Abiotic factors influence the dynamics of marine habitat use by a highly mobile “freshwater” top predator

Abstract

Cross-ecosystem movements of mobile consumers are a primary mechanism by which energy and nutrients are exchanged between disparate ecosystems. While factors influencing variation in bottom–up subsidies between ecosystems have been well studied, much less is known regarding how biotic and abiotic factors influence the dynamics of mobile consumer-driven connectivity. In a literature survey, we found only 14% of studies examined factors contributing to variation in cross-ecosystem marine foraging by freshwater-adapted consumers. Here, we examine the relationships between abiotic factors and cross-ecosystem movements of a highly mobile freshwater-adapted top predator, Alligator mississippiensis (American alligator). As alligators lack physiological adaptations to survive in marine environments, we predict this linkage would be affected by factors that modify the ability to cope with high salinities. Our results reveal that multiple abiotic factors (e.g., relative humidity, temperature, total precipitation) are key explanatory variables of the duration of cross-ecosystem foraging trips by alligators, and that the absence of salt glands does not preclude them from performing long forays into marine environments. More broadly, our results expand our understanding of mobile consumer-driven ecosystem connectivity at the land–sea interface by demonstrating connectivity is highest when physical stressors are relaxed, and access to and availability of resources are maximized.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Alberti, J., A. M. Casariego, P. Daleo, E. Fanjul, B. Silliman, M. Bertness & O. Iribarne, 2010. Abiotic stress mediates top-down and bottom-up control in a Southwestern Atlantic salt marsh. Oecologia 163: 181–191.

    Article  PubMed  Google Scholar 

  2. Barton, K., 2016. MuMIn: Multi-model inference (R package version 1.15.6) [available on internet at https://cran.r-project.org/package=MuMIn].

  3. Bates, D., M. Maechler, B. Bolker & S. Walker, 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1): 1–48.

    Article  Google Scholar 

  4. Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, New York: 515.

    Google Scholar 

  5. Campbell, H. A., M. E. Watts, S. Sullivan, M. A. Read, S. Choukroun, S. R. Irwin & C. E. Franklin, 2010. Estuarine crocodiles ride surface currents to facilitate long-distance travel. The Journal of animal ecology 79: 955–964.

    Article  PubMed  Google Scholar 

  6. Campbell, H. A., R. G. Dwyer, T. R. Irwin & C. E. Franklin, 2013. Home range utilisation and long-range movement of estuarine crocodiles during the breeding and nesting season. PLOS ONE 8(5): e62127.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Carlton, J. & J. Hodder, 2003. Maritime mammals: terrestrial mammals as consumers in marine intertidal communities. Marine Ecology Progress Series 256: 271–286.

    Article  Google Scholar 

  8. Craighead, F. C., 1968. The role of the alligator in shaping plant communities and maintaining wildlife in the southern Everglades. Florida Naturalist 41(67–74): 94.

    Google Scholar 

  9. D’eon, R. G. & D. Delparte, 2005. Effects of radio-collar position and orientation on GPS radio-collar performance, and the implications of PDOP in data screening. Journal of Applied Ecology 42: 383–388.

    Article  Google Scholar 

  10. Davis, J. E., J. R. Spotila & W. C. Schefler, 1980. Evaporative water loss from the American alligator, Alligator mississippiensis: the relative importance of respiratory and cutaneous components and the regulatory role of the skin. Comparative Biochemistry and Physiology Part A: Comparative Physiology 67: 439–446.

    Article  Google Scholar 

  11. Diebel, M., 2003. Morphology of meandering tidal channels on Sapelo Island. A report for Zoology 750-Problems in Oceanography. 19 pp.

  12. Estes, J. A., J. Terborgh, J. S. Brashares, M. E. Power, J. Berger, W. J. Bond, S. R. Carpenter, T. E. Essington, R. D. Holt, J. B. C. Jackson, R. J. Marquis, L. Oksanen, T. Oksanen, R. T. Paine, E. K. Pikitch, W. J. Ripple, S. A. Sandin, M. Scheffer, T. W. Schoener, J. B. Shurin, A. R. E. Sinclair, M. E. Soulé, R. Virtanen & D. A. Wardle, 2011. Trophic downgrading of planet Earth. Science 333: 301–306.

    CAS  Article  PubMed  Google Scholar 

  13. Fish, F. E. & L. A. Cosgrove, 1987. Behavioral thermoregulation of small american alligators in water: postural changes in relation to the thermal environment. Copeia 1987: 804–807.

    Article  Google Scholar 

  14. Fujisaki, I., K. M. Hart, F. J. Mazzotti, M. S. Cherkiss, A. R. Sartain, B. M. Jeffery, J. S. Beauchamp & M. Denton, 2014. Home range and movements of American alligators (Alligator mississippiensis) in an estuary habitat. Animal Biotelemetry 2(1): 1–10.

    Article  Google Scholar 

  15. Fujisaki, I., K. M. Hart, M. S. Cherkiss, F. J. Mazzotti, J. S. Beauchamp, B. M. Jeffery & L. A. Brant, 2016. Spatial and temporal variability in estuary habitat use by American alligators spatial and temporal variability in estuary habitat use by American alligators. Estuaries and Coasts 39(5): 1561–1569.

    CAS  Article  Google Scholar 

  16. Garcia, E. A., M. D. Bertness, J. Alberti & B. R. Silliman, 2011. Crab regulation of cross-ecosystem resource transfer by marine foraging fire ants. Oecologia 166: 1111–1119.

    Article  PubMed  Google Scholar 

  17. GCE-LTER, 2014. Georgia coastal ecosystems long term ecological research: GCE-LTER project data [available on internet at https://gce-lter.marsci.uga.edu/public/data/data.htm].

  18. Gelman, A., & Y. -S. Su, 2016. Arm: Data analysis using regression and multilevel/hierarchical models [available on internet at https://cran.r-project.org/package=arm].

  19. Gelman, A., 2008. Scaling regression inputs by dividing by two standard deviations. Statistics in Medicine 27: 2865–2873.

    Article  PubMed  Google Scholar 

  20. Gitzen, R. A., J. J. Millspaugh & B. J. Kernohan, 2006. Bandwidth selection for fixed-kernel analysis of animal utilization distributions. Journal of Wildlife Management 70: 1334–1344.

    Article  Google Scholar 

  21. Grueber, C. E., S. Nakagawa, R. J. Laws & I. G. Jamieson, 2011. Multimodel inference in ecology and evolution: challenges and solutions. Journal of Evolutionary Biology 24: 699–711.

    CAS  Article  PubMed  Google Scholar 

  22. Huxel, G. R. & K. McCann, 1998. Food web stability: the influence of trophic flows across habitats. The American Naturalist 152: 460–469.

    CAS  Article  PubMed  Google Scholar 

  23. Huxel, G. R., K. McCann & G. Polis, 2002. Effects of partitioning allochthonous and autochthonous resources on food web stability. Ecological Research 17: 419–432.

    Article  Google Scholar 

  24. Jackson, K., D. G. Butler & D. R. Brooks, 1996. Habitat and phylogeny influence salinity discrimination in crocodilians: implications for osmoregulatory physiology and historical biogeography. Biological Journal of the Linnaean Society 58: 371–383.

    Article  Google Scholar 

  25. Jefferies, R. L., 2000. Allochthonous inputs: integrating population changes and food-web dynamics. Trends in Ecology and Evolution 15: 19–22.

    CAS  Article  PubMed  Google Scholar 

  26. Joanen, T. & L. McNease, 1970. A telemetric study of nesting female alligators on Rockefeller Refuge, Louisiana. Proceedings of the Annual Conference of Southeastern Association of Fish and Wildlife Agencies 24: 249–265.

    Google Scholar 

  27. Joanen, T. & L. McNease, 1972. A telemetric study of adult male alligators on Rockefeller Refuge, Louisiana. Proceedings of the Annual Conference of Southeastern Association of Fish and Wildlife Agencies 26: 252–275.

    Google Scholar 

  28. Kay, W. R., 2004. A new method for attaching electronic devices to crocodilians. Herpetological Review 35: 354–357.

    Google Scholar 

  29. Lance, V. A., 2003. Alligator physiology and life history: the importance of temperature. Experimental Gerontology 38: 801–805.

    Article  PubMed  Google Scholar 

  30. Laver, P. N. & M. J. Kelly, 2008. A critical review of home range studies. Journal of Wildlife Management 72(1): 290–298.

    Article  Google Scholar 

  31. Lewis, L. Y. & R. E. Gatten, 1985. Aerobic metabolism of American alligators, Alligator mississippiensis, under standard conditions and during voluntary activity. Comparative Biochemistry and Physiology 80A: 441–447.

    Article  Google Scholar 

  32. Lewis, J. D., J. W. Cain III, & R. Denkhaus, 2014. Home range and habitat selection of an inland alligator (Alligator mississippiensis) population at the northwestern edge of the distribution range. Southeastern Naturalist 13: 261–279.

    Article  Google Scholar 

  33. Lillywhite, H., C. Sheehy & F. Zaidan, 2008. Pitviper scavenging at the intertidal zone: an evolutionary scenario for invasion of the sea. BioScience 58: 947–955.

    Article  Google Scholar 

  34. Lundberg, J. & F. Moberg, 2003. Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems 6: 87–98.

    Article  Google Scholar 

  35. Madden, M., T. R. Jordan, L. Chafin, A. Gaddis, C. Jordan, J. Masour, A. Parker & A. Wahid, 2014. Habitat and Land Cover Map of Sapelo Island, Center for Geospatial Research (CGR). Department of Geography, University of Georgia, Athens.

    Google Scholar 

  36. Mazzotti, F. J. & W. A. Dunson, 1984. Adaptations of Crocodylus acutus and Alligator for life in saline water. Comparative Biochemistry and Physiology Part A: Comparative Physiology 79: 641–646.

    Article  Google Scholar 

  37. Mazzotti, F. J. & W. A. Dunson, 1989. Osmoregulation in crocodilians. American Zoologist 29: 903–920.

    Article  Google Scholar 

  38. McCann, K. S., J. B. Rasmussen & J. Umbanhowar, 2005. The dynamics of spatially coupled food webs. Ecology Letters 8: 513–523.

    CAS  Article  PubMed  Google Scholar 

  39. McCauley, D. & H. Young, 2012. Assessing the effects of large mobile predators on ecosystem connectivity. Ecological Applications 22: 1711–1717.

    Article  PubMed  Google Scholar 

  40. McNease, L. & T. Joanen, 1977. Alligator diets in relation to marsh salinity. Annual Meeting of the Southeastern Association of Game and Fish Commissioners 31: 36–40.

    Google Scholar 

  41. Messel, H., G. C. Vorlicek, G. A. Wells, & W. J. Green, 1981. Monograph 1. Surveys of the tidal systems in the Northern Territory of Australia and their crocodile populations. The Blyth-Cadell River Systems Study and the Status of Crocodylus porosus populations in the tidal waterways of Northern Australia. Pergamon Press, Rushcutters Bay, New South Wales: 454–459.

  42. Messel, H., G. C. Vorlicek, G. A. Wells, & W. J. Green, 1982. Status and dynamics of Crocodylus porosus populations in the tidal waterways of northern Australia. International Union for Conservation of Nature and Natural Resources (IUCN) Publication Supplement Paper: 46 pp.

  43. Nifong, J. C., A. E. Rosenblatt, N. A. Johnson, W. Barichivich, B. R. Silliman & M. R. Heithaus, 2012. American alligator digestion rate of blue crabs and its implications for stomach contents analysis. Copeia 2012: 419–423.

    Article  Google Scholar 

  44. Nifong, J. C., 2016. Living on the edge: trophic ecology of Alligator mississippiensis (American alligator) with access to a shallow estuarine impoundment. Bulletin of the Florida Museum of Natural History 54: 13–49.

    Google Scholar 

  45. Nifong, J. C. & B. R. Silliman, 2013. Impacts of a large-bodied, apex predator (Alligator mississippiensis Daudin 1801) on salt marsh food webs. Journal of Experimental Marine Biology and Ecology 440: 185–191.

    Article  Google Scholar 

  46. Nifong, J. C., C. A. Layman & B. R. Silliman, 2015. Size, sex and individual-level behaviour drive intrapopulation variation in cross-ecosystem foraging of a top-predator. Journal of Animal Ecology 84: 35–48.

    Article  PubMed  Google Scholar 

  47. Peckarsky, B. L., P. A. Abrams, D. I. Bolnick, L. M. Dill, J. H. Grabowski, B. Luttbeg, J. L. Orrock, S. D. Peacor, E. L. Preisser, O. J. Schmitz & G. C. Trussell, 2008. Revisiting the classics: considering non-consumptive effects in textbook examples of predator-prey interactions. Ecology 89: 2416–2425.

    Article  PubMed  Google Scholar 

  48. Polis, G. A., W. B. Anderson & R. D. Holt, 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28: 289–316.

    Article  Google Scholar 

  49. R Core Development Team, 2013. R: A language and environment for statistical computing. [available on intenet at http://www.r-project.org/].

  50. Rootes, W., R. Chabreck, V. Wright & B. Brown, 1991. Growth rates of American alligators in estuarine and palustrine wetlands in Louisiana. Estuaries and Coasts 14: 489–494.

    Article  Google Scholar 

  51. Ross, C. A., & C. H. Ernst, 1994. Alligator mississippiensis (Daudin) American Alligator. Catalogue of American Amphibians and Reptiles 600: 1–14.

    Google Scholar 

  52. Rosenblatt, A. E. & M. R. Heithaus, 2011. Does variation in movement tactics and trophic interactions among American alligators create habitat linkages? The Journal of Animal Ecology 80: 786–798.

    Article  PubMed  Google Scholar 

  53. Rosenblatt, A. E., M. R. Heithaus, M. E. Mather, P. Matich, J. C. Nifong, W. J. Ripple & B. R. Silliman, 2013a. The roles of large top predators in coastal ecosystems new insights from long term ecological research. Oceanography 26: 156–167.

    Article  Google Scholar 

  54. Rosenblatt, A. E., M. R. Heithaus, F. J. Mazzotti, M. Cherkiss & B. M. Jeffery, 2013b. Intra-population variation in activity ranges, diel patterns, movement rates, and habitat use of American alligators in a subtropical estuary. Estuarine, Coastal and Shelf Science 135: 182–190.

    Article  Google Scholar 

  55. Rosenblatt, A. E., J. C. Nifong, M. R. Heithaus, F. J. Mazzotti, M. S. Cherkiss, B. M. Jeffery, R. M. Elsey, R. A. Decker, B. R. Silliman, L. J. Guillette, J. Russell & H. L. Justin, 2015. Factors affecting individual foraging specialization and temporal diet stability across the range of a large “generalist” apex predator. Oecologia 178: 5–16.

    Article  PubMed  Google Scholar 

  56. Schmitz, O. J., J. H. Grabowski, B. L. Peckarsky, E. L. Preisser, G. C. Trussell & J. R. Vonesh, 2008. From individuals to ecosystem function: toward an integration of evolutionary and ecosystem ecology. Ecology 89: 2436–2445.

    Article  PubMed  Google Scholar 

  57. Seaman, D. E., J. J. Millspaugh, B. J. Kernohan, G. C. Brundige, K. Raedeke & R. A. Gitzen, 1999. Effects of sample size on kernel home range estimates. The Journal of Wildlife Management 63(2): 739–747.

    Article  Google Scholar 

  58. Seaman, D. E. & R. A. Powell, 1996. An evaluation of the accuracy of kernel density estimators for home range analysis. Ecology 77(7): 2075–2085.

    Article  Google Scholar 

  59. Silliman, B. R., J. Van De Koppel, M. D. Bertness, L. E. Stanton & I. A. Mendelssohn, 2005. Drought, snails, and large-scale die-off of southern US salt marshes. Science 310: 1803–1806.

    CAS  Article  PubMed  Google Scholar 

  60. Signer, J. & N. Balkenhol, 2015. Reproducible home ranges (rhr): A new, user‐friendly R package for analyses of wildlife telemetry data. Wildlife Society Bulletin 39(2): 358–363 [available on internet at https://cran.r-project.org].

  61. Skaug, H., D. Fournier, B. Bolker, A. Magnusson & A. Nielsen, 2014. Generalized linear mixed models using AD model builder. R Statistical Program [available on internet at https://cran.r-project.org].

  62. Spencer, S. R., G. N. Cameron & R. K. Swihart, 1990. Operationally defining home range: temporal dependence exhibited by hispid cotton rat. Ecology 71(5): 1817–1822.

    Article  Google Scholar 

  63. Tamarack, J. L., 1989. Georgia’s coastal island alligators, variations and habitat and prey availability. Proceedings of the Eighth Working Meeting of the Crocodile Specialist Group: 105–118.

  64. Taplin, L. E., G. C. Grigg, P. Harlow, T. M. Ellis & W. A. Dunson, 1982. Lingual salt glands in Crocodylus acutus and C. johnstoni and their absence from Alligator mississippiensis and Caiman crocodilus. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 149: 43–47.

    Article  Google Scholar 

  65. van de Koppel, J., T. van der Heide, A. H. Altieri, B. K. Eriksson, T. J. Bouma, H. Olff & B. R. Silliman, 2015. Long-distance interactions regulate the structure and resilience of coastal ecosystems. Annual Review of Marine Science 7: 139–158.

    Article  PubMed  Google Scholar 

  66. Venables, W. N. & B. D. Ripley, 2002. Modern Applied Statistics with S. Springer, New York: 497.

    Google Scholar 

  67. White, G. & R. Bennetts, 1996. Analysis of frequency count data using the negative binomial distribution. Ecology 77: 2549–2557.

    Article  Google Scholar 

  68. Whitefield, A. K. & S. J. M. Blaber, 1979. Predation on Striped Mullet (Mugil cephalus) by Crocodylus niloticus at St. Lucia, South Africa. Copeia 1979: 266–269.

    Article  Google Scholar 

  69. Wilkinson, P. M. & W. E. Rhodes, 1992. Nesting habitat of american alligators in coastal South Carolina. Proceedings of the Annual Conference of the Southeast Association of Fish and Wildlife agencies 46: 260–265.

    Google Scholar 

Download references

Acknowledgements

We thank R. Nifong, R. McNolty, M. Hensel, D. Penniman, R. McCarville, C. Conegemi, and C. Letcher for their assistance in field and with data processing. Special thanks are given to R. Nifong, J. Ferguson, and A. Rosenblatt for their comments on statistical analyses and on earlier drafts of this manuscript. This research was conducted under Georgia Department of Natural Resources Special Permits 29-WBH-08-178, 29-WBH-09-56, and 29-WBH-10-33 and University of Florida IACUC protocol 201005071. This research was supported by the Estuarine Reserves Division, Office of Ocean and Coastal Resource Management, National Ocean Service, and National Oceanic and Atmospheric Administration (Award No. NA10NOS4200022). This research was supported in part by the Georgia Coastal Ecosystems LTER Project (NSF Awards OCE-0620959 and OCE-1237140). Lastly, we thank the people of Sapelo Island, Georgia, and the Hog Hammock community for their support during this project.

Author information

Affiliations

Authors

Corresponding author

Correspondence to James C. Nifong.

Additional information

Handling editor: Lee B. Kats

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nifong, J.C., Silliman, B. Abiotic factors influence the dynamics of marine habitat use by a highly mobile “freshwater” top predator. Hydrobiologia 802, 155–174 (2017). https://doi.org/10.1007/s10750-017-3255-7

Download citation

Keywords

  • Alligator mississippiensis
  • Crocodilian
  • Cross-ecosystem movement
  • Ecosystem connectivity
  • GPS–VHF telemetry
  • Mobile consumer
  • Trophic coupling