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Dung beetles in an avian-dominated island ecosystem: feeding and trophic ecology

Abstract

Globally, dung beetles (Scarabaeidae: Scarabaeinae) are linked to many critical ecosystem processes involving the consumption and breakdown of mammal dung. Endemic New Zealand dung beetles (Canthonini) are an anomaly, occurring at high abundance and low diversity on an island archipelago historically lacking terrestrial mammals, except bats, and instead dominated by birds. Have New Zealand’s dung beetles evolved to specialise on bird dung or carrion, or have they become broad generalist feeders? We test dietary preferences by analysing nitrogen isotope ratios of wild dung beetles and by performing feeding behaviour observations of captive specimens. We also use nitrogen and carbon stable isotopes to determine if the dung beetle Saphobius edwardsi will consume marine-derived carrion. Nitrogen isotope ratios indicated trophic generalism in Saphobius dung beetles and this was supported by behavioural observations where a broad range of food resources were utilised. Alternative food resource use was further illustrated experimentally by nitrogen and carbon stable isotope signatures of S. edwardsi, where individuals provided with decomposed squid had δ15N and δ13C values that had shifted toward values associated with marine diet. Our findings suggest that, in the absence of native mammal dung resources, New Zealand dung beetles have evolved a generalist diet of dung and carrion. This may include marine-derived resources, as provided by the seabird colonies present in New Zealand forests before the arrival of humans. This has probably enabled New Zealand dung beetles to persist in indigenous ecosystems despite the decline of native birds and the introduction of many mammal species.

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References

  • Aitchison J (1986) The statistical analysis of compositional data. Springer, Netherlands

    Book  Google Scholar 

  • Bassett IE, Elliott GP, Walker KJ, Thorpe S, Beggs JR (2014) Are nesting seabirds important determinants of invertebrate community composition on subantarctic Adams Island? Polar Biol 37:1–10

  • Beaver RA (1979) Host specificity of temperate and tropical animals. Nature 281:139–141

    Article  Google Scholar 

  • Bunce M et al (2003) Extreme reversed sexual size dimorphism in the extinct New Zealand moa Dinornis. Nature 425:172–175

    Article  CAS  PubMed  Google Scholar 

  • Bustamante-Sanchez MA, Grez AA, Simonetti JA (2004) Dung decomposition and associated beetles in a fragmented temperate forest. Rev Chile Hist Nat 77:107–120

    Google Scholar 

  • Cambefort Y (1991a) Dung beetles in tropical savannas. In: Cambefort Y, Hanski I (eds) Dung beetle ecology. Princeton University Press, Princeton, pp 156–178

    Google Scholar 

  • Cambefort Y (1991b) From saprophagy to coprophagy. In: Hanski I, Cambefort Y (eds) Dung beetle ecology. Princeton University Press, Princeton, pp 51–68

    Google Scholar 

  • Caut S et al. (2012) Seabird modulations of isotopic nitrogen on islands. PloS ONE 7:e39125

  • Daugherty CH, Gibbs GW, Hitchmough RA (1993) Mega-island or micro-continent? New Zealand and its fauna. Trends Ecol Evol 8:437–442

    Article  CAS  PubMed  Google Scholar 

  • Davis ALV (1996) Community organization of dung beetles (Coleoptera: scarabaeidae): differences in body size and functional group structure between habitats. Afr J Ecol 34:258–275

    Article  Google Scholar 

  • Davis ALV, Scholtz CH (2001) Historical vs. ecological factors influencing global patterns of scarabaeine dung beetle diversity. Divers Distrib 7:161–174

    Article  Google Scholar 

  • Davis AJ, Sutton SL (1997) A dung beetle that feeds on fig: implications for the measurement of species rarity. J Trop Ecol 13:759–766

    Article  Google Scholar 

  • de Wit MJ (2003) Madagascar: heads it’s a continent, tails it’s an Island. Annu Rev Earth Planet Sci 31:213–248

    Article  Google Scholar 

  • Ellis JC (2005) Marine birds on land: a review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecol 181:227–241

    Article  Google Scholar 

  • Fincher GT, Stewart TB, Davis R (1970) Attraction of coprophagous beetles to feces of various animals. J Parasitol 56:378–383

    Article  Google Scholar 

  • Fukami T et al (2006) Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol Lett 9:1299–1307

    Article  PubMed  Google Scholar 

  • Gannes LZ, O’Brien DM, Del Rio CM (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271–1276

    Article  Google Scholar 

  • Gardner-Gee R, Beggs JR (2009) Does the presence of burrowing seabirds increase local invertebrate abundance? NZ Entomol 32:41–47

    Article  Google Scholar 

  • Gibbs G (2010) Do New Zealand invertebrates reflect the dominance of birds in their evolutionary history? NZ J Ecol 34:152–157

    Google Scholar 

  • Gill BD (1991) Dung beetles in tropical American forests. In: Hanski I, Cambefort Y (eds) Dung beetle ecology. Princeton University Press, Princeton, pp 51–68

    Google Scholar 

  • Gratton C, Forbes AE (2006) Changes in delta 13C stable isotopes in multiple tissues of insect predators fed isotopically distinct prey. Oecologia 147:615–624

    Article  PubMed  Google Scholar 

  • Halffter G, Edmonds WD (1982) The nesting behavior of dung beetles (Scarabaeidae): an ecological and evolutive approach. Instituto de Ecología, México

  • Halffter G, Matthews EG (1966) The natural history of dung beetles in the subfamily Scarabaeinae (Coleoptera, Scarabaeidae). Fol Entomol Mex 12–14:1–312

    Google Scholar 

  • Hanski I (1991) The dung insect community. In: Hanski I, Cambefort Y (eds) Dung beetle ecology. Princeton University Press, Princeton

    Chapter  Google Scholar 

  • Hanski I, Cambefort Y (1991a) Competition in dung beetles. In: Hanski I, Cambefort Y (eds) Dung beetle ecology. Princeton University Press, Princeton

    Chapter  Google Scholar 

  • Hanski I, Cambefort Y (1991b) Spatial processes. In: Hanski I, Cambefort Y (eds) Dung beetle ecology. Princeton University Press, Priceton, pp 283–329

    Chapter  Google Scholar 

  • Harding JS, Hawke DJ, Holdaway RN, Winterbourn MJ (2004) Incorporation of marine-derived nutrients from petrel breeding colonies into stream food webs. Freshw Biol 49:576–586

    Article  Google Scholar 

  • Hawke DJ, Holdaway RN (2005) Avian assimilation and dispersal of carbon and nitrogen brought ashore by breeding Westland petrels (Procellaria westlandica): a stable isotope study. J Zool 266:419–426

    Article  Google Scholar 

  • Holdaway RN (1999) Introduced predators and avifaunal extinction in New Zealand. In: MacPhee, RDE (ed) Extinctions in near time—causes, contexts, and consequences. Kluwer, New York, pp 189–238

  • Holdaway RN, Worthy TH, Tennyson AJD (2001) A working list of breeding bird species of the New Zealand region at first human contact. NZ J Zool 28:119–187

    Article  Google Scholar 

  • Holter P, Scholtz CH (2007) What do dung beetles eat? Ecol Entomol 32:690–697

    Article  Google Scholar 

  • Holter P, Scholtz CH, Wardhaugh KG (2002) Dung feeding in adult scarabaeines (tunnellers and endocoprids): even large dung beetles eat small particles. Ecol Entomol 27:169–176

    Article  Google Scholar 

  • Hood-Nowotny R, Knols BGJ (2007) Stable isotope methods in biological and ecological studies of arthropods. Entomol Exp Appl 124:3–16

    Article  CAS  Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314

    Google Scholar 

  • Ikeda H, Kubota K, Kagaya T, Abe T (2007) Flight capabilities and feeding habits of silphine beetles: are flightless species really “carrion beetles”? Ecol Res 22:237–241

    Article  Google Scholar 

  • Imber M (1996) The food of Cook’s Petrel Pterodroma cookii during its breeding season on little barrier island, New Zealand. Emu 96:189–194

    Article  Google Scholar 

  • Innes J, Kelly D, Overton JMC, Gillies C (2010) Predation and other factors currently limiting New Zealand forest birds. NZ J Ecol 34:86–114

    Google Scholar 

  • Jones AG (2010) The ecology of native dung beetles in forests of Auckland, New Zealand. University of Auckland, New Zealand

  • Jones AG, Forgie SA, Scott DJ, Beggs JR (2012) Generalist dung attraction response in a New Zealand dung beetle that evolved with an absence of mammalian herbivores. Ecol Entomol 37:124–133

    Article  Google Scholar 

  • Kabir SMH, Kabir A, Majumder MZR (1990) Relative abundance and species composition of some dung beetles (Coleoptera: scarabaeinae) in Bangladesh. Med Vet Entomol 4:439–443

    Article  CAS  PubMed  Google Scholar 

  • Kasper J, Mumm R, Ruther J (2012) The composition of carcass volatile profiles in relation to storage time and climate conditions. Forensic Sci Int 223:64–71

    Article  CAS  PubMed  Google Scholar 

  • Krab EJ, Van Logtestijn RSP, Cornelissen JHC, Berg MP (2012) Reservations about preservations: storage methods affect δ13C signatures differently even in closely related soil fauna. Methods Ecol Evol 3:138–144

    Article  Google Scholar 

  • Larsen TH, Lopera A, Forsyth A (2006) Extreme trophic and habitat specialization by Peruvian dung beetles (Coleoptera: scarabaeidae: Scarabaeinae). Coleopter Bull 60:315–324

    Article  Google Scholar 

  • Lee WG, Wood JR, Rogers GM (2010) Legacy of avian-dominated plant-herbivore systems in New Zealand. NZ J Ecol 34

  • Markwell TJ, Daugherty CH (2002) Invertebrate and lizard abundance is greater on seabird-inhabited islands than on seabird-free islands in the Marlborough Sounds, New Zealand. Ecoscience 9:293–299

    Google Scholar 

  • McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390

    Article  CAS  Google Scholar 

  • McDowall RM (2008) Process and pattern in the biogeography of New Zealand—a global microcosm? J Biogeogr 35:197–212

    Article  Google Scholar 

  • Mulder CH et al (2009) Direct and indirect effects of rats: does rat eradication restore ecosystem functioning of New Zealand seabird islands? Biol Invasions 11:1671–1688

    Article  Google Scholar 

  • Nichols E, Spector S, Louzada J, Larsen T, Amezquita S, Favila ME (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol Conserv 141:1461–1474

    Article  Google Scholar 

  • Oelbermann K, Scheu S (2010) Trophic guilds of generalist feeders in soil animal communities as indicated by stable isotope analysis (15 N/14 N). Bull Entomol Res 100:511–520

    Article  CAS  PubMed  Google Scholar 

  • Parkes J, Murphy E (2003) Management of introduced mammals in New Zealand. NZ J Zool 30:335–359

    Article  Google Scholar 

  • Petersen H, Luxton M (1982) A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39:288–388

    Article  Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • Pianka ER (1974) Evolutionary ecology. Harper & Row, New York

    Google Scholar 

  • Polis GA, Hurd SD (1996) Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. Am Nat 147:396–423

    Article  Google Scholar 

  • Pollierer MM, Langel R, Scheu S, Maraun M (2009) Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15 N/14 N and 13C/12C). Soil Biol Biochem 41:1221–1226

    Article  CAS  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ridsdill-Smith TJ, Edwards PB (2011) Biological control: ecosystem functions provided by dung beetles ecology and evolution of dung beetles. Wiley, Chichester, pp 245–266

    Book  Google Scholar 

  • Sanchez-Pinero F, Polis GA (2000) Bottom-up dynamics of allochthonous input: direct and indirect effects of seabirds on islands. Ecology 81:3117–3132

    Article  Google Scholar 

  • Scheu S, Falca M (2000) The soil food web of two beech forests (Fagus sylvatica) of contrasting humus type: stable isotope analysis of a macro- and a mesofauna-dominated community. Oecologia 123:285–286

    Article  Google Scholar 

  • Schneider K et al (2004) Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15 N/14 N). Soil Biol Biochem 36:1769–1774

    Article  CAS  Google Scholar 

  • Scholtz CH, Davis ALV, Kryger U (2009) Evolutionary biology and conservation of dung beetles. Pensoft, Bulgaria

    Google Scholar 

  • Seldon DS, Beggs JR (2010) The efficacy of baited and live capture pitfall traps in collecting large-bodied forest carabids. NZ Entomol 33:30–37

    Article  Google Scholar 

  • Stavert JR, Drayton BA, Beggs JR, Gaskett AC (2014) The volatile compounds of introduced and native dung and carrion and their role in dung beetle foraging behaviour. Ecol Entomol (in press)

  • Tayasu I (1998) Use of carbon and nitrogen isotope ratios in termite research. Ecol Res 13:377–387

    Article  Google Scholar 

  • Tennyson AJD (2010) The origin and history of New Zealand’s terrestrial vertebrates. NZ J Ecol 34:6–27

    Google Scholar 

  • The University of Waikato (2006) Waikato Stable Isotope Unit

  • van den Boogaart KG, Tolosana-Delgado R (2013) Analyzing compositional data with R. Springer, Berlin

    Book  Google Scholar 

  • van den Boogaart GK, Tolosana R, Bren M (2014) Compositions: compositional data analysis. http://cran.rproject.org/package=compositions

  • Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet 15 N enrichment: a meta-analysis. Oecologia 136:169–182

    Article  PubMed  Google Scholar 

  • Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291

    Article  PubMed  Google Scholar 

  • Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3– an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259

    Article  Google Scholar 

  • Waters JM, Craw D (2006) Goodbye Gondwana? New Zealand biogeography, geology, and the problem of circularity. Syst Biol 55:351–356

    Article  PubMed  Google Scholar 

  • Wirta H, Orsini L, Hanski I (2008) An old adaptive radiation of forest dung beetles in Madagascar. Mol Phylogenet Evol 47:1076–1089

    Article  PubMed  Google Scholar 

  • Wirta H, Viljanen H, Orsini L, Montreuil O, Hanski I (2010) Three parallel radiations of Canthonini dung beetles in Madagascar. Mol Phylogenet Evol 57:710–727

    Article  PubMed  Google Scholar 

  • Worthy TH, Holdaway RN (1996) Quaternary fossil faunas, overlapping taphonomies, and palaeofaunal reconstruction in north Canterbury, South Island, New Zealand. J R Soc NZ 26:275–361

    Article  Google Scholar 

  • Worthy TH, Holdaway RN (2002) The lost world of the moa; prehistoric life of New Zealand. Indiana University Press, Bloomington

    Google Scholar 

  • Young OP (1981) The attraction of Neotropical Scarabaeinae (Coleoptera: scarabaeidae) to reptile and amphibian fecal material. Coleopt Bull 35:345–348

    Google Scholar 

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Acknowledgments

We thank Anjana Rajendram and the Waikato Stable Isotope team for analysis of stable isotope samples and Mauren Jaudal for help preparing samples. We thank Sandra Anderson, Joanne Peace, Bill Lee and two anonymous reviewers for helpful comments on the earlier manuscript. Lastly we thank John Allpress and Jill Brooking for access to dung beetle collection sites and The University of Auckland for financial support. Research was conducted under Department of Conservation research permit numbers AK-33027-RES, AK-33078-RES, AK-33217-RES and AK-32514-RES and Auckland Council research permit number WS478.

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Correspondence to J. R. Stavert.

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Communicated by Nina Farwig.

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Stavert, J.R., Gaskett, A.C., Scott, D.J. et al. Dung beetles in an avian-dominated island ecosystem: feeding and trophic ecology. Oecologia 176, 259–271 (2014). https://doi.org/10.1007/s00442-014-3001-z

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  • DOI: https://doi.org/10.1007/s00442-014-3001-z

Keywords

  • Stable isotope
  • Decomposition
  • Allochthonous input
  • Ecosystem function
  • Island restoration
  • Feeding behaviour