Advertisement

Biological Invasions

, Volume 19, Issue 3, pp 1001–1013 | Cite as

Different prey resources suggest little competition between non-native frogs and insectivorous birds despite isotopic niche overlap

  • Robyn L. Smith
  • Karen H. Beard
  • Aaron B. Shiels
Original Paper

Abstract

Non-native amphibians often compete with native amphibians in their introduced range, but their competitive effects on other vertebrates are less well known. The Puerto Rican coqui frog (Eleutherodactylus coqui) has colonized the island of Hawaii, and has been hypothesized to compete with insectivorous birds and bats. To address if the coqui could compete with these vertebrates, we used stable isotope analyses to compare the trophic position and isotopic niche overlap between the coqui, three insectivorous bird species, and the Hawaiian hoary bat. Coquis shared similar trophic position to Hawaii amakihi, Japanese white-eye, and red-billed leiothrix. Coquis were about 3 ‰ less enriched in δ15N than the Hawaiian hoary bat, suggesting the bats feed at a higher trophic level than coquis. Analyses of potential diet sources between coquis and each of the three bird species indicate that there was more dietary overlap between bird species than any of the birds and the coqui. Results suggest that Acari, Amphipoda, and Blattodea made up >90% of coqui diet, while Araneae made up only 2% of coqui diet, but approximately 25% of amakihi and white-eye diet. The three bird species shared similar proportions of Lepidoptera larvae, which were ~25% of their diet. Results suggest that coquis share few food resources with insectivorous birds, but occupy a similar trophic position, which could indicate weak competition. However, resource competition may not be the only way coquis impact insectivorous birds, and future research should examine whether coqui invasions are associated with changes in bird abundance.

Keywords

Stable isotope analyses 1315Hawaiian Islands Non-native amphibians 

Notes

Acknowledgements

USDA APHIS National Wildlife Research Center provided funding. This research was supported by the Utah Agricultural Experiment Station, Utah State University, and approved as journal paper number 8900. We thank A. Wallis and A. Crusoe for assistance collecting samples in Hawaii, B. Mossman for laboratory assistance and insect identification, and H. Coad for bat sample preparation. This research was conducted under USU’s IACUC permit # 2371, USFWS permit MB37092B-0, Hawaii Protected Wildlife permit WL14-07, a DOFAW insect collection permit, and a NARS scientific research access permit. We thank P. Banko and two anonymous reviewers for useful commentary on an earlier version of this manuscript.

Supplementary material

10530_2016_1333_MOESM1_ESM.docx (123 kb)
Supplementary material 1 (DOCX 123 kb)

References

  1. Baldwin PH (1953) Annual cycle, environment and evolution in the Hawaiian honeycreepers (Aves: Drepaniidae). Univ Calif Publ Zool 52:285–398Google Scholar
  2. Banko PC, Banko WE (2009) Evolution and ecology of food exploitation. In: Pratt TK, Atkinson CT, Banko PC, Jacobi JD, Woodworth BL (eds) Conservation biology of Hawaiian forest birds: implications for Island Avifauna. Yale University Press, New Haven, pp 159–193Google Scholar
  3. Banko PC, Peck RW, Yelenick SG, Paxton EH, Bonaccorso FK, Montoya-Aiona K, Foote D (2014) Dynamics and ecological consequences of the 2013–2014 koa moth outbreak at Hakalau forest national wildlife refuge. Hawaii Cooperative Studies Unit Technical Report HCSU-058. University of Hawaii Hilo, HIGoogle Scholar
  4. Banko PC, Peck RW, Brinck KW, Leonard DL (2015) Richness, diversity, and similarity of arthropod prey consumed by a community of Hawaiian forest birds. Hawaii Cooperative Studies Unit Technical Report HCSU-066. University of Hawaii Hilo, HIGoogle Scholar
  5. Beard KH (2007) Diet of the invasive frog, Eleutherodactylus coqui, in Hawaii. Copeia 2:281–291CrossRefGoogle Scholar
  6. Beard KH, O’Neill EM (2005) Infection of an invasive frog Eleutherodactylus coqui by the chytrid fungus Batrachochytrium dendrobatidis in Hawaii. Biol Conserv 126:591–595. doi: 10.1016/j.biocon.2005.07.004 CrossRefGoogle Scholar
  7. Beard KH, Pitt WC (2005) Potential consequences of the coqui frog invasion in Hawaii. Divers Distrib 11:427–433. doi: 10.1111/j.1366-9516.2005.00178.x CrossRefGoogle Scholar
  8. Beard KH, Pitt WC (2006) Potential predators of an invasive frog (Eleutherodactylus coqui) in Hawaiian forests. J Trop Ecol 22:345. doi: 10.1017/s0266467406003154 CrossRefGoogle Scholar
  9. Beard KH, Al-Chokhachy R, Tuttle NC, O’Neill EM (2008) Population density estimates and growth rates of Eleutherodactylus coqui in Hawaii. J Herpetol 42:626–636CrossRefGoogle Scholar
  10. Beard K, Pitt WC, Price EA (2009) Biology and impacts of Pacific island invasive species. 5. Eleutherodactylus coqui, the coqui frog (Anura: Leptodactylidae). Pac Sci 63:297–316CrossRefGoogle Scholar
  11. Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458CrossRefPubMedGoogle Scholar
  12. Bearhop S, Adams CE, Waldron S, Fuller R, Macleod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012CrossRefGoogle Scholar
  13. Beaulieu M, Sockman KW (2012) One meadow for two sparrows: resource partitioning in a high elevation habitat. Oecologia 170:529–540. doi: 10.1007/s00442-012-2327-7 CrossRefPubMedGoogle Scholar
  14. Bernard RF, Mautz WJ (2016) Dietary overlap between the invasive coqui frog (Eleutherodactylus coqui) and the Hawaiian hoary bat (Lasiurus cinereus semotus) on the Island of Hawai’i. Biol Invasions. doi: 10.1007/s10530-016-1232-0 Google Scholar
  15. Bisrat SA, White MA, Beard KH, Richard Cutler D (2012) Predicting the distribution potential of an invasive frog using remotely sensed data in Hawaii. Divers Distrib 18:648–660. doi: 10.1111/j.1472-4642.2011.00867.x CrossRefGoogle Scholar
  16. Boland CRJ (2004) Introduced cane toads Bufo marinus are active nest predators and competitors of rainbow bee-eaters Merops ornatus: observational and experimental evidence. Biol Conserv 120:53–62. doi: 10.1016/j.biocon.2004.01.025 CrossRefGoogle Scholar
  17. Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023CrossRefPubMedGoogle Scholar
  18. Bontempo L et al (2014) Comparison of methods for stable isotope ratio (δ13C, δ15N, δ2H, δ18O) measurements of feathers. Methods Ecol Evol 5:363–371. doi: 10.1111/2041-210x.12165 CrossRefGoogle Scholar
  19. Camp RJ, Gorresen PM, Pratt TK, Woodworth BL (2009) Population trends of native Hawaiian forest birds, 1976–2008: the data and statistical analyses. Hawai`i Cooperative Studies Unit Technical Report HCSU-012. University of Hawaii, Hilo, HIGoogle Scholar
  20. Cardwell JP (1996) The evolution of myrmecophagy and its correlates in poison frogs (Family Dendrobatidae). J Zool 240:75–101CrossRefGoogle Scholar
  21. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453. doi: 10.1111/j.1365-2664.2009.01620.x CrossRefGoogle Scholar
  22. Choi RT, Beard KH (2012) Coqui frog invasions change invertebrate communities in Hawaii. Biol Invasions 14:939–948. doi: 10.1007/s10530-011-0127-3 CrossRefGoogle Scholar
  23. Christy MT, Savidge JA, Rodda GH (2007) Multiple pathways for invasion of anurans on a Pacific island. Divers Distrib 13:598–607. doi: 10.1111/j.1472-4642.2007.00378.x CrossRefGoogle Scholar
  24. Cloyed CS, Newsome SD, Eason PK (2015) Trophic discrimination factors and incorporation rates of carbon- and nitrogen-stable isotopes in adult green frogs, Lithobates clamitans. Physiol Biochem Zool 88:576–585CrossRefPubMedGoogle Scholar
  25. del Hoyo J, Elliott A, Christie DA (2008) Handbook of the birds of the world, vol 13. Lynx Edicions, SpainGoogle Scholar
  26. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351CrossRefGoogle Scholar
  27. Foster JT (2009) The history and impact of introduced birds. In: Pratt TK, Atkinson CT, Banko PC, Jacobi JD, Woodworth BL (eds) Conservation biology of Hawaiian forest birds: implications for island avifauna. Yale University Press, New Haven, pp 312–330Google Scholar
  28. Freed LA, Cann RL (2009) Negative effects of an introduced bird species on growth and survival in a native bird community. Curr Biol 19:1736–1740. doi: 10.1016/j.cub.2009.08.044 CrossRefPubMedGoogle Scholar
  29. Freed LA, Cann RL (2012) Changes in timing, duration, and symmetry of molt of Hawaiian forest birds. PLoS ONE 7:e29834. doi: 10.1371/journal.pone.0029834.g001 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Fry B (2006) Stable isotope ecology. Springer Science + Business Media, LLC, New YorkCrossRefGoogle Scholar
  31. Gavrilchuk K, Lesage V, Ramp C, Sears R, Berube M, Bearhop S, Beauplet G (2014) Trophic niche partitioning among sympatric baleen whale species following the collapse of groundfish stocks in the Northwest Atlantic. Mar Ecol Prog Ser 497:285–301. doi: 10.3354/meps10578 CrossRefGoogle Scholar
  32. Giambelluca TW et al (2013) Online rainfall atlas of Hawai’i. Bull Am Meteor Soc 94:313–316. doi: 10.1175/bams-d-11-00228 CrossRefGoogle Scholar
  33. Greenlees MJ, Brown GP, Webb JK, Phillips BL, Shine R (2006) Effects of an invasive anuran the cane toad (Bufo marinus) on the invertebrate fauna of a tropical Australian floodplain. Anim Conserv 9:431–438. doi: 10.1111/j.1469-1795.2006.00057.x CrossRefGoogle Scholar
  34. Gruner DS (2004) Attenuation of top-down and bottom-up forces in a complex terrestrial community. Ecology 85:3010–3022CrossRefGoogle Scholar
  35. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—stable isotope bayesian ellipses in R. J Anim Ecol 80:595–602. doi: 10.1111/j.1365-2656.2011.01806.x CrossRefPubMedGoogle Scholar
  36. Jacobs DS (1994) Distribution and abundance of the endangered Hawaiian hoary bat, Lasiurus cinereus semotus, on the island of Hawai’i. Pac Sci 48:193–200Google Scholar
  37. Jacobs DS (1999) The diet of the insectivorous Hawaiian hoary bat (Lasiurus cinereus semotus) in an open and a cluttered habitat. Can J Zool 77:1603–1608. doi: 10.1139/cjz-77-10-1603 CrossRefGoogle Scholar
  38. Jaeger A, Blanchard P, Richard P, Cherel Y (2009) Using carbon and nitrogen isotopic values of body feathers to infer inter- and intra-individual variations of seabird feeding ecology during moult. Mar Biol 156:1233–1240. doi: 10.1007/s00227-009-1165-6 CrossRefGoogle Scholar
  39. Krab EJ, Van Logtestijn RSP, Cornelissen JHC, Berg MP (2012) Reservations about preservations: storage methods affect δ13C signatures differently even in closely related soil fauna. Methods Ecol Evol 3:138–144. doi: 10.1111/j.2041-210X.2011.00126.x CrossRefGoogle Scholar
  40. Kraus F (2009) Alien reptiles and amphibians: a scientific compendium and analysis, vol 4, 1st edn., Invading nature—Springer series in invasion ecology. Springer, The Netherlands. doi: 10.1007/978-1-4020-8946-6
  41. Kraus F (2015) Impacts from invasive reptiles and amphibians. Annu Rev Ecol Evol Syst 46:75–97. doi: 10.1146/annurev-ecolsys-112414-054450 CrossRefGoogle Scholar
  42. Kraus F, Campbell EW, Allison A, Pratt T (1999) Eleutherodactylus frog introductions to Hawaii. Herpetol Rev 30:21–25Google Scholar
  43. Kraus F, Medeiros A, Preston D, Jarnevich CS, Rodda GH (2012) Diet and conservation implications of an invasive chameleon, Chamaeleo jacksonii (Squamata: Chamaeleonidae) in Hawaii. Biol Invasions 14:579–593. doi: 10.1007/s10530-011-0099-3 CrossRefGoogle Scholar
  44. Kupferberg SJ (1997) Bullfrog (Rana catesbeiana) invasion of a California river: the role of larval competition. Ecology 78:1736–1751CrossRefGoogle Scholar
  45. LaPointe DA, Atkinson CT, Jarvi SI (2009) Managing disease. In: Pratt TK, Atkinson CT, Banko PC, Jacobi JD, Woodworth BL (eds) Conservation biology of Hawaiian forest birds: implications for island avifauna. Yale University Press, New Haven, pp 405–424Google Scholar
  46. Layman CA, Arrington DA, Montana CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48. doi: 10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2 CrossRefPubMedGoogle Scholar
  47. Menard T (2001) Activity patterns of the Hawaiian hoary bat (Lasiurus cinereus semotus) in relation to reproductive time periods. M.S. Thesis. University of Hawaii, ManoaGoogle Scholar
  48. Mountainspring S, Scott JM (1985) Interspecific competition among Hawaiian forest birds. Ecol Monogr 55:219–239CrossRefGoogle Scholar
  49. Olson CA, Beard KH (2012) Diet of the introduced greenhouse frog in Hawaii. Copeia 1:121–129. doi: 10.1643/ce-11-008 CrossRefGoogle Scholar
  50. Olson CA, Beard KH, Koons DN, Pitt WC (2012) Detection probabilities of two introduced frogs in Hawaii: implications for assessing non-native species distributions. Biol Invasions 14:889–900. doi: 10.1007/s10530-011-0125-5 CrossRefGoogle Scholar
  51. Paez-Rosas D, Rodriguez-Perez M, Riofrio-Lazo M (2014) Competition influence in the segregation of the trophic niche of otariids: a case study using isotopic Bayesian mixing models in Galapagos pinnipeds. Rapid Commun Mass Spectrom 28:2550–2558. doi: 10.1002/rcm.7047 CrossRefPubMedGoogle Scholar
  52. Parnell AC, Jackson AL (2013) siar: stable isotope analysis in R. vol R package version 4.2. http://cran.r-project.org
  53. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672. doi: 10.1371/journal.pone.0009672 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Phillips DL, Koch PL (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125. doi: 10.1007/s004420100786 CrossRefGoogle Scholar
  55. Phillips BL, Brown GP, Greenlees M, Webb JK, Shine R (2007) Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia. Austral Ecol 32:169–176. doi: 10.1111/j.1442-9993.2007.01664.x CrossRefGoogle Scholar
  56. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  57. Richter-Boix A, Garriga N, Montori A, Franch M, San Sebastián O, Villero D, Llorente GA (2012) Effects of the non-native amphibian species Discoglossus pictus on the recipient amphibian community: niche overlap, competition and community organization. Biol Invasions 15:799–815. doi: 10.1007/s10530-012-0328-4 CrossRefGoogle Scholar
  58. Roswag A, Becker NI, Encarnacao JA (2015) Isotopic discrimination and indications for turnover in hair and wing membranes of the temperate bat Nyctalus noctula. Eur J Wildl Res 61:703–709. doi: 10.1007/s10344-015-0944-2 CrossRefGoogle Scholar
  59. Sax DF, Gaines SD (2008) Species invasions and extinction: the future of native biodiversity on islands. Proc Natl Acad Sci USA 105:11490–11497. doi: 10.1073/pnas.0802290105 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Scott JM, Mountainspring S, Ramsey FL, Kepler CB (1986) Forest bird communities of the Hawaiian Islands: their dynamics, ecology, and conservation. Stud Avian Biol 9:1–431Google Scholar
  61. Shiels AB, Flores CA, Khamsing A, Krushelnycky PD, Mosher SM, Drake DR (2013) Dietary niche differentiation among three species of invasive rodents (Rattus rattus, R. exulans, Mus musculus). Biol Invasions 15:1037–1048. doi: 10.1007/s10530-012-0348-0 CrossRefGoogle Scholar
  62. Shine R, Amiel J, Munn AJ, Stewart M, Vyssotski AL, Lesku JA (2015) Is “cooling then freezing” a humane way to kill amphibians and reptiles? Biol Open. doi: 10.1242/bio.012179 PubMedPubMedCentralGoogle Scholar
  63. Sin H, Beard KH, Pitt WC (2008) An invasive frog, Eleutherodactylus coqui, increases new leaf production and leaf litter decomposition rates through nutrient cycling in Hawaii. Biol Invasions 10:335–345. doi: 10.1007/s10530-007-9133-x CrossRefGoogle Scholar
  64. Smith KG (2005) Effects of nonindigenous tadpoles on native tadpoles in Florida: evidence of competition. Biol Conserv 123:433–441. doi: 10.1016/j.biocon.2005.01.005 CrossRefGoogle Scholar
  65. Spotswood EN et al (2012) How safe is mist netting? Evaluating the risk of injury and mortality to birds. Methods Ecol Evol 3:29–38. doi: 10.1111/j.2041-210X.2011.00123.x CrossRefGoogle Scholar
  66. Stewart MM, Woolbright LL (1996) Amphibians. In: Reagan DP, Waide RB (eds) The food web of a tropical rain forest. University of Chicago Press, Chicago, pp 273–320Google Scholar
  67. 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. doi: 10.1126/science.1103538 CrossRefPubMedGoogle Scholar
  68. Turner TF, Collyer ML, Krabbenhoft TJ (2010) A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91:2227–2233. doi: 10.1890/09-1454.1 CrossRefPubMedGoogle Scholar
  69. van Riper SG (2000) Japanese White-eye (Zosterops japonicus). Cornell Lab of Ornithology, IthacaGoogle Scholar
  70. Wallis AC, Smith RL, Beard KH (2016) Temporal foraging patterns of non-native Coqui Frogs (Eleutherodactylus coqui) in Hawaii. J Herpetol 50:582–588. doi: 10.1670/15-170 CrossRefGoogle Scholar
  71. Woolbright LL (2005) A plot-based system of collecting population information on terrestrial breeding frogs. Herpetol Rev 36:139–142Google Scholar
  72. Woolbright LL, Hara AH, Jacobsen CM, Mautz WJ, Benevides FL (2006) Population densities of the coqui, Eleutherodactylus coqui Anura (Leptodactylidae) in newly invaded Hawaii and in native Puerto Rico. J Herpetol 40:122–126CrossRefGoogle Scholar
  73. Zelanko PM, Rice NH, Velinsky DJ (2011) Using carbon and nitrogen stable isotopes to distinguish the locations of feather growth in osprey (Pandion haliaetus). Proc Acad Nat Sci Phila 161:61–72CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Robyn L. Smith
    • 1
  • Karen H. Beard
    • 1
  • Aaron B. Shiels
    • 2
  1. 1.Department of Wildland Resources and the Ecology CenterUtah State UniversityLoganUSA
  2. 2.USDANational Wildlife Research CenterFt. CollinsUSA

Personalised recommendations