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Invasive fishes in the Hawaiian anchialine ecosystem: investigating potential predator avoidance by endemic organisms

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Abstract

Globally, introductions of alien species are increasingly common, with invasive predators potentially having detrimental effects via predation on native species. However, native prey may avoid predation by adopting new behaviors. To determine whether invasive fish populations consume endemic shrimp in invaded Hawaiian anchialine habitats or if adopted patterns of diel migration prevents predation as previously hypothesized, a total of 183 invasive poeciliids (158 Gambusia affinis and 25 Poecilia reticulata) were collected for gut content analyses from four anchialine sites during wet and dry seasons on the islands of Hawai‘i and Maui. Predation on shrimp was not detected in habitats where they retreat exclusively into the underlying aquifer diurnally and only emerge nocturnally. However, low levels of predation were detected (7/65 fishes, only by Gambusia affinis) at Waianapanapa Cave, Maui, where shrimp retreat into both the aquifer and a cave during the day. Thus, adopted behavioral responses to invasive fishes generally, though not universally, prevent predation on endemic Hawaiian anchialine shrimps. However, non-consumptive effects resulting from behavioral modification of shrimps may have appreciable impacts on the Hawaiian anchialine ecosystem and warrant further study.

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References

  • Ayala, J. R., R. B. Rader, M. C. Belk & G. B. Schaalje, 2007. Ground-truthing the impact of invasive species: spatio-temporal overlap between native least chub and introduced western mosquitofish. Biological Invasions 9: 857–869.

    Article  Google Scholar 

  • Bailey-Brock, J. H. & R. E. Brock, 1993. Feeding, reproduction, and sense organs of the Hawaiian anchialine shrimp Halocaridina rubra (Atyidea). Pacific Science 47: 338–355.

    Google Scholar 

  • Baltz, D. M. & P. B. Moyle, 1993. Invasion resistance to introduced species by a native assemblage of California stream fishes. Ecological Applications 3: 246–255.

    Article  Google Scholar 

  • Banner, A. H. & D. M. Banner, 1960. Contributions to the knowledge of shrimp of the Pacific Ocean. Part VII. On Metabetaeus Borradaile, species from Hawaii. Pacific Science 14: 299–303.

    Google Scholar 

  • Barbour, A. B., M. S. Allen, T. K. Frazer & K. D. Sherman, 2011. Evaluating the potential efficacy of invasive lionfish (Pterois volitans) removals. Plos One 6: e19666.

    Article  PubMed  CAS  Google Scholar 

  • Beard, K. H., E. A. Price & W. C. Pitt, 2009. Biology and impacts of Pacific island invasive species. 5. Eleutherodactylus coqui, the Coqui frog (Anura: Leptodactylidae). Pacific Science 63: 297–316.

    Article  Google Scholar 

  • Bourdeau, P. E., K. L. Pangle & S. D. Peacor, 2011. The invasive predator Bythotrephes induces changes in the vertical distribution of native copepods in Lake Michigan. Biological Invasions 13: 2533–2545.

    Article  Google Scholar 

  • Brock, R. E., 1977. Occurrence and variety of fishes in mixohaline ponds of the Kona, Hawai‘i coast. Copeia 1977: 134–139.

    Article  Google Scholar 

  • Brock, R. E. & A. K. H. Kam, 1997. Biological and water quality characterization of anchialine resources in Kaloko-Honokohau National Historical Park. Cooperative National Park Resources Studies Unit, University of Hawai‘i at Manoa, Honolulu. Univ. Hawai‘i Technical Report 112. 115 pp.

  • Brock, R. E., J. E. Norris, D. A. Ziemann & M. T. Lee, 1987. Characteristics of water quality in anchialine ponds of the Kona, Hawai‘i, coast. Pacific Science 41: 200–208.

    CAS  Google Scholar 

  • Brown, J. S., J. W. Laundré & M. Gurung, 1999. The ecology of fear: optimal foraging, game theory, and trophic interactions. Journal of Mammalogy 80: 385–399.

    Article  Google Scholar 

  • Cameron, A. C. & P. K. Trivedi, 1998. Regression Analysis of Count Data. Cambridge University Press, New York.

    Book  Google Scholar 

  • Capps, K. A., C. B. Turner, M. T. Booth, D. L. Lombardozzi, S. H. Mcart, D. Chai & N. G. Hairston, 2009. Behavioral responses of the endemic shrimp Halocaridina rubra (Malacostraca: Atyidae) to an introduced fish, Gambusia affinis (Actinopterygii: Poeciliidae) and implications for the trophic structure of Hawaiian anchialine ponds. Pacific Science 63: 27–37.

    Article  Google Scholar 

  • Carey, C. C., M. P. Ching, S. M. Collins, A. M. Early, W. W. Fetzer, D. Chai & N. G. Hairston, 2011. Predator-dependent diel migration by Halocaridina rubra shrimp (Malacostraca: Atyidae) in Hawaiian anchialine pools. Aquatic Ecology 45: 35–41.

    Article  CAS  Google Scholar 

  • Chipps, S. R. & J. E. Garvey, 2007. Quantitative assessment of food habits and feeding patterns. In Guy, C. S. & M. L. Brown (eds), Analysis and Interpretation of Freshwater Fisheries Data. American Fisheries Society, Bethesda, Maryland: 473–514.

    Google Scholar 

  • Craft, J. D., A. D. Russ, M. N. Yamamoto, T. Y. Iwai, S. Hau, J. Kahiapo, C. T. Chong, S. Ziegler-Chong, C. Muir, Y. Fujita, D. A. Polhemus, R. A. Kinzie & S. R. Santos, 2008. Islands under islands: the phylogeography and evolution of Halocaridina rubra Holthuis, 1963 (Crustacean: Decapoda: Atyidae) in the Hawaiian archipelago. Limnology and Oceanography 53: 675–689.

    Article  Google Scholar 

  • Cousyn, C., L. De Meester, J. K. Colbourne, L. Brendonck, D. Verschuren & F. Volckaert, 2001. Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proceedings of the National Academy of Sciences of the U.S. A. 98: 6256–6260.

    Article  CAS  Google Scholar 

  • Cox, J. G. & S. L. Lima, 2006. Naiveté and an aquatic-terrestrial dichotomy in the effects of introduced predators. Trends in Ecology Evolution 21: 674–680.

    Article  PubMed  Google Scholar 

  • Culver, S. L. & A. M. Kuris, 1998. The apparent eradication of a locally established introduced marine pest. Biological Invasions 2: 245–253.

    Article  Google Scholar 

  • Dalton, C. M., A. Mokiao-Lee, T. S. Sakihara, M. G. Weber, C. A. Roco, Z. Han, B. Dudley, R. A. MacKenzie & N. G. Hairston Jr., 2012. Density- and trait-mediated top–down effects modify bottom–up control of a highly endemic tropical aquatic food web. Oikos 122: 790–800.

    Article  Google Scholar 

  • Davis, M. A., 2003. Biotic globalization: does competition from introduced species threaten biodiversity? BioScience 53: 481–489.

    Article  Google Scholar 

  • De Grave, S. & T. S. Sakihara, 2011. Further records of the anchialine shrimp, Periclimenes pholeter Holthuis, 1973 (Crustacea, Decapoda, Palaemonidae). Zootaxa 2903: 64–68.

    Google Scholar 

  • Fritts, T. H. & G. H. Rodda, 1998. The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annual Review of Ecology, Evolution, and Systematics 29: 113–140.

    Article  Google Scholar 

  • Holthuis, L. B., 1963. On red coloured shrimps (Decapoda, Caridea) from tropical land-locked saltwater pools. Zoologische Mededelingen 16: 261–279.

    Google Scholar 

  • Holthuis, L. B., 1973. Caridean shrimps found in land-locked saltwater pools at four Indo-West Pacific localities (Sinia Peninsula, Funafuti Atoll, Maui and Hawai‘i islands), with the description of one new genus and four new species. Zoologische verhandelingen 128: 1–48.

    Google Scholar 

  • Kadye, W. T. & A. J. Booth, 2012. Detecting impacts of invasive non-native sharptooth catfish, Clarias gariepinus, within invaded and non-invaded rivers. Biodiversity and Conservation 21: 1997–2015.

    Article  Google Scholar 

  • Kovacs, E. K., M. S. Crowther, J. K. Webb & C. R. Dickman, 2012. Population and behavioural responses of native prey to alien predation. Oecologia 168: 947–957.

    Article  PubMed  Google Scholar 

  • Lê, S., J. Josse & F. Husson, 2008. FactoMineR: an R package for multivariate analysis. Journal of Statistical Software 25: 1–18.

    Google Scholar 

  • Light, T., 2005. Behavioral effects of invaders: alien crayfish and native sculpin in a California stream. Biological Invasions 7: 353–367.

    Article  Google Scholar 

  • Loose, C. J. & P. Dawidowicz, 1994. Trade-offs in diel vertical migration by zooplankton – the costs of predator avoidance. Ecology 75: 2255–2263.

    Article  Google Scholar 

  • Maciolek, J. A. & R. E. Brock, 1974. Aquatic survey for the Kona coast ponds, Hawai‘i Island. Univ. Hawai‘i Sea Grant Advisory Report AR-74-04. 73 pp.

  • Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans, M. Clout & F. A. Bazzaz, 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10: 689–710.

    Article  Google Scholar 

  • MacKenzie, R. A. & G. L. Bruland, 2012. Nekton communities in Hawaiian coastal wetlands: the distribution and abundance of introduced fish species. Estuaries and Coasts 35: 212–226.

    Article  CAS  Google Scholar 

  • Moyle, P. B. & T. Light, 1996. Fish invasions in California: do abiotic factors determine success? Ecology 77: 1666–1670.

    Article  Google Scholar 

  • Ng, P. K. L., 2011. Pele ramseyi, a new genus and new species of anchialine swimming crab (Crustacea: Brachyura: Portunidae) from the Hawaiian Islands. Zootaxa 2737: 34–48.

    Google Scholar 

  • Pangle, K. L., S. D. Peacor & O. E. Johannsson, 2007. Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88: 402–412.

    Article  PubMed  Google Scholar 

  • Peacock, M. M., K. H. Beard, E. M. O’Neil, V. S. Kirchoff & M. B. Peters, 2009. Strong founder effects and low genetic diversity in introduced populations of Coqui frogs. Molecular Ecology 18: 3603–3615.

    Article  PubMed  CAS  Google Scholar 

  • Peacor, S. D. & E. E. Werner, 1997. Trait-mediated indirect interactions in a simple aquatic food web. Ecology 78: 1146–1156.

    Article  Google Scholar 

  • Pejchar, L. & H. Mooney, 2009. Invasive species, ecosystem services and human well-being. Trends in Ecology and Evolution 24: 497–504.

    Article  PubMed  Google Scholar 

  • Peñuelas, J., J. Sardans, J. Llusia, S. M. Owen, J. Silva & Ü. Niinemets, 2010. Higher allocation to low cost chemical defenses in invasive species of Hawaii. Journal of Chemical Ecology 36: 1255–1270.

    Article  PubMed  Google Scholar 

  • Preisser, E. L., D. I. Bolnick & M. F. Benard, 2005. Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86: 501–509.

    Article  Google Scholar 

  • R Core Team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. http://www.R-project.org

  • Reaser, J. K., L. A. Meyerson, Q. Cronk, et al., 2007. Ecological and socioeconomic impacts of invasive alien species in island ecosystems. Environmental Conservation 34: 98–111.

    Article  Google Scholar 

  • Reebs, S. G., 2002. Plasticity of diel and circadian activity rhythms in fishes. Reviews in Fish Biology and Fisheries 12: 349–371.

    Article  Google Scholar 

  • Rhymer, J. M. & D. Simberloff, 1996. Extinction by hybridization and introgression. Annual Review of Ecology, Evolution, and Systematics 27: 83–109.

    Article  Google Scholar 

  • Robertson, D. R. & W. F. Smith-Vaniz, 2008. Rotenone: an essential but demonized tool for assessing marine fish diversity. Bioscience 58: 165–170.

    Article  Google Scholar 

  • Sakihara, T. S., 2012. A diel comparison of the unique faunal assemblage in remote anchialine pools on Hawai‘i Island. Pacific Science 66: 83–96.

    Article  Google Scholar 

  • Salo, P., E. Korpimäki, P. B. Banks, M. Nordström & C. R. Dickman, 2007. Alien predators are more dangerous than native predators to prey populations. Proceedings of the Royal Society B 274: 1237–1243.

    Article  PubMed  Google Scholar 

  • Santos, S. R. & D. A. Weese, 2011. Rocks and clocks: linking geologic history and rates of genetic differentiation in anchialine organisms. Hydrobiologia 677: 54–63.

    Article  Google Scholar 

  • Sih, A., D. I. Bolnick, B. Luttbeg, J. L. Orrock, S. D. Peacor, L. M. Pintor, E. Preisser, J. S. Rehage & J. R. Vonesh, 2010. Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119: 610–621.

    Article  Google Scholar 

  • Simberloff, D. & B. Von Holle, 1999. Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1: 21–32.

    Article  Google Scholar 

  • Sket, B., 1996. The ecology of anchialine caves. Trends in Ecology and Evolution 11: 221–225.

    Article  PubMed  CAS  Google Scholar 

  • Strictar-Pereira, L., A. A. Agostinho & L. C. Gomes, 2010. Cage culture with tilapia induces alteration in the diet of natural fish populations: the case of Auchenipterus osteomystax. Brazil Journal of Biology 70: 1021–1030.

    Article  CAS  Google Scholar 

  • Stone, C. P. & L. L. Loope, 1987. Reducing negative effects of introduced animals on native biotas in Hawaii: what is being done, what needs doing, and the role of national parks. Environmental Conservation 14: 245–258.

    Article  Google Scholar 

  • Strayer, D. L., 2012. Eight questions about invasions and ecosystem functioning. Ecology Letters 15: 1199–1210.

    Article  PubMed  Google Scholar 

  • Titelman, J., L. J. Hansson, T. Nilsen, S. P. Colin & J. H. Costello, 2012. Predator-induced vertical behavior of a ctenophore. Hydrobiologia 690: 181–187.

    Article  Google Scholar 

  • Vitousek, P., L. L. Loope & C. P. Stone, 1987. Introduced species in Hawai‘i. biological effects and opportunities for ecological research. Trends in Ecology and Evolution 2: 224–227.

    Article  PubMed  CAS  Google Scholar 

  • Vitule, J. R. S., C. A. Freire & D. Simberloff, 2009. Introduction of non-native freshwater fish can certainly be bad. Fish and Fisheries 10: 98–108.

    Article  Google Scholar 

  • Wagner, W., D. Herbst & S. Sohmer, 1999. Manual of flowering plants of Hawai‘i. University of Hawai‘i Press, Bishop Museum Press, Honolulu: 1948 pp.

  • Werner, E. E. & D. J. Hall, 1988. Habitat shifts in bluegill: the foraging rate-predation risk trade-off. Ecology 69: 1352–1366.

    Article  Google Scholar 

  • Werner, E. E. & S. D. Peacor, 2003. A review of trait-mediated indirect interactions. Ecology 84: 1083–1100.

    Article  Google Scholar 

  • Wilson, E. E. & D. A. Holway, 2010. Multiple mechanisms underlie displacement of solitary Hawaiian Hymenoptera by an invasive social wasp. Ecology 91: 3294–3302.

    Article  PubMed  CAS  Google Scholar 

  • Woodworth, B. L., C. T. Atkinson, D. A. LaPointe, et al., 2005. Host population persistence in the face of introduced vector-borne diseases: Hawai‘i amakihi and avian malaria. Proceedings of the National Academy of Sciences of the U.S.A. 102: 1531–1536.

    Article  CAS  Google Scholar 

  • Zabala, J., I. Zuberogoitia & J. A. Gonzalez-Oreja, 2010. Estimating costs and outcomes of invasive American mink (Neovison vison) management in continental areas: a framework for evidence based control and eradication. Biological Invasions 12: 2999–3012.

    Article  Google Scholar 

  • Zeileis, A., C. Kleiber & S. Jackman, 2008. Regression models for count data in R. Journal of Statistical Software 27: 1–25.

    Google Scholar 

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Acknowledgments

We thank D. A. Weese and R. A. Kinzie III for generous help and support associated with fieldwork. M. Ramsey assisted and provided comments and photos regarding the study at WC. D. P. German, T. S. DeVries, K. M. Kocot, S. A. Sefick, B. P. Schneid, M. S. Jarrell, and N. Liu provided useful comments on fish gut content analyses. T. D. Steury provided expertise on statistical analyses. Comments from two anonymous reviewers were valuable toward improving this study. Fishes from Pu’uhonua O Hōnaunau National Historical Park were collected in collaboration with the U.S. Geological Survey, with thanks to A. M. D. Brasher and M. Hayes. Site access and collections were conducted under the following scientific permits: State of Hawai‘i Native Invertebrate Research Permit # FHM10-232, PUHO: Scientific Research and Collecting Permit # PUHO-2011-SCI-0001, and MAKA: Kamehameha Schools Permit # 4803. All fishes were handled in accordance with Auburn University IACUC protocols 2010–1746 and 2011–1907 and the experiments conducted in this study comply with current laws of the United States and the State of Hawai‘i. Funding was provided by the National Science Foundation (DEB #0949855) to S.R.S., a Sigma Xi Grant in Aid of Research to J.C.H., and a 2011 P.A.D.I. Foundation Research award (#5089) to J.C.H. This represents contributions #105 and #12 to the Auburn University (AU) Marine Biology Program and Molette Biology Laboratory for Environmental and Climate Change Studies, respectively.

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  1. Department of Biological Sciences and Molette Biology Laboratory for Environmental and Climate Change Studies, Auburn University, 101 Rouse Life Sciences Building, Auburn, AL, 36830, USA

    Justin C. Havird, Jeffrey R. Weeks & Scott R. Santos

  2. Cellular and Molecular Biosciences Program, Auburn University, Auburn, AL, USA

    Justin C. Havird & Scott R. Santos

  3. Division of Aquatic Resources, State of Hawai‘i, 130 Mahalani St., Wailuku, HI, 96793, USA

    Skippy Hau

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  1. Justin C. Havird
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Correspondence to Justin C. Havird.

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10750_2013_1568_MOESM1_ESM.xls

Online Resource 1 Complete record of dietary items of invasive fishes collected from the four anchialine habitats in the study. These data were used to generate the PCAs in Figs. 2 & 3. Abbreviations are as in Fig. 1

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Havird, J.C., Weeks, J.R., Hau, S. et al. Invasive fishes in the Hawaiian anchialine ecosystem: investigating potential predator avoidance by endemic organisms. Hydrobiologia 716, 189–201 (2013). https://doi.org/10.1007/s10750-013-1568-8

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