Delayed insect access alters carrion decomposition and necrophagous insect community assembly

Ecosphere

Volumn 5, Issue 4, 2014, Pages

  Pechal, Jennifer L ^a,d   Benbow, M Eric ^b,e   Crippen, Tawni L ^c   Tarone, Aaron M ^a   Tomberlin, Jeffery K ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF DAYTON   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Carrion; Community assembly; Decomposition ecology; Ephemeral resource; Necrobiome; Necrophagous insects

Indexed keywords

EID: 84900431384     PISSN: None     EISSN: 21508925     Source Type: Journal    
DOI: 10.1890/ES14-00022.1     Document Type: Article

References (63)

1. Barton, P., S. Cunningham, D. Lindenmayer, and A. Manning. 2012. The role of carrion in maintaining biodiversity and ecological processes in terrestrial ecosystems. Oecologia 171:761-772.
2. Barton, P. S., S. A. Cunningham, B. C. T. Macdonald, S. McIntyre, D. B. Lindenmayer, and A. D. Manning. 2013. Species traits predict assemblage dynamics at ephemeral resource patches created by carrion. PLoS ONE 8:e53961.
3. Beasley, J. C., Z. Olson, and T. Devault. 2012. Carrion cycling in food webs: comparisons among terrestrial and marine ecosystems. Oikos 121:1021-1026.
4. Benbow, M., A. Lewis, J. Tomberlin, and J. Pechal. 2013. Seasonal necrophagous insect community assembly during vertebrate carrion decomposition. Journal of Medical Entomology 50:440-450.
5. Biondini, M. E., C. D. Bonham, and E. F. Redente. 1985. Secondary successional patterns in a sagebrush (Artemisia tridentata) community as they relate to soil disturbance and soil biological activity. Vegetation 60:25-36. (Pubitemid 16276876)
6. Braack, L. E. O. 1987. Community dynamics of carrionattendant arthropods in tropical African woodlands. Oecologia 72:402-409.
7. Burkepile, D. E., J. D. Parker, C. B. Woodson, H. J. Mills, J. Kubanek, P. A. Sobecky, and M. E. Hay. 2006. Chemically mediated competition between microbes and animals: microbes as consumers in food webs. Ecology 87:2821-2831. (Pubitemid 44904867)
8. Byrd, J. H., and J. L. Castner. 2001. Forensic entomology: The utility of arthropods in legal investigations. CRC Press, Boca Raton, Florida, USA.
9. Calvignac-Spencer, S., K. Merkel, N. Kutzner, H. Kuhl, C. Boesch, P. M. Kappeler, S. Metzger, G. Schubert, and F. H. Leendertz. 2013. Carrion fly-derived DNA as a tool for comprehensive and cost-effective assessment of mammalian biodiversity. Molecular Ecology 22:915-924.
10. Carter, D. O., D. Yellowlees, and M. Tibbett. 2007. Cadaver decomposition in terrestrial ecosystems. Naturwissenschaften 94:12-24. (Pubitemid 46015990)
11. Chase, J. M. 2010. Stochastic community assembly causes higher biodiversity in more productive environments. Science 328:1388-1391.
12. DeVault, T. L., O. E. Rhodes, and J. A. Shivik. 2003. Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102:225-234. (Pubitemid 36914265)
13. Dickinson, C. H., and G. J. F. Pugh. 1974. Biology of plant litter decomposition. Volume 1. Academic Press.
14. Faul, F., E. Erdfelder, A.-G. Lang, and A. Buchner. 2007. G Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods 39:175-191.
15. Fukami, T., and M. Nakajima. 2011. Community assembly: alternative stable states or alternative transient states? Ecology Letters 14:973-984.
16. Greenberg, B. 1991. Flies as forensic indicators. Journal of Medical Entomology 28:565-577.
17. Hanski, I. 1987. Carrion fly community dynamics: patchiness, seasonality and coexistence. Ecological Entomology 12:257-266.
18. Hartley, S., and B. Shorrocks. 2002. A general framework for the aggregation model of coexistence. Journal of Animal Ecology 71:651-662. (Pubitemid 34842158)
19. Hattenschwiler, S., A. V. Tiunov, and S. Scheu. 2005. Biodiversity and litter decomposition in terrestrial ecosystems. Annual Review of Ecology, Evolution, and Systematics 36:191-218. (Pubitemid 43068856)
20. Hawlena, D., M. S. Strickland, M. A. Bradford, and O. J. Schmitz. 2012. Fear of predation slows plantlitter decomposition. Science 336:1434-1438.
21. Hewadikaram, K. A., and M. L. Goff. 1991. Effect of carcass size on rate of decomposition and arthropod succession patterns. American Journal of Forensic Medicine and Pathology 12:235-240.
22. Hieber, M., and M. O. Gessner. 2002. Contribution of stream detrivores, fungi and bacteria to leaf breakdown based on biomass estimates. Ecology 83:1026-1038. (Pubitemid 36530994)
23. Hocking, M. D., and T. E. Reimchen. 2006. Consumption and distribution of salmon (Oncorhynchus spp.) nutrients and energy by terrestrial flies. Canadian Jounal of Fisheries and Aquatic Sciences 63:2076-2086. (Pubitemid 44757140)
24. Hocking, M., R. Ring, and T. Reimchen. 2009. The ecology of terrestrial invertebrates on Pacific salmon carcasses. Ecological Research 24:1091-1100.
25. Horn, H. S. 1974. The ecology of secondary succession. Annual Review of Ecology and Systematics 5:25-37.
26. Kominoski, J. S., L. B. Marczak, and J. S. Richardson. 2011. Riparian forest composition affects stream litter decomposition despite similar microbial and invertebrate communities. Ecology 92:151-159.
27. Lisi, P. J., and D. E. Schindler. 2011. Spatial variation in timing of marine subsidies influences riparian phenology through a plant-pollinator mutualism. Ecosphere 2:1-14.
28. Longino, J. T., and R. K. Colwell. 1997. Biodiversity assessment using structured inventory: capturing the ant fauna of a tropical rain forest. Ecological Applications 7:1263-1277. (Pubitemid 127447733)
29. Ma, Q., A. Fonseca, W. Liu, A. T. Fields, M. L. Pimsler, A. F. Spindola, A. M. Tarone, T. L. Crippen, J. K. Tomberlin, and T. K. Wood. 2012. Proteus mirabilis interkingdom swarming signals attract blow flies. ISME Journal 6:1356-1366.
30. McCune, B., and J. B. Grace. 2002. Analysis of ecological communities. MjM Software Design, Gleneden Beach, Oregon, USA.
31. Megyesi, M. S., S. P. Nawrocki, and N. H. Haskell. 2005. Using accumulated degree-days to estimate the postmortem interval from decomposed human remains. Journal of Forensic Sciences 50:618-626. (Pubitemid 40627989)
32. Melillo, J. M., J. D. Aber, and J. F. Muratore. 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621-626. (Pubitemid 13283591)
33. Michaud, J. P., and G. Moreau. 2011. A statistical approach based on accumulated degree-days to predict decomposition-related processes in forensic studies. Journal of Forensic Sciences 56:229-232.
34. Michaud, J.-P., K. G. Schoenly, and G. Moreau. 2012. Sampling flies or sampling flaws? Experimental design and inference strength in forensic entomology. Journal of Medical Entomology 49:1-10.
35. Norris, K. R. 1965. The bionomics of blow flies. Annual Review of Entomology 10:47-68.
36. Parmenter, R. R., and J. A. MacMahon. 2009. Carrion decomposition and nutrient cycling in a semiarid shrub-steppe ecosystem. Ecological Monographs 79:637-661.
37. Payne, J. A. 1965. A summer carrion study of the baby pig Sus scrofa Linnaeus. Ecology 46:592-602.
38. Pechal, J. L., T. L. Crippen, M. E. Benbow, A. M. Tarone, S. Dowd, and J. K. Tomberlin. 2014. The potential use of bacterial community succession in forensics as described by high throughput metagenomic sequencing. International Journal of Legal Medicine 128:193-205.
39. Pechal, J. L., T. L. Crippen, A. M. Tarone, A. J. Lewis, J. K. Tomberlin, and M. E. Benbow. 2013. Microbial community functional change during vertebrate carrion decomposition. PLoS ONE 8:e79035.
40. Post, W. M., and K. C. Kwon. 2000. Soil carbon sequestration and land-use change: Processes and potential. Global Change Biology 6:317-327. (Pubitemid 30233822)
41. R Development Core Team. 2010. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
42. Reed, H. B., Jr. 1958. A study of dog carcass communities in Tennessee, with special reference to the insects. American Midland Naturalist 59:213-245.
43. Scheiner, S. M. 1992. Measuring pattern diversity. Ecology 73:1860-1867. (Pubitemid 23397228)
44. Schoenly, K. G., N. H. Haskell, R. D. Hall, and J. R. Gbur. 2007. Comparative performance and complementarity of four sampling methods and arthropod preference tests from human and porcine remains at the forensic anthropology center in Knoxville, Tennessee. Journal of Medical Entomology 44:881-894. (Pubitemid 47442069)
45. Schoenly, K., and W. Reid. 1987. Dynamics of heterotrophic succession in carrion arthropod assemblages: discrete seres or a continuum of change? Oecologia 73:192-202.
46. Simmons, T., P. A. Cross, R. E. Adlam, and C. Moffatt. 2010. The influence of insects on decomposition rate in buried and surface remains. Journal of Forensic Sciences 55:889-892.
47. Sivakumar, M. V. K., R. P. Motha, D. A. Wilhite, and J. J. Qu, editors. 2011. Proceedings of an Expert Meeting on the Preparation of a Compendium on National Drought Policy. World Meteorological Organization, Washington, D.C., USA.
48. Smith, C. R., and A. R. Baco. 2003. Ecology of whale falls at the deep-sea floor. Oceanography and Marine Biology: an Annual Review 41:311-354.
49. Srivastava, D. S., B. J. Cardinale, A. L. Downing, J. E. Duffy, C. Jouseau, M. Sankaran, and J. P. Wright. 2009. Diversity has stronger top-down than bottom-up effects on decomposition. Ecology 90:1073-1083.
50. Strickland, M. S., C. Lauber, N. Fierer, and M. A. Bradford. 2009. Testing the functional significance of microbial community composition. Ecology 90:441-451.
51. Tack, A. J. M., S. Gripenberg, and T. Roslin. 2012. Cross-kingdom interactions matter: fungal-mediated interactions structure an insect community on oak. Ecology Letters 15:177-185.
52. Tomberlin, J. K., T. L. Crippen, A. M. Tarone, B. Singh, K. Adams, Y. H. Rezenom, M. E. Benbow, M. Flores, M. Longnecker, J. L. Pechal, D. H. Russell, R. C. Beier, and T. K. Wood. 2012. Interkingdom responses of flies to bacteria mediated by fly physiology and bacterial quorum sensing. Animal Behaviour 84:1449-1456.
53. Tomberlin, J. K., R. Mohr, M. E. Benbow, A. M. Tarone, and S. VanLaerhoven. 2011. A roadmap for bridging basic and applied research in forensic entomology. Annual Review of Entomology 56:401-421.
54. Towne, E. G. 2000. Prairie vegetation and soil nutrient responses to ungulate carcasses. Oecologia 122:232-239. (Pubitemid 30096242)
55. Triplehorn, C. A., and N. F. Johnson. 2005. Borror and DeLong's introduction to the study of insects. Seventh edition. Thomas Brooks/Cole, Belmont, California, USA.
56. Vass, A. A. 2001. Beyond the grave-understanding human decomposition. Microbiology Today 28:190-192.
57. Villet, M. H. 2011. African carrion ecosystsms and their insect communities in relation to forensic entomology. Pest Technology 5:1-15.
58. Whittaker, R. H. 1960. Vegetation of the Siskiyou Mountains, Oregon and California. Ecological Monographs 30:279-338.
59. Whitworth, T. 2006. Keys to the genera and species of blow flies (Diptera : Calliphoridae) of America North of Mexico. Proceedings of the Entomological Society of Washington 108:689-725. (Pubitemid 44081628)
60. Wilson, E. E., and E. M. Wolkovich. 2011. Scavenging: how carnivores and carrion structure communities. Trends in Ecology & Evolution 26:129-135.
61. Woodward, G., M. O. Gessner, P. S. Giller, V. Gulis, S. Hladyz, A. Lecerf, B. Malmqvist, B. G. McKie, S. D. Tiegs, H. Cariss, M. Dobson, A. Elosegi, V. Ferreira, M. A. S. Gra̧ca, T. Fleituch, J. O. Lacoursière, M. Nistorescu, J. Pozo, G. Risnoveanu, M. Schindler, A. Vadineanu, L. B.-M. Vought, and E. Chauvet. 2012. Continental-scale effects of nutrient pollution on stream ecosystem functioning. Science 336:1438-1440.
62. Yang, L. H., J. L. Bastow, K. O. Spence, and A. N. Wright. 2008. What can we learn from resource pulses? Ecology 89:621-634. (Pubitemid 351549999)
63. Zak, J. C., M. R. Willig, D. L. Moorhead, and H. G. Wildman. 1994. Functional diversity of microbial communities: A quantitative approach. Soil Biology and Biochemistry 26:1101-1108. (Pubitemid 2124877)