Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE (Open Access)

A comparison of ecomorphology between introduced and native Australian dung beetles

Alexander Harvey https://orcid.org/0000-0002-3996-6449 A and Emma Sherratt https://orcid.org/0000-0003-2164-7877 A B *
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.

B South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.

* Correspondence to: emma.sherratt@gmail.com

Handling Editor: Janine Deakin

Australian Journal of Zoology 70(4) 115-125 https://doi.org/10.1071/ZO22044
Submitted: 29 November 2022  Accepted: 23 February 2023   Published: 27 April 2023

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Among the many catastrophic introductions of exotic species to Australia, the Australian Dung Beetle Project stands apart as a success story. From 1965 dung beetles (Coleoptera: Scarabaeinae) were introduced for biological control purposes, and 23 species survived to become integrated into the environment with apparently little-to-no competition with native species. To understand this, we investigated ecomorphological diversity in the Australian dung beetle fauna, examining variation in functional traits among rolling and tunnelling species that are native to Australia and introduced. We found that introduced species are, on average, larger than native species of the same nidification strategy, but the size ranges overlap. Native and introduced tunnellers are convergent in body shape, whereas introduced rollers have distinct body shape compared with native species. Rollers and tunnellers also have distinct allometric patterns, where shape variation predicted by size aligns along two diverging allometric trajectories between nidification strategies. Our results suggest that ecomorphological differences do not explain the apparent lack of competition between tunnellers, but this may be the factor for rollers. Also, these results indicate that body size and associated allometric scaling is an important aspect of the ecomorphology of dung beetles that should be considered in future studies.

Keywords: convergence, diversity, dung beetles, ecomorphology, functional morphology, morphometrics, niche partitioning, Scarabaeinae.


References

Adams, DC, and Nistri, A (2010). Ontogenetic convergence and evolution of foot morphology in European cave salamanders (family: Plethodontidae). BMC Evolutionary Biology 10, 216.
Ontogenetic convergence and evolution of foot morphology in European cave salamanders (family: Plethodontidae).Crossref | GoogleScholarGoogle Scholar |

Adams DC, Collyer ML, Kaliontzopoulou A, Baken EK (2022) geomorph: software for geometric morphometric analyses. R package version 4.0. Available at https://cran.r-project.org/package=geomorph

Alves, VM, and Hernández, MIM (2019). Local extinctions may be evidenced by the holes of the morphometric hypervolume in dung beetle communities. Austral Ecology 44, 827–837.
Local extinctions may be evidenced by the holes of the morphometric hypervolume in dung beetle communities.Crossref | GoogleScholarGoogle Scholar |

Anderson, MJ (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.
A new method for non-parametric multivariate analysis of variance.Crossref | GoogleScholarGoogle Scholar |

Benítez, HA, Püschel, TA, and Suazo, MJ (2022). Drosophila wing integration and modularity: a multi-level approach to understand the history of morphological structures. Biology 11, 567.
Drosophila wing integration and modularity: a multi-level approach to understand the history of morphological structures.Crossref | GoogleScholarGoogle Scholar |

Bookstein, FL (1989). “Size and shape”: a comment on semantics. Systematic Zoology 38, 173–180.
“Size and shape”: a comment on semantics.Crossref | GoogleScholarGoogle Scholar |

Bornemissza, GF (1976). Australian dung beetle project, 1965–1975. AMRC Review. Australian Meat Research Committee 30, 1–30.

Briese, DT (2004). Weed biological control: applying science to solve seemingly intractable problems. Australian Journal of Entomology 43, 304–317.
Weed biological control: applying science to solve seemingly intractable problems.Crossref | GoogleScholarGoogle Scholar |

Carvalho, RL, Weir, T, Vasconcelos, HL, and Andersen, AN (2020). Dung beetles of an Australian tropical savanna: species composition, food preferences and responses to experimental fire regimes. Austral Ecology 45, 958–967.
Dung beetles of an Australian tropical savanna: species composition, food preferences and responses to experimental fire regimes.Crossref | GoogleScholarGoogle Scholar |

Claude, J (2013). Log-shape ratios, Procrustes superimposition, elliptic Fourier analysis: three worked examples in R. Hystrix – Italian Journal of Mammalogy 24, 94–102.
Log-shape ratios, Procrustes superimposition, elliptic Fourier analysis: three worked examples in R.Crossref | GoogleScholarGoogle Scholar |

Davis, ALV (1996). Community organization of dung beetles (Coleoptera: Scarabaeidae): differences in body size and functional group structure between habitats. African Journal of Ecology 34, 258–275.
Community organization of dung beetles (Coleoptera: Scarabaeidae): differences in body size and functional group structure between habitats.Crossref | GoogleScholarGoogle Scholar |

Davis, ALV, Scholtz, CH, and Philips, TK (2002). Historical biogeography of scarabaeine dung beetles. Journal of Biogeography 29, 1217–1256.
Historical biogeography of scarabaeine dung beetles.Crossref | GoogleScholarGoogle Scholar |

Dodd AP (1940) ‘The Biological Campaign against Prickly-pear.’ (AH Tucker, Government Printer: Brisbane, Qld, Australia)

Doube, BM (1990). A functional classification for analysis of the structure of dung beetle assemblages. Ecological Entomology 15, 371–383.
A functional classification for analysis of the structure of dung beetle assemblages.Crossref | GoogleScholarGoogle Scholar |

Doube, BM, and Macqueen, A (1991). Establishment of exotic dung beetles in Queensland: the role of habitat specificity. Entomophaga 36, 353–360.
Establishment of exotic dung beetles in Queensland: the role of habitat specificity.Crossref | GoogleScholarGoogle Scholar |

Doube B, Macqueen A, Ridsdill-Smith T, Weir T (2014) Native and introduced dung beetles in Australia. In ‘Dung Beetle Ecology’. (Eds I Hanski, Y Cambefort) pp. 255–278. (Princeton University Press: Princeton, NJ, USA)

Drake, AG, and Klingenberg, CP (2010). Large-scale diversification of skull shape in domestic dogs: disparity and modularity. The American Naturalist 175, 289–301.
Large-scale diversification of skull shape in domestic dogs: disparity and modularity.Crossref | GoogleScholarGoogle Scholar |

Duncan, RP, Cassey, P, and Blackburn, TM (2009). Do climate envelope models transfer? A manipulative test using dung beetle introductions. Proceedings of the Royal Society B: Biological Sciences 276, 1449–1457.
Do climate envelope models transfer? A manipulative test using dung beetle introductions.Crossref | GoogleScholarGoogle Scholar |

Ebert, KM, Monteith, GB, Menéndez, R, and Merritt, DJ (2019). Bait preferences of Australian dung beetles (Coleoptera: Scarabaeidae) in tropical and subtropical Queensland forests. Austral Entomology 58, 772–782.
Bait preferences of Australian dung beetles (Coleoptera: Scarabaeidae) in tropical and subtropical Queensland forests.Crossref | GoogleScholarGoogle Scholar |

Edwards PB (2007) Introduced dung beetles in Australia 1967–2007: current status and future directions. Landcare Australia, Sydney, NSW, Australia. p. 66.

Edwards P, Wilson P, Wright J (2015) ‘Introduced Dung beetles in Australia: a Pocket Field Guide.’ (CSIRO Publishing: Melbourne, Vic., Australia)

Ferrar, P (1975). Disintegration of dung pads in north Queensland before the introduction of exotic dung beetles. Australian Journal of Experimental Agriculture 15, 325–329.
Disintegration of dung pads in north Queensland before the introduction of exotic dung beetles.Crossref | GoogleScholarGoogle Scholar |

Finn, JA, and Gittings, T (2003). A review of competition in north temperate dung beetle communities. Ecological Entomology 28, 1–13.
A review of competition in north temperate dung beetle communities.Crossref | GoogleScholarGoogle Scholar |

Giller, PS, and Doube, BM (1989). Experimental analysis of inter- and intraspecific competition in dung beetle communities. Journal of Animal Ecology 58, 129–142.
Experimental analysis of inter- and intraspecific competition in dung beetle communities.Crossref | GoogleScholarGoogle Scholar |

Gunter, NL, Monteith, GB, Cameron, SL, and Weir, TA (2019). Evidence from Australian mesic zone dung beetles supports their Gondwanan origin and Mesozoic diversification of the Scarabaeinae. Insect Systematics & Evolution 50, 162–188.
Evidence from Australian mesic zone dung beetles supports their Gondwanan origin and Mesozoic diversification of the Scarabaeinae.Crossref | GoogleScholarGoogle Scholar |

Halffter G, Edmonds WD (1982) ‘The Nesting Behavior of Dung Beetles (Scarabaeinae). An Ecological and Evolutive Approach.’ (Instituto de Ecologia: Mexico)

Halffter, G, and Matthews, EG (1966). The natural history of dung beetles of the subfamily Scarabaeinae (Coleoptera, Scarabaeidae). Folia Entomologica Mexicana 12–14, 1–312.

Hanski I, Cambefort Y (2014) ‘Dung Beetle Ecology.’ (Princeton University Press: Princeton, NJ, USA)

Hernández, MIM, Monteiro, LR, and Favila, ME (2011). The role of body size and shape in understanding competitive interactions within a community of Neotropical dung beetles. Journal of Insect Science 11, 13.
The role of body size and shape in understanding competitive interactions within a community of Neotropical dung beetles.Crossref | GoogleScholarGoogle Scholar |

Hill, C (1993). The species composition and seasonality of an assemblage of tropical Australian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). The Australian Entomologist 20, 121–126.

Hill, CJ (1996). Habitat specificity and food preferences of an assemblage of tropical Australian dung beetles. Journal of Tropical Ecology 12, 449–460.
Habitat specificity and food preferences of an assemblage of tropical Australian dung beetles.Crossref | GoogleScholarGoogle Scholar |

Horgan, FG (2005). Aggregated distribution of resources creates competition refuges for rainforest dung beetles. Ecography 28, 603–618.
Aggregated distribution of resources creates competition refuges for rainforest dung beetles.Crossref | GoogleScholarGoogle Scholar |

Huxley, JS, and Teissier, G (1936). Terminology of relative growth. Nature 137, 780–781.
Terminology of relative growth.Crossref | GoogleScholarGoogle Scholar |

Inward, DJG, Davies, RG, Pergande, C, Denham, AJ, and Vogler, AP (2011). Local and regional ecological morphology of dung beetle assemblages across four biogeographic regions. Journal of Biogeography 38, 1668–1682.
Local and regional ecological morphology of dung beetle assemblages across four biogeographic regions.Crossref | GoogleScholarGoogle Scholar |

Jungers, WL, Falsetti, AB, and Wall, CE (1995). Shape, relative size, and size-adjustments in morphometrics. American Journal of Physical Anthropology 38, 137–161.
Shape, relative size, and size-adjustments in morphometrics.Crossref | GoogleScholarGoogle Scholar |

Karr JR, James FC (1975) Eco-morphological configurations and convergent evolution of species and communities. In ‘Ecology and Evolution of Communities’. (Eds ML Cody, JM Diamond) pp. 258–291. (Belknap: Cambridge, MA, USA)

Klingenberg, CP (2016). Size, shape, and form: concepts of allometry in geometric morphometrics. Development Genes and Evolution 226, 113–137.
Size, shape, and form: concepts of allometry in geometric morphometrics.Crossref | GoogleScholarGoogle Scholar |

Klingenberg, CP, and Zimmermann, M (1992). Static, ontogenetic, and evolutionary allometry: a multivariate comparison in nine species of water striders. The American Naturalist 140, 601–620.
Static, ontogenetic, and evolutionary allometry: a multivariate comparison in nine species of water striders.Crossref | GoogleScholarGoogle Scholar |

Losey, JE, and Vaughan, M (2006). The economic value of ecological services provided by insects. BioScience 56, 311–323.
The economic value of ecological services provided by insects.Crossref | GoogleScholarGoogle Scholar |

Marcy, AE, Guillerme, T, Sherratt, E, Rowe, KC, Phillips, MJ, and Weisbecker, V (2020). Australian rodents reveal conserved cranial evolutionary allometry across 10 million years of murid evolution. The American Naturalist 196, 755–768.
Australian rodents reveal conserved cranial evolutionary allometry across 10 million years of murid evolution.Crossref | GoogleScholarGoogle Scholar |

Marroig, G, and Cheverud, JM (2005). Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World monkeys. Evolution 59, 1128–1142.
Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World monkeys.Crossref | GoogleScholarGoogle Scholar |

Matthews, EG (1971). A revision of the Scarabaeine dung beetles of Australia. I. Tribe Onthophagini. Australian Journal of Zoology Supplementary Series 19, 3–330.
A revision of the Scarabaeine dung beetles of Australia. I. Tribe Onthophagini.Crossref | GoogleScholarGoogle Scholar |

Matthews, EG (1974). A revision of the Scarabaeine dung beetles of Australia. II. Tribe Scarabaeini*. Australian Journal of Zoology Supplementary Series 22, 1–211.
A revision of the Scarabaeine dung beetles of Australia. II. Tribe Scarabaeini*.Crossref | GoogleScholarGoogle Scholar |

Matthews, EG (1976). A revision of ths Scarabaeine dung beetles of Australia. III. Tribe Coprini*. Australian Journal of Zoology Supplementary Series 24, 1–52.
A revision of ths Scarabaeine dung beetles of Australia. III. Tribe Coprini*.Crossref | GoogleScholarGoogle Scholar |

Mosimann, JE (1970). Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions. Journal of the American Statistical Association 65, 930–945.
Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions.Crossref | GoogleScholarGoogle Scholar |

Nemes, SN, and Price, DL (2015). Illustrated keys to the Scarabaeinae (Coleoptera: Scarabaeidae) of Maryland. Northeastern Naturalist 22, 318–344.
Illustrated keys to the Scarabaeinae (Coleoptera: Scarabaeidae) of Maryland.Crossref | GoogleScholarGoogle Scholar |

Peters RH, Peters RH (1986) ‘The Ecological Implications of Body Size.’ (Cambridge University press: Cambridge, UK)

Raine, EH, Gray, CL, Mann, DJ, and Slade, EM (2018). Tropical dung beetle morphological traits predict functional traits and show intraspecific differences across land uses. Ecology and Evolution 8, 8686–8696.
Tropical dung beetle morphological traits predict functional traits and show intraspecific differences across land uses.Crossref | GoogleScholarGoogle Scholar |

R Development Core Team (2022) R: a language and environment for statistical computing (CRAN). Available at http://www.R-project.org

Ridsdill-Smith TJ, Edwards PB (2011) Biological control: ecosystem functions provided by dung beetles. In ‘Ecology and Evolution of Dung Beetles’. (Eds LW Simmons, TJ Ridsdill-Smith) pp. 243–263. (John Wiley & Sons: West Sussex, UK)

Stekhoven DJ, Stekhoven MDJ (2013) R Package “missForest”. Available at https://cran.r-project.org/web/packages/missForest

Tarasov, S, and Dimitrov, D (2016). Multigene phylogenetic analysis redefines dung beetles relationships and classification (Coleoptera: Scarabaeidae: Scarabaeinae). BMC Evolutionary Biology 16, 257.
Multigene phylogenetic analysis redefines dung beetles relationships and classification (Coleoptera: Scarabaeidae: Scarabaeinae).Crossref | GoogleScholarGoogle Scholar |

Vernes, K, Pope, LC, Hill, CJ, and Bärlocher, F (2005). Seasonality, dung specificity and competition in dung beetle assemblages in the Australian Wet Tropics, north-eastern Australia. Journal of Tropical Ecology 21, 1–8.
Seasonality, dung specificity and competition in dung beetle assemblages in the Australian Wet Tropics, north-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Williams EE (1972) The origin of faunas. Evolution of lizard congeners in a complex island fauna: a trial analysis. In ‘Evolutionary Biology, Vol. 6’. (Eds T Dobzhansky, MK Hecht, WC Steere) pp. 47–89. (Springer: New York, NY, USA)

Wright KL (1997) An examination of the commensal interaction between the Australian native dung beetle, Onthophagus peramelinus and the rufous bettong, Aepyprymnus rufescens. BSc Honours Thesis, James Cook University, Townsville, Qld, Australia.

Zelditch ML, Swiderski DL, Sheets HD (2012) ‘Geometric Morphometrics for Bologists: a Primer.’ (Elsevier: Amsterdam, The Netherlands)