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Top carnivore decline has cascading effects on scavengers and carrion persistence

Cunningham, Calum X., Johnson, Christopher N., Barmuta, Leon A., Hollings, Tracey, Woehler, Eric J., Jones, Menna E.·2018·Proceedings of the Royal Society B: Biological Sciences
DOI 10.1098/rspb.2018.1582
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Abstract

Top carnivores have suffered widespread global declines, with well-documented effects on mesopredators and herbivores. We know less about how carnivores affect ecosystems through scavenging. Tasmania's top carnivore, the Tasmanian devil (Sarcophilus harrisii) , has suffered severe disease-induced population declines, providing a natural experiment on the role of scavenging in structuring communities. Using remote cameras and experimentally placed carcasses, we show that mesopredators consume more carrion in areas where devils have declined. Carcass consumption by the two native mesopredators was best predicted by competition for carrion, whereas consumption by the invasive mesopredator, the feral cat ( Felis catus ), was better predicted by the landscape-level abundance of devils, suggesting a relaxed landscape of fear where devils are suppressed. Reduced discovery of carcasses by devils was balanced by the increased discovery by mesopredators. Nonetheless, carcasses persisted approximately 2.6-fold longer where devils have declined, highlighting their importance for rapid carrion removal. The major beneficiary of increased carrion availability was the forest raven ( Corvus tasmanicus ). Population trends of ravens increased 2.2-fold from 1998 to 2017, the period of devil decline, but this increase occurred Tasmania-wide, making the cause unclear. This case study provides a little-studied potential mechanism for mesopredator release, with broad relevance to the vast areas of the world that have suffered carnivore declines.

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  • Several studies report a reduction in scavenging efficiency when larger facultative scavengers are excluded.

    “For instance, several studies report a reduction in scavenging efficiency when larger facultative scavengers are excluded [165 -167].”

    From Forensic experiments on animal scavenging: A systematic literature review on what we have and what we need (2023) · cites this paper as [166]

    The ‘Carcass use and carrion cycling’ section reports slower carrion consumption after Tasmanian devil declines and summarizes several studies in which dominant scavengers were absent or excluded. However, its own study concerns a population decline, not experimental exclusion, and several of the exclusion examples involve vultures, which the Introduction identifies as obligate rather than facultative scavengers. (LLM, conf=0.84)

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  1. [2]2. Wilson EE, Wolkovich EM. 2011 Scavenging: how carnivores and carrion structure communities. Trends Ecol. Evol. 26 , 129-135. (doi:10.1016/j.tree.2010. 12.011) · DOI
  2. [3]3. Barton PS, Cunningham SA, Lindenmayer DB, Manning AD. 2013 The role of carrion in maintaining biodiversity and ecological processes in terrestrial ecosystems. Oecologia 171 , 761-772. (doi:10.1007/s00442-012-2460-3) Despite the staggering global declines of some specialized scavengers and large carnivores, little research has investigated the cascading effects of scavenging on food webs. To our knowledge, we report the most detailed evidence to date that declines of specialized scavengers can have cascading effects on carrion acquisition by mesopredators, representing a littlestudied mechanism for mesopredator release. Devils limit carrion acquisition by cats, a previously unexplored mechanism for mesopredator release in cats. This potentially represents a mechanism by which devils could suppress cat populations and indirectly protect small native vertebrate species, one of Australia's most pressing conservation issues [28]. Increased carcass persistence increases the risk of carcass colonization by disease-causing bacteria, which may increase the risk of infection in wildlife and livestock. Some questions remain unanswered, such as whether carrion consumption by mesopredators has cascading effects on prey species, and the implications of top carnivore decline on invertebrate scavengers, decomposition cycles and the spread of disease. In the context of a global trend of generalists replacing specialists [49], our study further emphasizes the importance of managing specialized species that serve key ecological functions. Ethics. This study was conducted in accordance with the University of Tasmania Animal Ethics Committee Permit A15274 and DPIPWE scientific permits TFA15245 and TFA 16161. Data accessibility. Scavenging data are available from the Dryad Digital Repository at: https://doi.org/10.5061/dryad.6d5046c [65]. Bird survey data were used under licence and are available from BirdLife Australia. Authors' contributions. C.X.C., M.E.J. and C.N.J. conceived the ideas and designed the study. C.X.C. conducted the field work, led the writing and analysis. L.A.B. and T.H. provided statistical assistance. E.W. contributed expert guidance regarding the bird surveys. All authors contributed to writing. Competing interests. We declare no competing interests. Funding. Funding was provided by the Australian Research Council (ARC) (DP110103069) and Holsworth Wildlife Research Endowment. C.X.C. is supported by a top-up scholarship from the Save the Tasmanian Devil Appeal, M.J. on an ARC Future Fellowship (FT100100250), C.J. on an ARC Professorial Fellowship (DP110103069), E.W. by BirdLife Tasmania, and T.H. by CEBRA and Arthur Rylah Institute. Acknowledgements. Mike Newman, BirdLife Tasmania and BirdLife Australia facilitated access to bird survey data. Parks and Wildlife staff assisted with field accommodation. For their assistance with fieldwork, we thank Angus McNab, Beccy Abbott, Alex Ford, Rhiannon Mundana, Tiana Pirtle, Cassandra Holt and Hanna Zoldi. Tristan Derham and Mike Newman provided comments on a draft. · DOI
  3. [4]4. Houston DC. 1979 The adaptations of scavengers. In Serengeti: dynamics of an ecosystem (eds ARE Sinclair, MN Griffiths), pp. 263-286. Chicago, IL: University of Chicago Press.
  4. [5]5. DeVault TL, Rhodes JOE, Shivik JA. 2003 Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102 , 225-234. (doi:10.1034/j.1600-0706.2003.12378.x) · DOI
  5. [7]7. Burkepile DE, Parker JD, Woodson CB, Mills HJ, Kubanek J, Sobecky PA, Hay ME. 2006 Chemically mediated competition between microbes and animals: microbes as consumers in food webs. Ecology 87 , 2821-2831. (doi:10.1890/00129658(2006)872821:CMCBMA]2.0.CO;2) · DOI
  6. [10]10. Terborgh J et al. 2001 Ecological meltdown in predator-free forest fragments. Science 294 , 1923-1926. (doi:10.1126/science.1064397) · DOI · Paper page
  7. [12]12. Crooks KR, Soule ´ ME. 1999 Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400 , 563-566. (doi:10.1038/23028) · DOI · Paper page
  8. [13]13. Ritchie EG, Johnson CN. 2009 Predator interactions, mesopredator release and biodiversity conservation. Ecol. Lett. 12 , 982-998. (doi:10.1111/j.1461-0248. 2009.01347.x) · DOI
  9. [14]14. Buechley ER, S ¸ekerciog ˘ lu ÇH. 2016 The avian scavenger crisis: looming extinctions, trophic cascades, and loss of critical ecosystem functions. Biol. Conserv. 198 , 220-228. (doi:10.1016/j.biocon. 2016.04.001) · DOI
  10. [17]17. Moleo ´n M, Sa ´nchez-Zapata JA, Selva N, Dona ´zar JA, Owen-Smith N. 2014 Inter-specific interactions linking predation and scavenging in terrestrial vertebrate assemblages. Biol. Rev. 89 , 1042-1054. (doi:10.1111/brv.12097) · DOI
  11. [18]18. Allen ML, Elbroch LM, Wilmers CC, Wittmer HU. 2014 Trophic facilitation or limitation? Comparative effects of pumas and black bears on the scavenger community. PLoS ONE 9 , e102257. (doi:10.1371/ journal.pone.0102257)
  12. [19]19. Sekercioglu CH. 2006 Increasing awareness of avian ecological function. Trends Ecol. Evol. 21 , 464-471. (doi:10.1016/j.tree.2006.05.007) · DOI
  13. [21]21. Markandya A, Taylor T, Longo A, Murty MN, Murty S, Dhavala K. 2008 Counting the cost of vulture decline: an appraisal of the human health and other benefits of vultures in India. Ecol. Econ. 67 , 194-204. (doi:10.1016/j.ecolecon.2008.04.020) · DOI
  14. [22]22. Vidal D, Anza I, Taggart MA, Pe ´rez-Ramı ´rez E, Crespo E, Hofle U, Mateo R. 2013 Environmental factors influencing the prevalence of a Clostridium botulinum type C/D mosaic strain in nonpermanent Mediterranean wetlands. Appl. Environ. Microbiol. 79 , 4264-4271. (doi:10.1128/aem.01191-13) · DOI
  15. [23]23. Jones ME. 2003 Convergence in ecomorphology and guild structure among marsupial and placental carnivores. In Predators with pouches: the biology of carnivorous marsupials (eds ME Jones, CR Dickman, M Archer), pp. 281-292. Melbourne, Australia: CSIRO Publishing.
  16. [24]24. Hawkins CE et al . 2006 Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii . Biol. Conserv. 131 , 307-324. (doi:10.1016/j.biocon. 2006.04.010) · DOI
  17. [25]25. McCallum H, Tompkins DM, Jones M, Lachish S, Marvanek S, Lazenby B, Hocking G, Wiersma J, Hawkins CE. 2007 Distribution and impacts of Tasmanian devil facial tumor disease. EcoHealth 4 , 318-325. (doi:10.1007/s10393-007-0118-0) · DOI
  18. [26]26. Lazenby BT et al. 2018 Density trends and demographic signals uncover the long-term impact of transmissible cancer in Tasmanian devils. J. Appl. Ecol. 55 , 1368-1379. (doi:10.1111/1365-2664. 13088) · DOI
  19. [27]27. Hollings T, Jones M, Mooney N, McCallum H. 2014 Trophic cascades following the disease-induced decline of an apex predator, the Tasmanian devil. Conserv. Biol. 28 , 63-75. (doi:10.1111/cobi.12152) · DOI
  20. [28]28. Woinarski JCZ, Burbidge AA, Harrison PL. 2015 Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement. Proc. Natl Acad. Sci. USA 112 , 4531-4540. (doi:10.1073/pnas.1417301112) · DOI
  21. [29]29. O'Neil ST, Coates PS, Brussee BE, Jackson PJ, Howe KB, Moser AM, Foster LJ, Delehanty DJ. 2018 Broadscale occurrence of a subsidized avian predator: reducing impacts of ravens on sage-grouse and other sensitive prey. J. Appl. Ecol. 55 , 2641-2652. (doi:10.1111/1365-2664.13249) · DOI
  22. [31]31. Andersen GE, Johnson CN, Barmuta LA, Jones ME. 2017 Dietary partitioning of Australia's two marsupial hypercarnivores, the Tasmanian devil and the spotted-tailed quoll, across their shared distributional range. PLoS ONE 12 , e0188529. (doi:10.1371/journal.pone.0188529) · DOI
  23. [32]32. Hosmer D, Lemeshow S, May S. 2008 Applied survival analysis: regression modeling of time-toevent data , 2nd edn. Hoboken, NJ: Wiley.
  24. [33]33. Lefcheck JS. 2016 piecewiseSEM: piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol. Evol. 7 , 573-579. (doi:10.1111/2041-210X.12512) · DOI
  25. [34]34. Grace JB, Schoolmaster DR, Guntenspergen GR, Little AM, Mitchell BR, Miller KM, Schweiger EW. 2012 Guidelines for a graph-theoretic implementation of structural equation modeling. Ecosphere 3 , 1-44. (doi:10.1890/ES12-00048.1) · DOI
  26. [35]35. Grace JB, Scheiner SM, Schoolmaster DR. 2015 Structural equation modeling: building and evaluating causal models. In Ecological statistics: contemporary theory and application (eds GA Fox, S Negrete-Yanlelevich, VJ Sosa), pp. 168-199. New York, NY: Oxford University Press.
  27. [36]36. Shipley B. 2009 Confirmatory path analysis in a generalized multilevel context. Ecology 90 , 363-368. (doi:10.1890/08-1034.1) · DOI · Paper page
  28. [38]38. Nakagawa S, Schielzeth H. 2013 A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4 , 133-142. (doi:10.1111/j.2041-210x.2012.00261.x) · DOI · Paper page
  29. [42]42. Jones ME, Barmuta LA. 2000 Niche differentiation among sympatric Australian dasyurid carnivores. J. Mammal. 81 , 434-447. (doi:10.1644/15451542(2000)081 , 0434:NDASAD . 2.0.CO;2) · DOI
  30. [43]43. Jones ME, Barmuta LA. 1998 Diet overlap and relative abundance of sympatric dasyurid carnivores: a hypothesis of competition. J. Anim. Ecol. 67 , 410-421. (doi:10.1046/j.1365-2656.1998.00203.x) · DOI
  31. [44]44. Ogada DL, Torchin ME, Kinnaird MF, Ezenwa VO. 2012 Effects of vulture declines on facultative scavengers and potential implications for mammalian disease transmission. Conserv. Biol. 26 , 453-460. (doi:10.1111/j.1523-1739.2012. 01827.x) · DOI
  32. [45]45. Hill JE, DeVault TL, Beasley JC, Rhodes OE, Belant JL. 2018 Effects of vulture exclusion on carrion consumption by facultative scavengers. Ecol. Evol. 8 , 2518-2526. (doi:10.1002/ece3.3840) · DOI
  33. [46]46. Morales-Reyes Z, Sa ´nchez-Zapata JA, Sebastia ´nGonza ´lez E, Botella F, Carrete M, Moleo ´n M. 2017 Scavenging efficiency and red fox abundance in Mediterranean mountains with and without vultures. Acta Oecol. 79 , 81-88. (doi:10.1016/j. actao.2016.12.012) · DOI
  34. [49]49. Clavel J, Julliard R, Devictor V. 2011 Worldwide decline of specialist species: toward a global functional homogenization? Front. Ecol. Environ. 9 , 222-228. (doi:10.1890/080216) · DOI
  35. [50]50. Mateo-Toma ´s P, Olea PP, Moleo ´n M, Selva N, Sa ´nchez-Zapata JA. 2017 Both rare and common species support ecosystem services in scavenger communities. Global Ecol. Biogeogr. 26 , 1459-1470. (doi:10.1111/geb.12673) · DOI
  36. [51]51. Prior KA, Weatherhead PJ. 1991 Competition at the carcass: opportunities for social foraging by turkey vultures in southern Ontario. Can. J. Zool. 69 , 1550-1556. (doi:10.1139/z91-218) · DOI
  37. [52]52. Lazenby BT, Dickman CR. 2013 Patterns of detection and capture are associated with cohabiting predators and prey. PLoS ONE 8 , e0059846. (doi:10. 1371/journal.pone.0059846)
  38. [53]53. Fancourt BA. 2016 Avoiding the subject: the implications of avoidance behaviour for detecting predators. Behav. Ecol. Sociobiol. 70 , 1535-1546. (doi:10.1007/s00265-016-2162-7) · DOI
  39. [54]54. Hollings T, McCallum H, Kreger K, Mooney N, Jones M. 2015 Relaxation of risk-sensitive behaviour of prey following disease-induced decline of an apex predator, the Tasmanian devil. Proc. R. Soc. B 282 , 20150124. (doi:10.1098/ rspb.2015.0124)
  40. [55]55. Corte ´s-Avizanda A, Selva N, Carrete M, Dona ´zar JA. 2009 Effects of carrion resources on herbivore spatial distribution are mediated by facultative scavengers. Basic Appl. Ecol. 10 , 265-272. (doi:10.1016/j.baae. 2008.03.009) · DOI
  41. [57]57. Higgins PJ, Peter JM, Cowling SJ. 2006 Handbook of Australian, New Zealand & Antarctic birds: boatbill to starlings . Melbourne, Australia: Oxford University Press.
  42. [58]58. Hollings T, Jones M, Mooney N, McCallum HI. 2016 Disease-induced decline of an apex predator drives invasive dominated states and threatens biodiversity. Ecology 97 , 394-405. (doi:10.1890/150204.1) · DOI
  43. [59]59. Jones E. 1977 Ecology of the feral cat, Felis catus (L.), (Carnivora:Felidae) on Macquarie Island. Wildl. Res. 4 , 249-262. (doi:10.1071/WR9770249) · DOI
  44. [12]12. cascades: is mesopredator release of feral cats inhibiting recovery of the eastern quoll? PLoS ONE 10 , e0119303. (doi:10.1371/journal.pone.0119303) · DOI
  45. [62]62. Glen AS, Dickman CR. 2008 Niche overlap between marsupial and eutherian carnivores: does competition threaten the endangered spotted-tailed quoll? J. Appl. Ecol. 45 , 700-707. (doi:10.1111/j. 1365-2664.2007.01449.x) · DOI
  46. [63]63. Turner KL, Abernethy EF, Mike Conner L, Rhodes OE, Beasley JC. 2017 Abiotic and biotic factors modulate carrion fate and vertebrate scavenging communities. Ecology 98 , 2413-2424. (doi:10.1002/ecy.1930) · DOI

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Authors
Cunningham, C. X., Johnson, C. N., Barmuta, L. A., Hollings, T., Woehler, E. J., & Jones, M. E.
Affiliations
  • School of Natural Sciences, University of Tasmania, Hobart, Tasmania 7001, Australia
  • Department of Environment, Land, Water and Planning, Arthur Rylah Institute for Environmental Research, Heidelberg, Victoria 3084, Australia
  • Birdlife Tasmania, GPO Box 68, Hobart, Tasmania, Australia
ORCID
Venue
Proceedings of the Royal Society B: Biological Sciences
Publisher
The Royal Society
Published
2018-11-28
Volume
285
Issue
1892
ISSN
  • 0962-8452
  • 1471-2954
DOI
10.1098/rspb.2018.1582
Cited by
94
References
3
Language
en
Licence
royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Funders
  • Australian Research Council (DP110103069)
  • ARC Future Fellowship (FT100100250)
  • ARC Professorial Fellowship (DP110103069)

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