Hostname: page-component-76fb5796d-9pm4c Total loading time: 0 Render date: 2024-04-29T21:59:11.855Z Has data issue: false hasContentIssue false
  • English
  • Français

Cuticular lipid profiles of selected species of cyclocephaline beetles (Melolonthidae, Cyclocephalini)

Published online by Cambridge University Press:  25 January 2024

Geanne Karla N. Santos ,
Daniela Maria do Amaral F. Navarro  and
Artur Campos D. Maia Open the ORCID record for Artur Campos D. Maia [Opens in a new window]
Geanne Karla N. Santos
Affiliation:
Secretaria Executiva de Meio Ambiente de Paulista (SEMA), Prefeitura Municipal do Paulista, Paulista, 53401-441, Brazil Department of Fundamental Chemistry, Centro de Ciências Exatas e da Natureza, Universidade Federal de Pernambuco, Recife, 50740-560, Brazil
Daniela Maria do Amaral F. Navarro
Affiliation:
Department of Fundamental Chemistry, Centro de Ciências Exatas e da Natureza, Universidade Federal de Pernambuco, Recife, 50740-560, Brazil
Artur Campos D. Maia*
Affiliation:
Department of Zoology, Centro de Biociências, Universidade Federal de Pernambuco, Recife PE, 50670-901, Brazil Laboratory of Sciences for the Environment, University of Corsica, UMR 6134 SPE, Ajaccio, France
*
Corresponding author: Artur Campos D. Maia; Email: arturmaia@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Neotropical cyclocephaline beetles, a diverse group of flower-loving insects, significantly impact natural and agricultural ecosystems. In particular, the genus Cyclocephala, with over 350 species, displays polymorphism and cryptic complexes. Lacking a comprehensive DNA barcoding framework, accessible tools for species differentiation are needed for research in taxonomy, ecology, and crop management. Moreover, cuticular hydrocarbons are believed to be involved in sexual recognition mechanisms in these beetles. In the present study we examined the cuticular chemical profiles of six species from the genus Cyclocephala and two populations of Erioscelis emarginata and assessed their efficiency in population, species, and sex differentiation. Overall we identified 74 compounds in cuticular extracts of the selected taxa. Linear alkanes and unsaturated hydrocarbons were prominent, with ten compounds between them explaining 85.6% of species dissimilarity. Although the cuticular chemical profiles efficiently differentiated all investigated taxa, only C. ohausiana showed significant cuticular profile differences between sexes. Our analysis also revealed two E. emarginata clades within a larger group of ‘Cyclocephala’ species, but they were not aligned with the two studied populations. Our research underscores the significance of cuticular lipid profiles in distinguishing selected cyclocephaline beetle species and contemplates their potential impact as contact pheromones on sexual segregation and speciation.

Keywords

alkeneschemotaxonomycontact pheromonesflorivorypollinationscarabaeidae
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 114 , Issue 1 , February 2024 , pp. 124 - 133
Check for updates
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albuquerque, LSCD, Grossi, PC and Iannuzzi, L (2016) Flight patterns and sex ratio of beetles of the subfamily Dynastinae (Coleoptera, Melolonthidae). Revista Brasileira de Entomologia 60, 248–254.CrossRefGoogle Scholar
Bagnères, A-G and Wicker-Thomas, C (2010) Introduction: history and overview of insect hydrocarbons. In Blomquist, GJ and Bagnères, A-G (eds), Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. New York, USA: Cambridge University Press, pp. 3–18.Google Scholar
Barros, RP, Astúa, D, Grossi, PC, Iannuzzi, L and Maia, ACD (2020) Landmark-based geometric morphometrics as a tool for the characterization of biogeographically isolated populations of the pollinator scarab beetle Erioscelis emarginata (Coleoptera: Melolonthidae). Zoologischer Anzeiger 288, 97–102.CrossRefGoogle Scholar
Beach, JH (1982) Beetle pollination of Cyclanthus bipartitus (Cyclanthaceae). American Journal of Botany 69, 1074–1081.CrossRefGoogle Scholar
Blomquist, GJ (2010) Structure and analysis of insect hydrocarbons. In Blomquist, GJ and Bagnères, A-G (eds), Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. New York, USA: Cambridge University Press, pp. 19–34.CrossRefGoogle Scholar
Brückner, A and Heethoff, M (2017) A chemo-ecologists’ practical guide to compositional data analysis. Chemoecology 27, 33–46.CrossRefGoogle Scholar
Caselli, A, Favaro, R, Petacchi, R, Valicenti, M and Angeli, S (2023) The cuticular hydrocarbons of Dasineura oleae show differences between sex, adult age and mating status. Journal of Chemical Ecology 49, 369–383.CrossRefGoogle ScholarPubMed
Costa, MS, Silva, RJ, Paulino-Neto, HF and Pereira, MJB (2017) Beetle pollination and flowering rhythm of Annona coriacea Mart.(Annonaceae) in Brazilian cerrado: behavioral features of its principal pollinators. PLoS One 12, e0171092.CrossRefGoogle ScholarPubMed
Dahbi, A, Cerdá, X, Hefetz, A and Lenoir, A (1996) Social closure, aggressive behavior, and cuticular hydrocarbon profiles in the polydomous ant Cataglyphis iberica (Hymenoptera, Formicidae). Journal of Chemical Ecology 22, 2173–2186.CrossRefGoogle Scholar
El-Sayed, AM (2023) The Pherobase: Database of Pheromones and Semiochemicals. Available at https://www.pherobase.comGoogle Scholar
Endrödi, S (1985) The Dynastinae of the World (Series Entomologica V. 28). Hungary: Budapest: Dr W. Junk Publishers.Google Scholar
Fletcher, MT, Allsopp, PG, McGrath, MJ, Chow, S, Gallagher, OP, Hull, C, Cribb, BW, Moore, CJ and Kitching, W (2008) Diverse cuticular hydrocarbons from Australian canebeetles (Coleoptera: Scarabaeidae). Australian Journal of Entomology 47, 153–159.CrossRefGoogle Scholar
Francis, GW and Veland, K (1987) Alkylthiolation for the determination of double-bond positions in linear alkenes. Journal of Chromatography A 219, 379–384.CrossRefGoogle Scholar
Garwood, RJ and Edgecombe, GD (2011) Early terrestrial animals, evolution, and uncertainty. Evolution: Education and Outreach 4, 489–501.Google Scholar
Gibernau, M (2015) Pollination ecology of two Dieffenbachia in French Guiana. Aroideana 38E, 38–66.Google Scholar
Gibernau, M and Barabé, D (2002) Pollination ecology of Philodendron squamiferum (Araceae). Canadian Journal of Botany 80, 316–320.CrossRefGoogle Scholar
Gibernau, M, Barabé, D, Cerdan, P and Dejean, A (1999) Beetle pollination of Philodendron solimoesense (Araceae) in French Guiana. International Journal of Plant Sciences 160, 1135–1143.CrossRefGoogle ScholarPubMed
Gibernau, M, Barabé, D, Labat, D, Cerdan, P and Dejean, A (2003) Reproductive biology of Montrichardia arborescens (Araceae) in French Guiana. Journal of Tropical Ecology 19, 103–107.CrossRefGoogle Scholar
Ginzel, MD (2010) Hydrocarbons as contact pheromones of longhorned beetles (Coleoptera: cerambycidae). In Blomquist, GJ and Bagnères, A-G (eds), Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. New York, USA: Cambridge University Press, pp. 375–389.CrossRefGoogle Scholar
Gottsberger, G and Silberbauer-Gottsberger, I (1991) Olfactory and visual attraction of Erioscelis emarginata (Cyclocephalini, Dynastinae) to the inflorescences of Philodendron selloum (Araceae). Biotropica 23, 23–28.CrossRefGoogle Scholar
Greene, MJ and Gordon, DM (2003) Cuticular hydrocarbons inform task decisions. Nature 423, 32–32.CrossRefGoogle ScholarPubMed
Hadley, NF (1980) Surface waxes and integumentary permeability: lipids deposited on or associated with the surface of terrestrial plants and animals help protect them from a lethal rate of desiccation. American Scientist 68, 546–553.Google Scholar
Hammer, Ø, Harper, DA and Ryan, PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 9.Google Scholar
Hartke, J, Sprenger, PP, Sahm, J, Winterberg, H, Orivel, J, Baur, H, Beuerle, T, Schmitt, T, Feldmeyer, B and Menzel, F (2019) Cuticular hydrocarbons as potential mediators of cryptic species divergence in a mutualistic ant association. Ecology and Evolution 9, 9160–9176.CrossRefGoogle Scholar
Henderson, A (1986) A review of pollination studies in the Palmae. The Botanical Review 52, 221–259.CrossRefGoogle Scholar
Hirai, Y, Akino, T, Wakamura, S and Arakaki, N (2008) Morphological and chemical comparison of males of the white grub beetle Dasylepida ishigakiensis (Coleoptera: Scarabaeidae) among four island populations in the Sakishima Islands of Okinawa. Applied Entomology and Zoology 43, 65–72.CrossRefGoogle Scholar
Howard, RW and Blomquist, GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annual Review of Entomology 50, 371–393.CrossRefGoogle ScholarPubMed
Ingleby, FC (2015) Insect cuticular hydrocarbons as dynamic traits in sexual communication. Insects 6, 732–742.CrossRefGoogle ScholarPubMed
Jutsum, AR, Saunders, TS and Cherrett, JM (1979) Intraspecific aggression is the leaf-cutting ant Acromyrmex octospinosus. Animal Behavior 27, 839–844.CrossRefGoogle Scholar
Kather, R and Martin, SJ (2012) Cuticular hydrocarbon profiles as a taxonomic tool: advantages, limitations and technical aspects. Physiological Entomology 37, 25–32.CrossRefGoogle Scholar
Lagomarsino, LP and Frost, LA (2020) The central role of taxonomy in the study of neotropical biodiversity. Annals of the Missouri Botanical Garden 105, 405–421.CrossRefGoogle Scholar
Liang, D and Silverman, J (2000) “You are what you eat”: diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87, 412–416.CrossRefGoogle Scholar
Lockey, KH (1988) Lipids of the insect cuticle: origin, composition and function. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 89, 595–645.CrossRefGoogle Scholar
Lockey, KH (1991) Insect hydrocarbon classes: implications for chemotaxonomy. Insect Biochemistry 21, 91–97.CrossRefGoogle Scholar
Lyal, C, Kirk, P, Smith, D and Smith, R (2008) The value of taxonomy to biodiversity and agriculture. Biodiversity 9, 8–13.CrossRefGoogle Scholar
Maia, ACD, Schlindwein, C, Navarro, DMAF and Gibernau, M (2010) Pollination of Philodendron acutatum (Araceae) in the Atlantic forest of northeastern Brazil: a single scarab beetle species guarantees high fruit set. International Journal of Plant Sciences 171, 740–748.CrossRefGoogle Scholar
Maia, AC, Dötterl, S, Kaiser, R, Silberbauer-Gottsberger, I, Teichert, H, Gibernau, M, do Amaral Ferraz Navarro, DM, Schlindwein, C and Gottsberger, G (2012) The key role of 4-methyl-5-vinylthiazole in the attraction of scarab beetle pollinators: a unique olfactory floral signal shared by Annonaceae and Araceae. Journal of Chemical Ecology 38, 1072–1080.Google ScholarPubMed
Maia, ACD, Gibernau, M, Carvalho, AT, Gonçalves, EG and Schlindwein, C (2013) The cowl does not make the monk: scarab beetle pollination of the Neotropical aroid Taccarum ulei (Araceae: Spathicarpeae). Biological Journal of the Linnean Society 108, 22–34.CrossRefGoogle Scholar
Maia, ACD, Santos, GKN, Gonçalves, EG, Navarro, DMDAF and Nuñez-Avellaneda, LA (2018) 2-Alkyl-3-methoxypyrazines are potent attractants of florivorous scarabs (Melolonthidae, Cyclocephalini) associated with economically exploitable Neotropical palms (Arecaceae). Pest Management Science 74, 2053–2058.CrossRefGoogle Scholar
Maia, ACD, Reis, LK, Navarro, DM, Aristone, F, Colombo, CA, Carreño‐Barrera, J, Núñez‐Avellaneda, LA and Santos, GK (2020) Chemical ecology of Cyclocephala forsteri (Melolonthidae), a threat to macauba oil palm cultivars (Acrocomia aculeata, Arecaceae). Journal of Applied Entomology 144, 33–40.CrossRefGoogle Scholar
Moore, MR (2011) Disentangling the phenotypic variation and pollination biology of the Cyclocephala sexpunctata species complex (Coleoptera: Scarabaeidae: Dynastinae) (Unpublished MSc thesis). Wichita State University.Google Scholar
Moore, MR and Jameson, ML (2013) Floral associations of cyclocephaline scarab beetles. Journal of Insect Science 13, 100.CrossRefGoogle ScholarPubMed
Moore, MR, Cave, RD and Branham, MA (2018a) Annotated catalog and bibliography of the cyclocephaline scarab beetles (Coleoptera, Scarabaeidae, Dynastinae, Cyclocephalini). ZooKeys 745, 101–378.CrossRefGoogle Scholar
Moore, MR, Cave, RD and Branham, MA (2018b) Synopsis of the cyclocephaline scarab beetles (Coleoptera, Scarabaeidae, Dynastinae). ZooKeys 745, 1–99.CrossRefGoogle Scholar
Morel, L, Vander Meer, RK and Lavine, BK (1988) Ontogeny of nestmate recognition cues in the red carpenter ant (Camponotus floridanus). Behavioral Ecology and Sociobiology 22, 175–183.CrossRefGoogle Scholar
Neita-Moreno, JC (2021) A review of the black species of Cyclocephala Dejean (Coleoptera: Scarabaeidae: Dynastinae) from Colombia. Zootaxa 5026, 1–58.CrossRefGoogle ScholarPubMed
Niogret, J, Felix, AE, Nicot, A and Lumaret, JP (2019) Chemosystematics using cuticular compounds: a powerful tool to separate species in Mediterranean dung beetles (Coleoptera: Geotrupidae). Journal of Insect Science 19, 18.CrossRefGoogle ScholarPubMed
Nóbrega, RL, Maia, ACD, Lima, CHM, Felix, KES, Souza, TB and Pontes, WJT (2022) Behavioral traits and sexual recognition: multiple signaling in the reproductive behavior of Cyclocephala distincta (Melolonthidae, Cyclocephalini). Anais da Academia Brasileira de Ciências 94, e20200694.CrossRefGoogle ScholarPubMed
Nogueira, GAL, Rodrigues, SR and Tiago, EF (2013) Biological aspects of Cyclocephala tucumana Brethes, 1904 and Cyclocephala melanocephala (Fabricius, 1775) (Coleoptera: Scarabaeidae). Biota Neotropica 13, 86–90.CrossRefGoogle Scholar
Núñez Avellaneda, LA (2014) Patrones de asociación entre insectos polinizadores y palmas silvestres en Colombia con énfasis en palmas de importancia económica (Unpublished PhD thesis). Universidad Nacional de Colombia.Google Scholar
Oliveira, HN and Ávila, CJ (2011) Ocorrência de Cyclocephala forsteri em Acronomia aculeata. Pesquisa Agropecuária Tropical 41, 293–295.CrossRefGoogle Scholar
Parizotto, DR and Grossi, PC (2019) Revisiting pollinating Cyclocephala scarab beetles (Coleoptera: Melolonthidae: Dynastinae) associated with the soursop (Annona muricata, Annonaceae). Neotropical Entomology 48, 415–421.CrossRefGoogle ScholarPubMed
Potter, DA and Haynes, KF (1993) Field-testing pheromone traps for predicting masked chafer (Coleoptera: Scarabaeidae) grub density in golf course turf and home lawns. Journal of Entomological Science 28, 205–212.CrossRefGoogle Scholar
Ratcliffe, BC, Cave, RD and Cano, E (2013) The dynastine scarab beetles of Mexico, Guatemala, and Belize (Coleoptera: Scarabaeidae). Bulletin of the University of Nebraska State Museum 27, 1–666.Google Scholar
Ratcliffe, BC, Cave, RD and Paucar-Cabrera, A (2020) The dynastine scarab beetles of Ecuador (Coleoptera: Scarabaeidae: Dynastinae). Bulletin of the University of Nebraska State Museum 32, 1–586.Google Scholar
Rodrigues, SR, Nogueira, GA, Echeverria, RR and Oliveira, VS (2010) Aspectos biológicos de Cyclocephala verticalis Burmeister (Coleoptera: Scarabaeidae). Neotropical Entomology 39, 15–18.CrossRefGoogle Scholar
Santos, MD (2014) Revisão do grupo “latericia” do gênero Cyclocephala Dejean, 1821 (Melolonthidae, Dynastinae, Cyclocephalini) (Unpublished BSc dissertation). Universidade Federal do Paraná.Google Scholar
Santos, V and Ávila, CJ (2007) Aspectos bioecológicos de Cyclocephala forsteri Endrodi, 1963 (Coleoptera: Melolonthidae) no estado do Mato Grosso do Sul. Brazilian Journal of Agriculture 82, 298–303.Google Scholar
Scariot, AO, Lleras, E and Hay, JD (1991) Reproductive biology of the palm Acrocomia aculeata in Central Brazil. Biotropica 23, 12–22.CrossRefGoogle Scholar
Schulz, S and Möllerke, A (2022) MACE – an open access data repository of mass spectra for chemical ecology. Journal of Chemical Ecology 48, 589–597.CrossRefGoogle ScholarPubMed
Scott, MP, Madjid, K and Orians, CM (2008) Breeding alters cuticular hydrocarbons and mediates partner recognition by burying beetles. Animal Behaviour 76, 507–513.CrossRefGoogle Scholar
Singer, TL (1998) Roles of hydrocarbons in the recognition systems of insects. American Zoologist 38, 394–405.CrossRefGoogle Scholar
Soon, V, Castillo-Cajas, RF, Johansson, N, Paukkunen, J, Rosa, P, Ødegaard, F, et al. (2021) Cuticular hydrocarbon profile analyses help clarify the species identity of dry-mounted cuckoo wasps (Hymenoptera: Chrysididae), including type material, and reveal evidence for a cryptic species. Insect Systematics and Diversity 5, 3.CrossRefGoogle Scholar
Souza, TB, Maia, ACD, Schlindwein, C, Albuquerque, LSC and Iannuzzi, L (2014) The life of Cyclocephala celata Dechambre, 1980 (Coleoptera: Scarabaeidae: Dynastinae) in captivity with descriptions of the immature stages. Journal of Natural History 48, 275–283.CrossRefGoogle Scholar
Steiger, S and Stökl, J (2014) The role of sexual selection in the evolution of chemical signals in insects. Insects 5, 423–438.CrossRefGoogle ScholarPubMed
Thomas, ML and Simmons, LW (2008) Sexual dimorphism in cuticular hydrocarbons of the Australian field cricket Teleogryllus oceanicus (Orthoptera: Gryllidae). Journal of Insect Physiology 54, 1081–1089.CrossRefGoogle ScholarPubMed
van Den Dool, H and Kratz, PD (1963) A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. Journal of Chromatography 11, 463–471.CrossRefGoogle Scholar
van Zweden, JS and d'Ettorre, P (2010) The role of hydrocarbons in nestmate recognition. In Blomquist, GJ and Bagnères, A-G (eds), Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. New York, USA: Cambridge University Press, pp. 222–243.CrossRefGoogle Scholar
Wagner, D, Brown, MJ, Broun, P, Cuevas, W, Moses, LE, Chao, DL and Gordon, DM (1998) Task-related differences in the cuticular hydrocarbon composition of harvester ants, Pogonomyrmex barbatus. Journal of Chemical Ecology 24, 2021–2037.CrossRefGoogle Scholar
Young, HJ (1986) Beetle pollination of Dieffenbachia longispatha (Araceae). American Journal of Botany 73, 931–944.CrossRefGoogle Scholar
Supplementary material: File

Santos et al. supplementary material

Santos et al. supplementary material
Download Santos et al. supplementary material(File)
File 95 KB