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First record of the largest copro-necrophagous beetle in South America (Coprophanaeus lancifer) feeding on fruits

ABSTRACT

Coprophanaeus lancifer is a copro-necrophagous beetle endemic to the Amazon region. Although beetles belonging to the subfamily Scarabaeinae primarily feed on dung, some have a greater diet plasticity that includes carrion, fungi, rotten fruits and invertebrates. The diet of the scavenger beetle C. lancifer mainly consists of vertebrate carcasses, although it is also attracted to mammal faeces. Here, we describe the first record of this species feeding on fruits of the genus Nectandra.

KEYWORDS:
Peru; dung beetle; frugivory; diet plasticity; Scarabaeinae; Amazon

RESUMEN

Coprophanaeus lancifer es un escarabajo copro-necrófago endémico de la región amazónica. Aunque los escarabajos pertenecientes a la subfamilia Scarabaeinae se alimentan principalmente de excrementos, algunos tienen una mayor plasticidad dietética que incluye carroña, hongos, frutas podridas y invertebrados. La dieta del escarabajo carroñero C. lancifer consiste principalmente en cadáveres de vertebrados, aunque, también se siente atraído por heces de mamíferos. Aquí, describimos el primer registro de esta especie alimentándose de frutos del género Nectandra.

PALABRAS CLAVE:
Perú; escarabajo coprófago; frugívoro; plasticidad dietética; Scarabaeinae; Amazonía

The dung beetle Coprophanaeus lancifer Linnaeus, 1767 is a member of the Scarabaeidae family (subfamily Scarabaeinae) and, together with C. ensifer (Germar), C. bonariensis (Gory) and C. bellicosus (Olivier), is a valid member of the Megaphanaeus subgenus (Maldaner et al. 2017Maldaner, M.E.; Cupello, M.; Ferreira, D.C.; Vaz-de-Mello, F.Z. 2017. Type specimens and names assigned to Coprophanaeus (Megaphanaeus) d’Olsoufieff, 1924, the largest New World dung beetles (Coleoptera: Scarabaeidae: Phanaeini). Zootaxa, 4272: 83-102.; Maldaner et al. 2018Maldaner, M.E.; Vaz-de -Mello, F.Z.; Takiya, D.M.; Ferreira, D.C. 2018. Molecular Phylogeny of Coprophanaeus (Megaphanaeus) d’Olsoufieff, 1924 (Coleoptera: Scarabaeidae: Scarabaeinae) and the position of C. bellicosus. Insect Systematics & Evolution, 51: 241-255.). It reaches a length of up to 55 mm (Edmonds 1972Edmonds, W.D. 1972. Comparative skeletal morphology, systematic and evolution of the phanaeine dung beetles (Coleoptera: Scarabaeidae). The Kansas University Science Bulletin, 49: 731-874.) and weighs up to 10 g (pers. comm. Sandra María Bejár Hermoza), more than most hummingbirds (pers. comm. G. Chacon, who weighed individuals of 10 different species of hummingbirds in the Kosñipata valley (Peru), with just one individual exceeding 10 g). It is the largest copro-necrophagous beetle in South America and its range extends throughout Venezuela, French Guiana, Guyana, Suriname, Brazil, Bolivia and Peru, in the Amazonian subregion (Edmonds and Zídek 2010; Maldaner et al. 2018Maldaner, M.E.; Vaz-de -Mello, F.Z.; Takiya, D.M.; Ferreira, D.C. 2018. Molecular Phylogeny of Coprophanaeus (Megaphanaeus) d’Olsoufieff, 1924 (Coleoptera: Scarabaeidae: Scarabaeinae) and the position of C. bellicosus. Insect Systematics & Evolution, 51: 241-255.).

Coprophanaeus lancifer is mostly found in terra firme habitats, of both pristine and second growth forests, and less commonly in floodplain forests (Hamel-Leigue et al. 2009Hamel-Leigue, A.C.; Herzog, S.K.; Mann, D.J.; Larsen, T.H.; Gill, B.D.; Edmonds, W.D.; Spector, S. 2009. Distribución e historia natural de escarabajos coprófagos de la tribu Phanaeini (Coleoptera: Scarabaeidae: Scrarabaeinae) en Bolivia. Kempffiana, 5: 43-95.; Larsen 2015Larsen, T.H. 2015. Coprophanaeus lancifer. ( (https://scarabaeinae.myspecies.info/node/198 ). Accessed on 30 Oct 2022.
https://scarabaeinae.myspecies.info/node...
). As all other copro-necrophagous beetles, it carries out an important part of the nutrient-cycling process in tropical rainforests (Halffter and Favila 1993Halffter, G.; Favila, ME 1993. Os Scarabaeinae (Insecta: Coleoptera), um Grupo Animal para Análise, Inventário e Monitoramento da Biodiversidade em Floresta Tropical e Paisagens Modificadas. Biology International, 27: 15-21.). This species flies up to 5 km per day, generally at dusk (Feer and Pincebourde 2005Feer, F.; Pincebourde, S. 2005. Diel flight activity and ecological segregation within an assemblage of tropical forest dung and carrion beetles. Journal of Tropical Ecology, 21: 21-30. ) to find and bury animal faeces and small carcasses, especially in the wet season, according to our hitherto unpublished investigations. Its feeding habits also make it useful in forensic entomology, mostly due to its ability to cause tissue injury and by moving the cadaver from its original position (Ururahy-Rodrigues et al. 2008Ururahy-Rodrigues, A.; Marques, H.; Rafael, J.; Wanderley, R.; Pujol-Luz, J. 2008. Coprophanaeus lancifer (Coleoptera, Scarabaeidae) activity causes the rolling movement of a man-sized carcass in Amazonia, Brazil: a forensic taphonomy report. Forensic Science International, 182: 19-22.).

Although dung beetle species are mostly coprophagous, there are many species that feed on carrion, rotten fruits or fungi (Larsen et al. 2006Larsen, T.H.; Lopera, A.; Forsyth, A. 2006. Extreme trophic and habitat specialization by Peruvian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). The Coleoptersists Bulletin, 60: 315-324. ; Halffter and Halffter 2009Halffter, G.; Halffter, V. 2009. Why and where coprophagous beetles (Coleoptera: Scarabaeinae) eat seeds, fruits or vegetable detritus. Boletín de la Sociedad Entomológica Aragonesa, 45: 1-22.; Amézquita and Favila 2011Amézquita, S.J.; Favila, M.E. 2011. Carrion removal and diel activity of necrophagous beetles (Coleoptera: Scarabaeinae) in a fragmented tropical rain forest. Enviromental Entomology, 40: 239-246.; Salomão et al. 2017Salomão, R.P.; Maia, A.C.D.; Bezerra, B.M.; Iannuzzi, L. 2017. Attractiveness of different food resources to dung beetles (Coleoptera: Scarabaeidae) of a dry tropical area. Neotropical Entomology, 47: 69-78., 2021Salomão, R.P.; Cerqueira, L.V.M.P.; Gomes, A. de A.C.; González‐Tokman, D.; Maia, A.C.D.; Iannuzzi, L. 2021. Dung or carrion? Sex and age determine resource attraction in dung beetles. Ecological Entomology, 47: 52-62.; Langton-Myers 2022Langton-Myers, S.S. 2022. An endemic dung beetle species feeding on kauri snail carrion in Northland, New Zealand. Austral Ecology, 47: 127-130. ; Santiago et al. 2022Santiago, D.H.; Mathielo, R.S.; De Souza, A.S.B.; Silva-Soares, T. 2022. First record of necrophagy by the scarab beetle Coprophanaeus (Megaphanaeus) ensifer (Germar, 1821) on Lichtenstein’s Green Racer, Philodryas olfersii (Lichtenstein, 1823). Herpetology Notes, 15: 83-84.), and there are even some that predate upon millipedes (Larsen et al. 2009Larsen, T.H.; Lopera, A.; Forsyth, A.; Genier, F. 2009. From coprophagy to predation: a dung beetle that kills millipedes. Biology Letters, 5: 152-155. ) and leaf-cutter ant queens (Aquino et al. 2018Aquino, P.S.R.; Jesus, F.G.; Rocha, E.C.; Lucia, T.M.C.D.; Zanuncio, J.C.; Araújo, M.D.S. 2018. Predation rates of a beetle (Canthon virens) that kills female leaf-cutting ants (Atta spp.).International Journal of Agriculture and Biology, 20: 1247-1250.). As they use faeces and carrion as feeding sites for adults, they also build brood balls with these decomposing substrates to lay their eggs and feed their larvae (Gittings et al. 1998Gittings, T.; Giller, P.S. 1998. Resource quality and the colonisation and succession of coprophagous dung beetles. Ecography, 21: 581-592.; Byk and Piętka 2018Byk, A.; Piętka, J. 2018. Dung beetles and their role in the nature. Edukacja Biologiczna i Srodowiskowa, 1: 17-26.; Santiago et al. 2022).

The diet of C. lancifer mainly consists of vertebrate carcasses, which it quickly buries in the soil, often after intense competitive battles within and between the sexes, both of which are armed with large horns (Otronen 1988Otronen, M. 1988. lntra- and intersexual interactions at breeding burrows in the horned beetle, Coprophanaeus ensifer. Animal Behaviour, 36: 741-748.). These beetles are also attracted to mammal faeces. Edmonds and Zideck (2010Edmonds, W.D.; Zídek, J. 2010. A taxonomic review of the neotropical genus Coprophanaeus Olsoufieff, 1924 (Coleoptera: Scarabaeidae, Scarabaeinae). Insecta Mundi, 129: 1-111.), in their taxonomic review of Coprophanaeus, comment that beetles of this genus were observed feeding on decomposing millipedes. There are no reports of this species consuming foods other than carrion and dung. Here we report the first observations of C. lancifer feeding on fruits.

On March 24th 2022, at approximately 9:45 am, an individual of C. lancifer was found feeding on drupes of the genus Nectandra (Lauraceae). The drupe was completely ripe, with no evident smell, and was about half the size of the beetle (Figure 1). The feeding event was registered in a terra firme forest, on a trail (12°33’48.1392’’S, 70°5’51.5508’’W) at Los Amigos Biological Station (LABS), an Amazonian lowland research station located in the Madre de Dios watershed of southern Peru.

Figure 1
A - Individual of Coprophanaeus lancifer feeding on a Nectandra sp. drupe, at Los Amigos Biological Station, Peru; B - Close-up of Nectandra sp. drupes, the decomposing one on the right subsequently selected by one individual of C. lancifer. This figure is in color in the electronic version.

The beetle was collected along with a sample of the fruit, in the absence of a camera to document the event, and stored in a plastic zip-lock bag for later identification. During that same day, four more individuals of C. lancifer were collected using non-lethal carrion-baited pitfall traps in order to replicate the observation with more than one individual. On March 25th 2022, the five individuals were transported in a tupperware to the same site where the first individual was observed eating the drupe and released at 10:00 am close to where the Nectandra sp. fruits were located.

Within a few minutes, three out of the five individuals had moved away from the trail and hidden under the litter, while the remaining two had encountered a drupe and had started consuming it (Figure 2). During this observation, one of the individuals had also started digging a small hole in the soil to bury the drupe and the seed, even though the action of burying was not completed, as the beetle interrupted it and went away a few minutes later. The activity of two individuals eating and moving the fruits lasted 30 minutes and was registered on video (https://drive.google.com/drive/folders/1N5R9P_c1d2mSSZLH9UM9tQZwKRDE_Ztc?usp=sharing) until both spontaneously left the site. We noticed that both beetles seemed to prefer the decomposing fruits, already mashed or opened, over fresh and intact fruits on the forest floor. A total of three individuals were observed feeding on Nectandra fruits over two days.

Figure 2
A,B - Two individuals of Coprophanaeus lancifer consuming ripe Nectandra sp. fruits at Los Amigos Biological Station, Peru. This figure is in color in the electronic version.

Many species of Neotropical Scarabaeinae are considered generalists (Raine et al. 2019Raine, E.H.; Mikich, S.B.; Lewis, O.T.; Slade, E.M. 2019. Interspecific and intraspecific variation in diet preference in five Atlantic forest dung beetle species.Ecological Entomology, 44: 436-439.) with some feeding on fallen fruits (Davis and Sutton 1997Davis, A.J.; Sutton, S.L. 1997. A Dung Beetle That Feeds on Fig: Implications for the Measurement of Species Rarity. Journal of Tropical Ecology, 13: 759-766.; Sarges et al. 2012Sarges, R.; Halffter, G.; Rojas, A.D. 2012. The importance of frugivory to the survival of the dung beetle Onthophagus rhinolophus Harold (Coleoptera: Scarabaeidae: Scarabaeinae) under changing ecological conditions.The Coleopterists Bulletin, 66: 166-168.). However, the vast majority of papers on dung beetle diet preferences are derived from collection of beetles with baited pitfall traps rather than observations of feeding behavior under natural conditions. Most carrion feeders of the genus Coprophanaeus are facultative dung consumers, as is the case of C. lancifer which is only known to consume rotten meat and feaces. The ability to feed on alternative seasonal resources may be a consequence of the difficulty to find patchily distributed food sources such as dung ad carrion. In this context, fruit such as the Nectandra drupes may help to provide the necessary energy to keep on foraging, but probably would not be used for nesting, a hypothesis that remains to be tested. Our observation raises questions regarding the importance of alternative food sources such as fruits for the interaction between this species with plants and the provision of ecosystem services.

Dung beetles play an important role in secondary seed dispersal all over the world (Vulinec 2002Vulinec, K. 2002. Dung beetle communities and seed dispersal in primary forest and disturbed land in Amazonia. Biotropica, 34: 297-309.; Koike et al. 2012Koike, S.; Morimoto, H.; Kozakai, C.; Arimoto, I.; Soga, M.; Yamazaki, K.; Koganezawa, M. 2012. The role of dung beetles as a secondary seed disperser after dispersal by frugivore mammals in a temperate deciduous forest. Acta Oecologica, 41: 74-81.; Midgley et al. 2015Midgley, J.J.; White, J.D.M.; Johnson, S.D.; Bronner, G.N. 2015. Faecal mimicry by seeds ensures dispersal by dung beetles. Nature Plants, 1: 1-3.; Midgley et al. 2021Midgley, J.J.; White, J.D.M.; Scholtz, C.H.; Johnson, S.D. 2021. Seed dispersal by dung beetles in Ceratocaryum pulchrum (Restionaceae): Another example of faecal mimicry in plants. South African Journal of Botany, 137: 365-368.; Pedersen 2022Pedersen, K.M.; Blüthgen, N. 2022. Seed size and pubescence facilitate secondary dispersal by dung beetles. Biotropica, 54: 215- 225. ). Our observations suggest that C. lancifer may not only contribute to seed dispersal indirectly through dung removal but may be involved in the process of directly dispersing seeds that are not eaten and dispersed by other animals and, consequently, are not found in their scats.

Coprophanaeus lancifer presents an even greater feeding plasticity than what was already known. This argues for more effort at observations of live beetles under field conditions rather than complete reliance on baited pitfall traps.

ACKNOWLEDGMENTS

We wish to thank the Andes Amazon Fund for the funding and support of this research. We also thank Asociación para la Conservación de la Cuenca Amazónica (ACCA) for hosting us at Los Amigos Biological Station (LABS). The beetles sampled were collected under the SERFOR permit AUT-IFS-2021-021.

REFERENCES

  • Amézquita, S.J.; Favila, M.E. 2011. Carrion removal and diel activity of necrophagous beetles (Coleoptera: Scarabaeinae) in a fragmented tropical rain forest. Enviromental Entomology, 40: 239-246.
  • Aquino, P.S.R.; Jesus, F.G.; Rocha, E.C.; Lucia, T.M.C.D.; Zanuncio, J.C.; Araújo, M.D.S. 2018. Predation rates of a beetle (Canthon virens) that kills female leaf-cutting ants (Atta spp.).International Journal of Agriculture and Biology, 20: 1247-1250.
  • Byk, A.; Piętka, J. 2018. Dung beetles and their role in the nature. Edukacja Biologiczna i Srodowiskowa, 1: 17-26.
  • Davis, A.J.; Sutton, S.L. 1997. A Dung Beetle That Feeds on Fig: Implications for the Measurement of Species Rarity. Journal of Tropical Ecology, 13: 759-766.
  • Edmonds, W.D. 1972. Comparative skeletal morphology, systematic and evolution of the phanaeine dung beetles (Coleoptera: Scarabaeidae). The Kansas University Science Bulletin, 49: 731-874.
  • Edmonds, W.D.; Zídek, J. 2010. A taxonomic review of the neotropical genus Coprophanaeus Olsoufieff, 1924 (Coleoptera: Scarabaeidae, Scarabaeinae). Insecta Mundi, 129: 1-111.
  • Feer, F.; Pincebourde, S. 2005. Diel flight activity and ecological segregation within an assemblage of tropical forest dung and carrion beetles. Journal of Tropical Ecology, 21: 21-30.
  • Gittings, T.; Giller, P.S. 1998. Resource quality and the colonisation and succession of coprophagous dung beetles. Ecography, 21: 581-592.
  • Halffter, G.; Favila, ME 1993. Os Scarabaeinae (Insecta: Coleoptera), um Grupo Animal para Análise, Inventário e Monitoramento da Biodiversidade em Floresta Tropical e Paisagens Modificadas. Biology International, 27: 15-21.
  • Halffter, G.; Halffter, V. 2009. Why and where coprophagous beetles (Coleoptera: Scarabaeinae) eat seeds, fruits or vegetable detritus. Boletín de la Sociedad Entomológica Aragonesa, 45: 1-22.
  • Hamel-Leigue, A.C.; Herzog, S.K.; Mann, D.J.; Larsen, T.H.; Gill, B.D.; Edmonds, W.D.; Spector, S. 2009. Distribución e historia natural de escarabajos coprófagos de la tribu Phanaeini (Coleoptera: Scarabaeidae: Scrarabaeinae) en Bolivia. Kempffiana, 5: 43-95.
  • Koike, S.; Morimoto, H.; Kozakai, C.; Arimoto, I.; Soga, M.; Yamazaki, K.; Koganezawa, M. 2012. The role of dung beetles as a secondary seed disperser after dispersal by frugivore mammals in a temperate deciduous forest. Acta Oecologica, 41: 74-81.
  • Langton-Myers, S.S. 2022. An endemic dung beetle species feeding on kauri snail carrion in Northland, New Zealand. Austral Ecology, 47: 127-130.
  • Larsen, T.H.; Lopera, A.; Forsyth, A. 2006. Extreme trophic and habitat specialization by Peruvian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). The Coleoptersists Bulletin, 60: 315-324.
  • Larsen, T.H.; Lopera, A.; Forsyth, A.; Genier, F. 2009. From coprophagy to predation: a dung beetle that kills millipedes. Biology Letters, 5: 152-155.
  • Larsen, T.H. 2015. Coprophanaeus lancifer ( (https://scarabaeinae.myspecies.info/node/198 ). Accessed on 30 Oct 2022.
    » https://scarabaeinae.myspecies.info/node/198
  • Maldaner, M.E.; Cupello, M.; Ferreira, D.C.; Vaz-de-Mello, F.Z. 2017. Type specimens and names assigned to Coprophanaeus (Megaphanaeus) d’Olsoufieff, 1924, the largest New World dung beetles (Coleoptera: Scarabaeidae: Phanaeini). Zootaxa, 4272: 83-102.
  • Maldaner, M.E.; Vaz-de -Mello, F.Z.; Takiya, D.M.; Ferreira, D.C. 2018. Molecular Phylogeny of Coprophanaeus (Megaphanaeus) d’Olsoufieff, 1924 (Coleoptera: Scarabaeidae: Scarabaeinae) and the position of C. bellicosus Insect Systematics & Evolution, 51: 241-255.
  • Midgley, J.J.; White, J.D.M.; Johnson, S.D.; Bronner, G.N. 2015. Faecal mimicry by seeds ensures dispersal by dung beetles. Nature Plants, 1: 1-3.
  • Midgley, J.J.; White, J.D.M.; Scholtz, C.H.; Johnson, S.D. 2021. Seed dispersal by dung beetles in Ceratocaryum pulchrum (Restionaceae): Another example of faecal mimicry in plants. South African Journal of Botany, 137: 365-368.
  • Otronen, M. 1988. lntra- and intersexual interactions at breeding burrows in the horned beetle, Coprophanaeus ensifer Animal Behaviour, 36: 741-748.
  • Pedersen, K.M.; Blüthgen, N. 2022. Seed size and pubescence facilitate secondary dispersal by dung beetles. Biotropica, 54: 215- 225.
  • Raine, E.H.; Mikich, S.B.; Lewis, O.T.; Slade, E.M. 2019. Interspecific and intraspecific variation in diet preference in five Atlantic forest dung beetle species.Ecological Entomology, 44: 436-439.
  • Salomão, R.P.; Maia, A.C.D.; Bezerra, B.M.; Iannuzzi, L. 2017. Attractiveness of different food resources to dung beetles (Coleoptera: Scarabaeidae) of a dry tropical area. Neotropical Entomology, 47: 69-78.
  • Salomão, R.P.; Cerqueira, L.V.M.P.; Gomes, A. de A.C.; González‐Tokman, D.; Maia, A.C.D.; Iannuzzi, L. 2021. Dung or carrion? Sex and age determine resource attraction in dung beetles. Ecological Entomology, 47: 52-62.
  • Santiago, D.H.; Mathielo, R.S.; De Souza, A.S.B.; Silva-Soares, T. 2022. First record of necrophagy by the scarab beetle Coprophanaeus (Megaphanaeus) ensifer (Germar, 1821) on Lichtenstein’s Green Racer, Philodryas olfersii (Lichtenstein, 1823). Herpetology Notes, 15: 83-84.
  • Sarges, R.; Halffter, G.; Rojas, A.D. 2012. The importance of frugivory to the survival of the dung beetle Onthophagus rhinolophus Harold (Coleoptera: Scarabaeidae: Scarabaeinae) under changing ecological conditions.The Coleopterists Bulletin, 66: 166-168.
  • Ururahy-Rodrigues, A.; Marques, H.; Rafael, J.; Wanderley, R.; Pujol-Luz, J. 2008. Coprophanaeus lancifer (Coleoptera, Scarabaeidae) activity causes the rolling movement of a man-sized carcass in Amazonia, Brazil: a forensic taphonomy report. Forensic Science International, 182: 19-22.
  • Vulinec, K. 2002. Dung beetle communities and seed dispersal in primary forest and disturbed land in Amazonia. Biotropica, 34: 297-309.
  • CITE AS:

    Chaboteaux, E.; Lopera Toro, A.; Forsyth, A. 2023. First record of the largest copro-necrophagous beetle in South America (Coprophanaeus lancifer) feeding on fruits. Acta Amazonica 53: 154-157.

Edited by

ASSOCIATE EDITOR:

Pitágoras C. Bispo

Publication Dates

  • Publication in this collection
    28 Apr 2023
  • Date of issue
    Apr-Jun 2023

History

  • Received
    18 May 2022
  • Accepted
    18 Nov 2022
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