Skip to main content

Advertisement

SpringerLink
Log in

Scavenging dynamics on Guam and implications for invasive species management

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Deployment of mouse carcasses laced with acetaminophen has become a common management tool to control invasive brown tree snakes (Boiga irregularis; BTS) on Guam. Additionally, anticoagulant rodenticides may be used to control invasive rats (Rattus spp.) if their populations increase due to predator release in the wake of BTS eradication. However, there has been little research examining how scavengers on Guam could be incidentally exposed to toxicants by scavenging carcasses of animals that die from these population control strategies. Furthermore, there is a limited understanding of how the proliferation of invasive species on Guam has influenced the composition of the scavenger community. We investigated these topics by examining scavenger consumption of mouse, rat, and BTS carcasses on Guam in both a coastal and upland site during the wet (May–Aug 2016) and dry season (Jan–Apr 2017). We documented carcass consumption by 9 species, which scavenged 48% of carcasses. Interactions between season, habitat, and carcass type influenced probability of scavenging, and appeared to be driven by consumption by the two main scavenger species, BTS and cane toads (Rhinella marina), both of which are invasive on Guam. Baiting programs should consider the potential for toxin exposure to land crabs (Coenobita spp., Birgus latro), native species that scavenged at every combination of carcass type, habitat, and season. Overall, 60% of scavenging events were attributed to species considered pests that are recent introductions to Guam. Invasive species on Guam are the primary scavengers of small vertebrate carrion, suggesting a substantial role in trophic dynamics that extends beyond predation.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The datasets generated during the current study are included in its supplementary information files.

References

  • Abernethy EF, Turner KL, Beasley JC et al (2016) Carcasses of invasive species are predominantly utilized by invasive scavengers in an island ecosystem. Ecosphere 7:e01496

    Article  Google Scholar 

  • Beasley JC, Olson ZH, DeVault TL (2015) Ecological role of vertebrate scavengers. In: Benbow ME, Tomberlin JK, Tarone AM (eds) Carrion ecology, evolution, and their applications. CRC Press, Boca Raton

    Google Scholar 

  • Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biol Lett 12:20150623

    Article  PubMed  PubMed Central  Google Scholar 

  • Bispo R, Bernardino J, Marques TA et al (2013) Modeling carcass removal time for avian mortality assessment in wind farms using survival analysis. Environ Ecol Stat 20:147–165

    Article  Google Scholar 

  • Blázquez MC, Delibes-Mateos M, Vargas JM et al (2016) Stable isotope evidence for Turkey vulture reliance on food subsidies from the sea. Ecol Indic 63:332–336

    Article  Google Scholar 

  • Brooke MdL, Cuthbert R, Harrison G et al (2013) Persistence of brodifacoum in cockroach and woodlice: implications for secondary poisoning during rodent eradications. Ecotoxicol Environ Saf 97:183–188

    Article  CAS  Google Scholar 

  • Brown MB, Schlacher TA, Schoeman DS et al (2015) Invasive carnivores alter ecological function and enhance complementarity in scavenger assemblages on ocean beaches. Ecology 96:2715–2725

    Article  PubMed  Google Scholar 

  • Bump JK, Peterson RO, Vucetich JA (2009) Wolves modulate soil nutrient heterogeneity and foliar nitrogen by configuring the distribution of ungulate carcasses. Ecology 90:3159–3167

    Article  PubMed  Google Scholar 

  • Butler-Valverde M, DeVault TL, Beasley JC (2022) Trophic interactions at avian carcasses. Do scavengers feed on vulture carrion? Food Webs 31:e00230

    Article  Google Scholar 

  • Clark L, Savarie PJ (2012) Efficacy of aerial broadcast baiting in reducing brown treesnake numbers. Hum Wildl Interact 6:212–221

    Google Scholar 

  • Clark L, Savarie PJ, Shivik JA et al (2012) Efficacy, effort, and cost comparisons of trapping and acetaminophen-baiting for control of brown treesnakes on Guam. Hum Wildl Interact 6:222–236

    Google Scholar 

  • Clark L, Clark C, Siers S (2017) Brown tree snakes: methods and approaches for control. In: Pitt WC, Beasley J, Witmer GW (eds) Ecology and management of terrestrial vertebrate invasive species in the United States. CRC Press, Boca Raton, pp 107–134

    Chapter  Google Scholar 

  • Clergeau P, Yésou P (2006) Behavioural flexibility and numerous potential sources of introduction for the sacred ibis: Causes of concern in western Europe? Biol Invasions 8:1381–1388

    Article  Google Scholar 

  • Courchamp F, Chapuis J-L, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383

    Article  PubMed  Google Scholar 

  • Courchamp F, Hoffmann BD, Russell JC et al (2014) Climate change, sea-level rise, and conservation: keeping island biodiversity afloat. Trends Ecol Evol 29:127–130

    Article  PubMed  Google Scholar 

  • DeVault TL, Krochmal AR (2002) Scavenging by snakes: an examination of the literature. Herpetologica 58:429–436

    Article  Google Scholar 

  • DeVault TL, Rhodes OE Jr (2002) Identification of vertebrate scavengers of small mammal carcasses in a forested landscape. Acta Theriol 47:185–192

    Article  Google Scholar 

  • DeVault TL, Rhodes OE Jr, Shivik JA (2003) Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102:225–234

    Article  Google Scholar 

  • DeVault TL, Brisbin IL, Rhodes OE Jr (2004) Factors influencing the acquisition of rodent carrion by vertebrate scavengers and decomposers. Can J Zool 82:502–509

    Article  Google Scholar 

  • DeVault TL, Olson ZH, Beasley JC et al (2011) Mesopredators dominate competition for carrion in an agricultural landscape. Basic Appl Ecol 12:268–274

    Article  Google Scholar 

  • Doherty TS, Glen AS, Nimmo DG et al (2016) Invasive predators and global biodiversity loss. Proc Natl Acad Sci USA 113:11261–11265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorr BS, Clark CS, Savarie PJ (2016) Aerial application of Acetaminophen-treated baits for control of Brown treesnakes. US Department of Defense, Alexandria

    Google Scholar 

  • Dryden G (1965) The food and feeding habits of Varanus indicus on Guam. Micronesica 2:73–76

    Google Scholar 

  • Engeman RM, Shiels AB, Clark CS (2018) Objectives and integrated approaches for the control of brown tree snakes: an updated overview. J Environ Manag 219:115–124

    Article  Google Scholar 

  • Faegre SK, Nietmann L, Hannon P et al (2020) Age-related differences in diet and foraging behavior of the critically endangered Mariana Crow (Corvus kubaryi), with notes on the predation of Coenobita hermit crabs. J Ornithol 161:149–158

    Article  Google Scholar 

  • Fritts TH, Rodda GH (1998) The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annu Rev Ecol Syst 29:113–140

    Article  Google Scholar 

  • Hill JE, DeVault TL, Beasley JC et al (2018a) Effects of vulture exclusion on carrion consumption by facultative scavengers. Ecol Evol 8:2518–2526

    Article  PubMed  PubMed Central  Google Scholar 

  • Hill JE, DeVault TL, Beasley JC et al (2018b) Roads do not increase carrion use by a vertebrate scavenging community. Sci Rep 8:16331

    Article  PubMed  PubMed Central  Google Scholar 

  • Inger R, Per E, Cox DT et al (2016) Key role in ecosystem functioning of scavengers reliant on a single common species. Sci Rep 6:1–5

    Article  Google Scholar 

  • Invasive Species Specialist Group (2021) Gobal invasive species database. IUCN. http://www.iucngisd.org/gisd/100_worst.php

  • Jędrzejewski W, Jędrzejewska B (1992) Foraging and diet of the red fox Vulpes vulpes in relation to variable food resources in Biatowieza National Park. Pol Ecography 15:212–220

    Article  Google Scholar 

  • Jędrzejewski W, Zalewski A, Jędrzejewska B (1993) Foraging by pine marten Martes martes in telation to food resources in Białowieża National Park, Poland. Acta Theriol 38:405–426

    Article  Google Scholar 

  • Johnston J, Savarie P, Primus T et al (2002) Risk assessment of an acetaminophen baiting program for chemical control of brown tree snakes on Guam: evaluation of baits, snake residues, and potential primary and secondary hazards. Environ Sci Technol 36:3827–3833

    Article  CAS  PubMed  Google Scholar 

  • Lenth R, Singmann H, Love J et al (2019) Package ‘emmeans’

  • Lujan DT, Vice DS, Guerrero JP et al (2010) Rodent eradication on Cocos Island, Guam: integrating wildlife damage management, resort operations, and non-target concerns. In: Proceedings of the vertebrate pest conference

  • Mack RN, Simberloff D, Mark Lonsdale W et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Masuda BM, Fisher P, Jamieson IG (2014) Anticoagulant rodenticide brodifacoum detected in dead nestlings of an insectivorous passerine. N Z J Ecol 38:110–115

    Google Scholar 

  • Moleón M, Sánchez-Zapata JA, Sebastián‐González E et al (2015) Carcass size shapes the structure and functioning of an african scavenging assemblage. Oikos 124:1391–1403

    Article  Google Scholar 

  • Moleón M, Martínez-Carrasco C, Muellerklein OC et al (2017) Carnivore carcasses are avoided by carnivores. J Anim Ecol 86:1179–1191

    Article  PubMed  Google Scholar 

  • Mortensen HS, Dupont YL, Olesen JM (2008) A snake in paradise: disturbance of plant reproduction following extirpation of bird flower-visitors on Guam. Biol Conserv 141:2146–2154

    Article  Google Scholar 

  • Muller BJ, Schwarzkopf L (2018) Relative effectiveness of trapping and hand-capture for controlling invasive cane toads (Rhinella marina). Int J Pest Manag 64:185–192

    Article  CAS  Google Scholar 

  • Muller BJ, Cade BS, Schwarzkopf L (2018) Effects of environmental variables on invasive amphibian activity: using model selection on quantiles for counts. Ecosphere 9:e02067

    Article  Google Scholar 

  • Muñoz-Lozano C, Martín-Vega D, Martínez-Carrasco C et al (2019) Avoidance of carnivore carcasses by vertebrate scavengers enables colonization by a diverse community of carrion insects. PLoS ONE 14:e0221890

    Article  PubMed  PubMed Central  Google Scholar 

  • Nigro KM, Hathaway SA, Wegmann AS et al (2017) Stable isotope analysis as an early monitoring tool for community-scale effects of rat eradication. Restor Ecol 25:1015–1025

    Article  Google Scholar 

  • NOAA (2021) Climate data online. In: National oceanic and atmospheric administration. http://www.ncdc.noaa.gov/cdo-web/datasets. Accessed 4 Jan 2021

  • Olson ZH, Beasley JC, Rhodes OE Jr (2016) Carcass type affects local scavenger guilds more than habitat connectivity. PLoS ONE 11:e0147798

    Article  PubMed  PubMed Central  Google Scholar 

  • Page H, Willason S (1983) Feeding activity patterns and carrion removal by terrestrial hermit crabs at Enewetak Atoll, Marshall Islands. Pac Sci 37:151–155

    Google Scholar 

  • Pain DJ, Brooke MdL, Finnie J et al (2000) Effects of brodifacoum on the land crab of Ascension Island. J Wildl Manag 64:380–387

    Article  Google Scholar 

  • Pimental D (2007) Environmental and economic costs of vertebrate species invasions into the United States. Manag Vertebr Invasive Species 38:1–8

    Google Scholar 

  • Pitt WC, Driscoll LC, Sugihara RT (2011) Efficacy of rodenticide baits for the control of three invasive rodent species in Hawaii. Arch Environ Contam Toxicol 60:533–542

    Article  CAS  PubMed  Google Scholar 

  • Preiszner B, Czeglédi I, Boros G et al (2020) Scavenging behaviour and size-dependent carcass consumption of the black bullhead (Ameiurus melas). J Fish Biol 97:1113–1119

    Article  PubMed  Google Scholar 

  • R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rayner MJ, Hauber ME, Imber MJ et al (2007) Spatial heterogeneity of mesopredator release within an oceanic island system. Proc Natl Acad Sci USA 104:20862–20865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Redd R (2021) raredd/rawr version 1.0.1

  • Reed RN, Bakkegard KA, Desy GE et al (2007) Diet composition of the invasive cane toad (Chaunus marinus) on Rota, Northern Mariana Islands. Pac Conserv Biol 13:219–222

    Article  Google Scholar 

  • Richmond JQ, Wood DA, Stanford JW et al (2015) Testing for multiple invasion routes and source populations for the invasive brown treesnake (Boiga irregularis) on Guam: implications for pest management. Biol Invasions 17:337–349

    Article  Google Scholar 

  • Rodda GH, Savidge JA (2007) Biology and impacts of pacific island invasive species. 2. Boiga irregularis, the brown tree snake (Reptilia: Colubridae) 1. Pac Sci 61:307–324

    Article  Google Scholar 

  • Rodda G, Fritts T, Reichel J (1991) The distributional patterns of reptiles and amphibians in the Mariana Islands. Micronesica 24:195–210

    Google Scholar 

  • Rodda GH, Fritts TH, Conry PJ (1992) Origin and population growth of the brown tree snake, Boiga irregularis, on Guam. Pac Sci 46:46–57

    Google Scholar 

  • Savidge JA (1988) Food habits of Boiga irregularis, an introduced predator on Guam. J Herpetol 22:275–282

    Article  Google Scholar 

  • Schwarzkopf L, Alford RA (2002) Nomadic movement in tropical toads. Oikos 96:492–506

    Article  Google Scholar 

  • Sebastián-González E, Morales‐Reyes Z, Botella F et al (2020) Network structure of vertebrate scavenger assemblages at the global scale: drivers and ecosystem functioning implications. Ecography 43:1143–1155

    Article  Google Scholar 

  • Selva N, Jędrzejewska B, Jędrzejewski W et al (2005) Factors affecting carcass use by a guild of scavengers in european temperate woodland. Can J Zool 83:1590–1601

    Article  Google Scholar 

  • Siers S, Pitt W, Eisemann J et al (2019) In situ evaluation of an automated aerial bait delivery system for landscape-scale control of invasive brown treesnakes on Guam. In: Veitch C, Clout MN, Martin A, Russell JC, West C et al (eds) Island invasives: scaling up to meet the challenge. IUCN, Gland, pp 348–355

    Google Scholar 

  • Siers SR, Goetz SM, Volsteadt RM et al (2021) Evaluating lethal toxicant doses for the largest individuals of an invasive vertebrate predator with indeterminate growth. Manag Biol Invasions 12:476–494

    Article  Google Scholar 

  • Sih A, Bolnick DI, Luttbeg B et al (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621

    Article  Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: Invasional meltdown? Biol Invasions 1:21–32

    Article  Google Scholar 

  • Smith JB, Turner KL, Beasley JC et al (2016) Brown tree snake (Boiga irregularis) population density and carcass locations following exposure to acetaminophen. Ecotoxicology 25:1556–1562

    Article  CAS  PubMed  Google Scholar 

  • Smith JB, Laatsch LJ, Beasley JC (2017) Spatial complexity of carcass location influences vertebrate scavenger efficiency and species composition. Sci Rep 7:1–8

    Article  Google Scholar 

  • Therneau T, Lumley T, Atkinson E et al (2020) Survival: survival analyses. R package version 3-2-3

  • Turner K, Abernethy E, Conner LM et al (2017) Abiotic and biotic factors modulate carrion fate and vertebrate scavenging communities. Ecology 98:2413–2424

    Article  PubMed  Google Scholar 

  • Wegmann A, Howald G, Kropidlowski S et al (2019) No detection of brodifacoum residues in the marine and terrestrial food web three years after rat eradication at Palmyra Atoll, Central Pacific. In: Veitch C, Clout MN, Martin A, Russell JC, West C et al (eds) Island Invasives: scaling up to meet the challenges. IUCN, Gland, pp 600–603

    Google Scholar 

  • Weijola V, Vahtera V, Koch A et al (2020) Taxonomy of micronesian monitors (Reptilia: Squamata: Varanus): endemic status of new species argues for caution in pursuing eradication plans. R Soc Open Sci 7:200092

    Article  PubMed  PubMed Central  Google Scholar 

  • Wikramanayake ED, Dryden G (1988) The reproductive ecology of Varanus indicus on Guam. Herpetologica 44:338–344

    Google Scholar 

  • Wiles GJ (1987) The status of fruit bats on Guam. Pac Sci 41:148–157

    Google Scholar 

  • Wiles GJ, Bart J, Beck RE Jr et al (2003) Impacts of the brown tree snake: patterns of decline and species persistence in Guam’s avifauna. Conserv Biol 17:1350–1360

    Article  Google Scholar 

  • Wilson EE, Wolkovich EM (2011) Scavenging: how carnivores and carrion structure communities. Trends Ecol Evol 26:129–135

    Article  PubMed  Google Scholar 

  • Zhang Z (2016) Parametric regression model for survival data: Weibull regression model as an example. Ann Transl Med 4:1–8

    Article  CAS  Google Scholar 

Download references

Funding

This study was conducted via agreement 14-7439-1097 between the USDA National Research Center and Naval Facilities Engineering Command, Marianas. Funding was also provided by the Department of Energy Office of Environmental Management under Award number DE-EM0004391.

Author information

Authors and Affiliations

  1. Savannah River Ecology Laboratory, University of Georgia, Aiken, SC, USA

    Jacob E. Hill, Kelsey L. Turner, Joshua B. Smith, Matthew T. Hamilton & Travis L. DeVault

  2. Smithsonian Conservation Biology Institute, Smithsonian Institution, Front Royal, VA, USA

    William C. Pitt

  3. Savannah River Ecology Laboratory, Warnell School of Forestry and Natural Resources, University of Georgia, Aiken, SC, USA

    James C. Beasley

  4. Savannah River Ecology Laboratory, Odum School of Ecology, University of Georgia, Aiken, SC, USA

    Olin E. Rhodes Jr.

Authors
  1. Jacob E. Hill
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kelsey L. Turner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joshua B. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matthew T. Hamilton
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Travis L. DeVault
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. William C. Pitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. James C. Beasley
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Olin E. Rhodes Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jacob E. Hill.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 156 KB)

Supplementary file2 (PDF 552 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hill, J.E., Turner, K.L., Smith, J.B. et al. Scavenging dynamics on Guam and implications for invasive species management. Biol Invasions 25, 1845–1858 (2023). https://doi.org/10.1007/s10530-023-03014-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-023-03014-6

Keywords

Search

Navigation