Skip to main content

Advertisement

SpringerLink
Log in

The evolution of the mouthpart structures in the Eucraniini (Coleoptera, Scarabaeidae)

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

The Eucraniini are a small dung beetle tribe endemic to Argentina (4 genera with 14 species), adapted to live in extremely arid environments, usually feeding on dry, small mammal dung pellets. These beetles grasp the dried pellets lifting them by the foretibiae and run forward on the middle and hindlegs. Here, the eucraniine mouthparts (epipharynx, labium, mandibles and maxillae) and ventral part of the clypeus were examined. According to the results, the structures were collectively defined as MOS (i.e., mouthpart structures), which is related to the unique feeding behavior displayed by these dung beetles (i.e., the food-lifting). The modification patterns of the MOS were examined in the lifters Eucraniini and compared to those of Neotropical tunneler species of Phanaeini and Dichotomiini, but also to the Afrotropical genus Pachysoma, with which they share many characters. Well-differentiated and distinguished MOS were detected in the three Neotropical tribes Eucraniini, Phanaeini, and Dichotomiini, evidencing also how the variation patterns of this complex system mirror the phylogenetic relationships among these tribes, and also within the Eucraniini genera.

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
Fig. 6

Similar content being viewed by others

Data Availability

The datasets analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Ahrens, D., Schwarzer, J., & Vogler, A.P. (2014). The evolution of scarab beetles tracks the sequential rise of angiosperms and mammals. Proceedings of the Royal Society B, https://doi.org/10.1098/rspb.2014.1470.

  • Arnaudin, M. E., Teutsch, C. D., Watson, D. W., Wildeus, S. A. J., & Abaye, A. O. (2014). Dung Beetle (Coleoptera: Scarabaeidae) Abundance and Diversity in Alpaca Pastures of Virginia USA. Journal of Entomological Science, 49, 97–109.

    Article  Google Scholar 

  • Bai, M., Li, S., Lu, Y., Yang, H., Tong, Y., & Yang, X. (2015). Mandible evolution in the Scarabaeinae (Coleoptera: Scarabaeidae) and adaptations to coprophagous habits. Frontiers in Zoology. https://doi.org/10.1186/s12983-015-0123-z.

  • Bryant, D., & Moulton, V. (2004). NeighborNet: an agglomerative algorithm for the construction of phylogenetic networks. Molecular Biology and Evolution, 21, 255–265.

    Article  CAS  Google Scholar 

  • Casiraghi, M., Labra, M., Ferri, E., Galimberti, A., & De Mattia, F. (2010). DNA barcoding: a six-question tour to improve users’ awareness about the method. Briefings in Bioinformatics. https://doi.org/10.1093/bib/bbq003.

  • Cupello, M., & Vaz-De-Mello, F. Z. (2013). Taxonomic revision of the South American dung beetle genus Gromphas Brullé, 1837 (Coleoptera: Scarabaeidae: Scarabaeinae: Phanaeini: Gromphadina). Zootaxa, 3722, 439–482.

    Article  Google Scholar 

  • Dellacasa, G. (1983). Sistematica e nomenclatura degli Aphodiini italiani. Monografie del Museo regionale di Scienze naturali, 1, 1–464.

    Google Scholar 

  • Dellacasa, G., & Dellacasa, M. (2006). Fauna d’Italia. Coleoptera Aphodiidae Aphodiinae. Bologna: Edagricole.

    Google Scholar 

  • Forsythe, T. G. (1983). Mouthparts and feeding in certain ground beetles (Coleoptera: Carabidae). Zoological Journal of the Linnean Society, 79, 319–376.

    Article  Google Scholar 

  • Genise, J. F. (2017). Ichnoentomology - insect traces in soils and paleosols. Berlin: Springer.

    Google Scholar 

  • Gunter, N. L., Weir, T. A., Slipinksi, A., Bocak, L., & Cameron, S. L. (2016). If dung beetles (Scarabaeidae: Scarabaeinae) arose in association with dinosaurs, Did They Also Suffer a Mass Co-Extinction at the KPg Boundary? PLoS One. https://doi.org/10.1371/journal.pone.0153570.

  • Halffter, G., & Edmonds, W. D. (1982). The nesting behavior of dung beetles (Scarabaeinae). An ecological and evolutive approach. Mexico: Instituto de Ecologia.

    Google Scholar 

  • Halffter, G., & Halffter, V. (2009). Why and where coprophagous beetles (Coleoptera: Scarabaeinae) eat seeds, fruits or vegetable detritus. Boletín de la SEA, 45, 1–22.

    Google Scholar 

  • Halffter, G., & Matthews, E. G. (1966). The natural history of dung beetles of the subfamily Scarabaeinae. Folia Entomológica Mexicana, 12–14, 1–312.

    Google Scholar 

  • Hebert, P. D. N., Cywinska, A., Ball, S. L., & Dewaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B, 270, 313–322.

  • Holter, P. (2000). Particle feeding in Aphodius dung beetles (Scarabaeidae): old hypotheses and new experimental evidence. Functional Ecology, 14, 631–637.

    Article  Google Scholar 

  • Holter, P., & Scholtz, C. H. (2005). Are ball-rolling (Scarabaeini, Gymnopleurini, Sisyphini) and tunnelling scarabaeine dung beetles equally choosy about the size of ingested dung particles? Ecological Entomology, 30, 700–705.

    Article  Google Scholar 

  • Holter, P., & Scholtz, C. H. (2011). Re-establishment of biting mouthparts in desert-living dung beetles (Scarabaeidae: Scarabaeinae) feeding on plant litter—old structures reacquired or new ones evolved? Journal of Morphology. https://doi.org/10.1002/jmor.10968.

  • Holter, P., Scholtz, C. H., & Wardhaugh, K. G. (2002). Dung feeding in adult scarabaeines (tunnellers and endocoprids): even large dung beetles eat small particles. Ecological Entomology, 27, 169–176.

    Article  Google Scholar 

  • Hörnschemeyer, T., Bond, J., & Young, P. G. (2013). Analysis of the functional morphology of mouthparts of the beetle Priacma serrata, and a discussion of possible food sources. Journal of Insect Science. https://doi.org/10.1673/031.013.12601.

  • Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254–267.

    Article  CAS  Google Scholar 

  • Huson, D. H., Rupp, R., & Scornavacca, C. (2010). Phylogenetic networks: concepts, algorithms and applications. Cambridge University Press.

  • Karolyi, F., Gorb, S. N., & Krenn, H. W. (2009). Pollen grains adhere to the moist mouthparts in the flower visiting beetle Cetonia aurata (Scarabaeidae, Coleoptera). Arthropod-Plant Interactions. https://doi.org/10.1007/s11829-008-9052-5.

  • Karolyi, F., Hansal, T., Krenn, H. W., & Colville, J. F. (2016). Comparative morphology of the mouthparts of the megadiverse South African monkey beetles (Scarabaeidae: Hopliini): feeding adaptations and guild structure. PeerJ. https://doi.org/10.7717/peerj.1597.

  • Kerman, K., Roggero, A., Rolando, A., & Palestrini, C. (2018). Evidence for male horn dimorphism and related pronotal shape variation in Copris lunaris (Linnaeus, 1758) (Coleoptera: Scarabaeidae, Coprini). Insects. https://doi.org/10.3390/insects9030108.

  • Lemey, P., Salemi, M., & Vandamme, A.-M. (2009). A practical approach to phylogenetic analysis and hypothesis testing. Cambridge: Cambridge University Press.

    Google Scholar 

  • Maldaner, M. E., Nunes, R. V., & Vaz-de-Mello, F. Z. (2015). Taxonomic revision of the Dichotomius speciosus (Waterhouse, 1891) species group (Coleoptera:Scarabaeidae: Scarabaeinae). Zootaxa, 3986, 549–560.

    Article  Google Scholar 

  • Monteresino, E. M., & Zunino, M. (2003). Sobre el comportamiento de la alimentación de Eucraniini (Coleoptera: Scarabaeidae: Scarabaeinae). In G. Onore, P. Reyes Castillo, & M. Zunino (Eds.), Escarabeidos de Latinoamerica. Estado Actual del Conocimiento (pp. 75–80). Zaragoza: SEA.

  • Moon, M.-J., Park, J.-G., & Kim, K.-H. (2008). Fine structure of the mouthparts in the ambrosia beetle Platypus koryoensis (Coleoptera: Curculionidae: Platypodinae). Animal Cells and Systems, 12, 101–108.

    Article  Google Scholar 

  • Nei, M., & Kumar, S. (2000). Molecular evolution and phylogenetics. New York: Oxford University Press.

    Google Scholar 

  • Nel, A., & De Villiers, W. M. (1988). Mouthpart structure in adult scarab beetles (Coleoptera: Scarabaeoidea). Entomologia Generalis, 13, 95–114.

    Article  Google Scholar 

  • Nunes, R. V., & Vaz-de-Mello, F. Z. (2013). New brachypterous species of Dichotomius Hope, with taxonomic notes in the subgenus Luederwaldtinia Martínez (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa, 3609, 411–420.

    Article  Google Scholar 

  • Nunes, R. V., Carvalho, M. S., & Vaz-de-Mello, F. Z. (2016). Taxonomic review of the Dichotomius (Luederwaldtinia) assifer (Eschscholtz) species-group (Coleoptera: Scarabaeidae). Zootaxa, 4078, 230–244.

    Article  Google Scholar 

  • Ocampo, F. C. (2004). Food relocation behavior and synopsis of the southern South American genus Glyphoderus Westwood (Scarabaeidae: Scarabaeinae: Eucraniini). Coleopterists Bulletin, 58, 295–305.

    Article  Google Scholar 

  • Ocampo, F. C. (2005). Revision of the southern South American endemic genus Anomiopsoides Blackwelder 1944 (Coleoptera: Scarabaeidae: Scarabaeinae: Eucraniini) with description of its food relocation behavior. Journal of Natural History, 39, 2537–2557.

    Article  Google Scholar 

  • Ocampo, F. C. (2007). El género argentino de escarabajos estercoleros Anomiopsoides (Scarabaeidae: Scarabaeinae: Eucraniini): descripcción de una especie nueva y nuevas sinonimias para A. heteroclyta. Revista de la Sociedad Entomológica Argentina, 66, 159–168.

    Google Scholar 

  • Ocampo, F. C. (2010a). The South American dung beetle genus Ennearabdus Lansberge (Coleoptera: Scarabaeidae: Scarabaeinae: Eucraniini). Journal of Insect Science. https://doi.org/10.1673/031.010.9301.

  • Ocampo, F. C. (2010b). A revision of the Argentinean endemic genus Eucranium Brullé (Coleoptera: Scarabaeidae: Scarabaeinae) with description of one new species and new synonymies. Journal of Insect Science. https://doi.org/10.1673/031.010.20501.

  • Ocampo, F. C., & Hawks, D. C. (2006). Molecular phylogenetics and evolution of the food relocation behaviour of the dung beetle tribe Eucraniini (Coleoptera: Scarabaeidae: Scarabaeinae.) Invertebrate Systematics, 20, 557–570.

  • Ocampo, F. C., & Philips, T. K. (2005). Food relocation behavior of the Argentinian dung beetle genus Eucranium Brullé and comparison with the southwest African Scarabaeus (Pachysoma) MacLeay (Coleoptera: Scarabaeidae: Scarabaeinae). Revista de la Sociedad Entomológica Argentina, 64, 53–59.

    Google Scholar 

  • Pentinsaari, M., Salmela, H., Mutanen, M., & Roslin, T. (2016). Molecular evolution of a widely-adopted taxonomic marker (COI) across the animal tree of life. Scientific Reports, 6, 35275.

    Article  CAS  Google Scholar 

  • Puillandre, N., Lambert, A., Brouillet, S., & Achaz, G. (2011). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology. https://doi.org/10.1111/j.1365-294X.2011.05239.x.

  • Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology. https://doi.org/10.1093/sysbio/syy032.

  • Roggero, A., Barbero, E., & Palestrini, C. (2015). Phylogenetic and biogeographical review of the Drepanocerina (Coleoptera, Scarabaeidae, Oniticellini). Arthropod Systematics & Phylogeny, 73, 153–174.

    Google Scholar 

  • Roggero, A., Barbero, E., & Palestrini, C. (2017a). Revised classification and phylogeny of an Afrotropical species group based on molecular and morphological data, with the description of a new genus (Coleoptera: Scarabaeidae: Onthophagini). Organisms, Diversity and Evolution, 17, 181–198.

    Article  Google Scholar 

  • Roggero, A., Dierkens, M., Barbero, E., & Palestrini, C. (2017b). Combined phylogenetic analysis of two new Afrotropical genera of Onthophagini (Coleoptera, Scarabaeidae). Zoological Journal of the Linnean Society, 180, 298–320. https://doi.org/10.1111/zoj.12498.

    Article  Google Scholar 

  • Ronquist, F., Huelsenbeck, J., & Teslenko, M. (2011). MrBayes version 3.2 manual. Available online at http://mrbayes.sourceforge.net.

  • Schoolmeesters, P. (2018). Scarabs: World Scarabaeidae Database (version May 2018). In Y. Roskov, T. Orrell, D. Nicolson, N. Bailly, P.M. Kirk, T. Bourgoin, R.E. DeWalt, W. Decock, A. De Wever, E. van Nieukerken, J. Zarucchi, & L. Penev (Eds), Species 2000 & ITIS Catalogue of Life. Digital resource at http://www.catalogueoflife.org/col. Species 2000: Naturalis, Leiden, the Netherlands. ISSN 2405–8858. Accessed 29th Aug 2018.

  • Smith, J. B. (1892). The mouth parts of Copris carolina; with notes on the homologies of the mandibles. Transactions of the American Entomological Society, 19, 83–87.

    Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    Article  CAS  Google Scholar 

  • Tarasov, S., & Dimitrov, D. (2016). Multigene phylogenetic analysis redefines dung beetles relationships and classification (Coleoptera: Scarabaeidae: Scarabaeinae). BMC Evolutionary Biology. https://doi.org/10.1186/s12862-016-0822-x.

  • Tarasov, S., & Génier, F. (2015). Innovative Bayesian and parsimony phylogeny of dung beetles (Coleoptera, Scarabaeidae, Scarabaeinae) enhanced by ontology-based partitioning of morphological characters. PLoS One. https://doi.org/10.1371/journal.pone.0116671.

  • Tarasov, S. I., & Solodovnikov, A. Y. (2011). Phylogenetic analyses reveal reliable morphological markers to classify megadiversity in Onthophagini dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). Cladistics, 27, 490–528.

    Article  Google Scholar 

  • Tocco, C., Roggero, A., Rolando, A., & Palestrini, C. (2011). Interspecific shape divergence in Aphodiini dung beetles: the case of Amidorus obscurus and A. immaturus (Coleoptera: Scarabaeoidea). Organisms, Diversity and Evolution. https://doi.org/10.1007/s13127-011-0055-1.

  • Valois, M. C., Vaz-de-Mello, F. Z., & Silva, F. A. B. (2017). Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa, 4277, 503–530.

    Article  Google Scholar 

  • Vaz-de-Mello, F. Z. (2007). Revision and phylogeny of the dung beetle genus Zonocopris Arrow 1932 (Coleoptera: Scarabaeidae: Scarabaeinae), a phoretic of land snails. Annales de la Société Entomologique de France, 43, 231–239. https://doi.org/10.1080/00379271.2007.10697516.

    Article  Google Scholar 

  • Víctor, J., & Zúñiga, G. (2016). Phylogeny of Dendroctonus bark beetles (Coleoptera: Curculionidae: Scolytinae) inferred from morphological and molecular data. Systematic Entomology, 41. https://doi.org/10.1111/syen.12149.

  • Wang, Z.-L., Wang, T.-Z., Zhu, H.-F., Wang, Z.-Y., & Yu, X.-P. (2018). DNA barcoding evaluation and implications for phylogenetic relationships in ladybird beetles (Coleoptera: Coccinellidae). Mitochondrial DNA Part A. https://doi.org/10.1080/24701394.2018.1446950.

  • Wilhelmi, A. P., & Krenn, H. W. (2012). Elongated mouthparts of nectar-feeding Meloidae (Coleoptera). Zoomorphology. https://doi.org/10.1007/s00435-012-0162-3.

  • Williams, I. W. (1936). The comparative morphology of the mouthparts in the order Coleoptera treated from the standpoint of phylogeny. http://scholarworks.umass.edu/dissertations_1/877. Accessed 25 Jul 2018.

  • Yavorskaya, M., Beutel, R. G., & Polilov, A. (2017). Head morphology of the smallest beetles (Coleoptera: Ptiliidae) and the evolution of sporophagy within Staphyliniformia. Arthropod Systematics and Phylogeny, 75, 417–434.

    Google Scholar 

  • Zou, S., Li, Q., Kong, L., Yu, H., & Zheng, X. (2011). Comparing the usefulness of distance, monophyly and character-based DNA barcoding methods in species identification: a case study of Neogastropoda. PLoS One. https://doi.org/10.1371/journal.pone.0026619.

  • Zunino, M., Barbero, E., & Luzzatto, M. (1989). Food relocation behavior in Eucraniina beetles (Scarabaeidae) and the constraints of xeric environment. Tropical Zoology, 2, 235–240.

    Article  Google Scholar 

Download references

Funding

The study benefited from the Bruker MicroCT facility of the Geometric Morphometrics Laboratory at the Dpt. of Life Sciences and Systems Biology of Torino University, equipped thanks to funds from the CRT Foundation, Research and Education section (Torino, Italy).

Author information

Authors and Affiliations

  1. Department of Life Sciences and Systems Biology, University of Torino, Via Accademia Albertina 13, 10123, Torino, Italy

    Claudia Palestrini, Enrico Barbero & Angela Roggero

Authors
  1. Claudia Palestrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Enrico Barbero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Angela Roggero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angela Roggero.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(PDF 4245 kb)

ESM 2

(WMV 21123 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Palestrini, C., Barbero, E. & Roggero, A. The evolution of the mouthpart structures in the Eucraniini (Coleoptera, Scarabaeidae). Org Divers Evol 20, 451–465 (2020). https://doi.org/10.1007/s13127-020-00449-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-020-00449-w

Keywords

Search

Navigation