi:10.1111/j.1461-0248.2004.00657.x CrossRefGoogle Scholar
  18. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  19. Maerz JC, Brown CJ, Chapins CT, Blossey B (2005) Can secondary compounds of an invasive plant affect larval amphibians? Funct Ecol 19:970–975. doi:10.1111/j.1365-2435.2005.01054.x CrossRefGoogle Scholar
  20. Mathis A, Murray KL, Hickman CR (2003) Do experience and body size play a role in responses of larval ringed salamanders, Ambystoma annulatum, to predator kairomones? Laboratory and field assays. Ethology 109:159–170CrossRefGoogle Scholar
  21. Moore MK, Townsend VR (1998) The interaction of temperature, dissolved oxygen and predation pressure in an aquatic predator-prey system. Oikos 81:329–336CrossRefGoogle Scholar
  22. Orrock JL, Witter MS, Reichman OJ (2008) Apparent competition with an exotic plant reduces native plant establishment. Ecology 89:1168–1174. doi:10.1890/07-0223.1 CrossRefPubMedGoogle Scholar
  23. Orrock JL, Holt RD, Baskett ML (2010) Refuge-mediated apparent competition in plant-consumer interactions. Ecol Lett 13:11–20. doi:10.1111/j.1461-0248.2009.01412.x CrossRefPubMedGoogle Scholar
  24. Rasband WS (2009) ImageJ. Available at: http://rsb.info.nih.gov/ij US National Institutes of Health, Bethesda
  25. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol. Invasions 1:21–32. doi:10.1023/A:1010086329619 CrossRefGoogle Scholar
  26. Skelly DK (1995) A behavioral trade-off and its consequences for the distribution of Pseudacris treefrog larvae. Ecology 76:150–164. doi:10.2307/1940638 CrossRefGoogle Scholar
  27. Swab RM, Zhang L, Mitsch WJ (2008) Effects of hydrologic restoration and Lonicera maackii removal on herbaceous understory vegetation in a bottomland hardwood forest. Res Ecol 16:453–463. doi:10.1111/j.1526-100X.2007.00315.x CrossRefGoogle Scholar
  28. Temmink JHM, Field JA, van Haastrecht JC, Merkelback RCM (1989) Acute and sub-acute toxicity of bark tannin in carp (Cyprinus carpio L). Water Res 23:341–344CrossRefGoogle Scholar
  29. Ultsch GR, Bradford DF, Feda J (1999) Physiology: coping with the environment. In: McDiarmid RW, Altig R (eds) Tadpoles. The University of Chicago Press, Chicago, pp 189–214Google Scholar
  30. Van Buskirk J (2002) A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. Am Nat 160:87–102. doi:10.1086/340599 CrossRefPubMedGoogle Scholar
  31. Van Buskirk J (2003) Habitat partitioning in European and North American pond-breeding frogs and toads. Divers Distrib 9:399–410. doi:10.1046/j.1472-4642.2003.00038.x CrossRefGoogle Scholar
  32. Wassersug RJ, Feder ME (1983) The effects of aquatic oxygen concentration, body size and respiratory behaviour on the stamina of obligate aquatic (Anaxyrus americanus) and facultative air-breathing (Xenopus laevis and Lithobates berlandieri) anuran larvae. J Exp Biol 105:173–190PubMedGoogle Scholar
  33. Wassersug RJ, Seibert EA (1975) Behavioral responses of amphibian larvae to variation in dissolved oxygen. Copeia 1975:86–103CrossRefGoogle Scholar
  34. Watling JI, Orrock JL (2010) Measuring edge contrast using biotic criteria helps define edge effects on the density of an invasive plant. Landscape Ecol 25:69–78. doi:10.1007/s10980-009-9416-y CrossRefGoogle Scholar
  35. Watling JI, Hickman CR, Orrock JL (2010) Predators and invasive plants affect performance of amphibian larvae. Oikos. doi:10.1111/j.1600-0706.2010.19255.x
  36. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100. doi:10.1890/0012-9658 CrossRefGoogle Scholar
  37. White EM et al (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455. doi:10.1111/j.1366-9516.2006.00265.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • J. I. Watling
    • 1
  • C. R. Hickman
    • 2
  • E. Lee
    • 3
  • K. Wang
    • 3
  • J. L. Orrock
    • 2
  1. 1.Ft Lauderdale Research and Education CenterUniversity of FloridaFt LauderdaleUSA
  2. 2.Department of ZoologyUniversity of WisconsinMadisonUSA
  3. 3.Department of BiologyWashington University in St LouisSt LouisUSA

Personalised recommendations