Strata Use in a Canopy Beetle Community of a Lowland Neotropical Rainforest in Southern Venezuela

Abstract

Stratification of tropical rainforests and their arthropods is highly pronounced. I hypothesize that the occurrence of rainforest canopy beetles in the understory is not random but related to the ecology of the taxa, such as feeding guilds and larval development. Therefore, the ecological characteristics of stratum generalists recorded in both the canopy and the lower understory were analyzed. Adult beetles were collected manually and with traps in the northern part of the Amazonian rainforest for a cumulative year. Seventy out of a total of 862 canopy beetle species from 45 families associated with 23 tree species were shared between both strata. The beetle families represented by most species in the canopy and ground samples were Curculionidae, Chrysomelidae, and Carabidae. For Elateridae and Scarabaeidae, the proportion of shared species between the strata was ≥20%. In contrast, the species-rich families (≥20 canopy species) Cerambycidae, Mordellidae, and Buprestidae did not comprise species sampled in both strata. Thus, beetle families comprising many stratum generalists are either largely predatory, or their larvae often develop in the soil.

Keywords

Biodiversity / Amazonas / Canopy crane / Specialization / Coleoptera / Tropical ecology / Guilds / Diel activity

Acknowledgments

The Austrian Academy of Sciences and colleagues are acknowledged for their support and permission to join the Surumoni Project in Venezuela. I cordially thank Jens Wesenberg for assistance in all botanical matters and field work. I am delighted for the identification of beetles by Joachim Adis (Solenogenys funkei Adis); Erik Arndt (Notiobia Perty); Shawn M. Clark, Wills Flowers, David Furth, and Lev N. Medvedev (Chrysomelidae); Paul J. Johnson (Elateridae); Martin Lillig (Tenebrionidae); Alistair S. Ramsdale (Cantharidae); Brett C. Ratcliffe (Scarabaeidae); Sergio Antonio Vanin (Curculionidae); and Vadim R. Viviani (Lampyridae). I appreciate the four reviewers for their constructive feedback, which helped to improve this paper significantly. Leopoldina, Germany, supported this study through scientific, financial, and logistic means.

Author Contributions

The author is responsible for conceptualization, methodology, analysis, investigation, writing of the manuscript and editing.

Ethics Statement

This article does not present research with ethical considerations. Permit: license and authorization for the beetle survey were issued under the number 15-1277 by Servicio Autonoma de Fauna, Ministerio del Ambiente de los Recusos Naturales Renovables, Caracas, Venezuela.

Informed Consent Statement

Not applicable.

Data Availability Statement

The canopy beetle dataset is available at https://doi.org/10.5061/dryad.kprr4xhc7 [62]. All other data produced in this study are provided in this manuscript.

Funding

The fieldwork was supported, in part, by grants from the ESF Tropical Canopy Programme and the Stiftung der Deutschen Wirtschaft, Germany. Funding for this study is provided by The Royal Society, London, UK.

Declaration of Competing Interest

The author declares that she has no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

[1] Nakamura A, Kitching RL, Cao M, Creedy TJ, Fayle TM, Freiberg M, et al. Forests and their canopies: Achievements and horizons in canopy science. Trends Ecol. Evol. 2017, 32, 438-451. doi:10.1016/j.tree.2017.02.020.

[2] Basset Y. Invertebrates in the canopy of tropical rain forests: How much do we really know? Plant Ecol. 2001, 153, 87-107.

[3] Davis AJ, Sutton SL. Estimating species richness through three dimensions. Sepilok Bull. 2012, 15, 69-83.

[4] Ashton LA, Nakamura A, Basset Y, Burwell CJ, Cao M, Eastwood R, et al. Vertical stratification of moths across elevation and latitude. J. Biogeogr. 2016, 43, 59-69.

[5] Somavilla A, Moraes Junior RNM, Rafael JA. Is the social wasp fauna in the tree canopy different from the understory? Study of a particular area in the Brazilian Amazon Rainforest. Sociobiology 2019, 66, 179-185. doi:10.13102/sociobiology.v66i1.3568.

[6] Stork NE, Grimbacher PS. Beetle assemblages from an Australian tropical rainforest show that the canopy and the ground strata contribute equally to biodiversity. Proc. R. Soc. B 2006, 273, 1969-1975.

[7] Basset Y, Hammond PM, Barrios H, Holloway JD, Miller SE. Vertical stratification of arthropod assemblages. In Arthropods of Tropical Forests. Spatio-Temporal Dynamics and Resource Use in the Canopy; Basset Y, Novotny V, Miller SE, Kitching RL,Eds.; Cambridge University Press: Cambridge, UK, 2003; pp. 17-27.

[8] Stork NE, McBroom J, Gely C, Hamilton A. New approaches narrow global species estimates for beetles, insects, and terrestrial arthropods. Proc. Natl. Acad. Sci. USA 2015, 112, 7519-7523.

[9] Basset Y, Cizek L, Cuénoud P, Didham RK, Novotny V, Ødegaard F, et al. Arthropod Distribution in a Tropical Rainforest: Tackling a Four Dimensional Puzzle. PLoS ONE 2015, 10, e0144110. doi:10.1371/journal.pone.0144110.

[10] WaIter DE. Dancing on the head of a pin: mites in the rainforest canopy. Rec. Aust. Mus. 1995, 52, 49-53.

[11] Rogers DJ, Kitching RL. Vertical stratification of rainforest collembolan (Collembola: Insecta) assemblages: Description of ecological patterns and hypotheses concerning their generation. Ecography 1998, 21, 392-400.

[12] Amorim DS, Brown BV, Boscolo D, Ale-Rocha R, Alvarez-Garcia DM, Balbi MIPA, et al. Vertical stratification of insect abundance and species richness in an Amazonian tropical forest. Sci. Rep. 2022, 12, 1734. doi:10.1038/s41598-022-05677-y.

[13] Brühl CA, Gunsalam G, Linsenmair KE. Stratification of ants (Hymenoptera, Formicidae) in a primary rain forest in Sabah. Borneo. J. Trop. Ecol. 1998, 14, 285-297.

[14] DeVries PJ, Alexander LG, Chacon IA, Fordyce JA. Similarity and difference among rainforest fruit-feeding Butterfly communities in Central and South America. J. Anim. Ecol. 2012, 81, 472-482. doi:10.1111/j.1365-2656.2011.01922.x.

[15] Mena S, Kozak KM, Cárdenas RE, Checa MF. Forest stratification shapes allometry and flight morphology of tropical butterflies. Proc. R. Soc. B 2020, 287, 20201071. doi:10.1098/rspb.2020.1071.

[16] Basset Y, Aberlenc HP, Barrios H, Curletti G, Béranger JM, Vesco JP, et al. Stratification and diel activity of arthropods in a lowland rain forest in Gabon. Biol. J. Linn. Soc. 2001, 72, 585-607.

[17] Frenne PD, Zellweger F, Rodríguez-Sánchez F, Scheffers BR, Hylander K, Luoto M, et al. Global buffering of temperatures under forest canopies. Nat. Ecol. Evol. 2019, 3, 744-749. doi:10.1038/s41559-019-0842-1.

[18] Hallé F.Distribution verticale des métabolites secondaires en forêt équatoriale—une hypothèse. In Biologie d’une Canopée de Forêt Equatoriale—III. Rapport de la Mission d’ Exploration Scientifique de la Canopée de Guyane, Octobre—Décembre 1996; Hallé F, Ed.; Pro-Natura International & Opération Canopée: Paris, France, 1998; pp. 129-138.

[19] Szarzynski J, Anhuf D. Micrometerological conditions and canopy energy exchanges of a neotropical rain forest (Surumoni-Crane Project, Venezuela). Plant Ecol. 2001, 153, 231-239.

[20] Cunningham-Minnick MJ, Roberts HP, Milam J, King DI. Sampling the understory, midstory, and canopy is necessary to fully characterize native bee communities of temperate forests and their dynamic environmental relationships. Front. Ecol. Evol. 2024, 12, 1352266. doi:10.3389/fevo.2024.1352266.

[21] Leksono AS,Nakagoshi N. A review of Vertical and Spatial Variations of Canopy Insects. In Secondary Forests in Central Japan and East Java, Indonesia, Proceeding of 6th ICGRC International Conference on Global Resource Conservation (ICGRC), Malang, Indonesia, 30 November 2015; ICGRC: Malang, Indonesia, 2015; pp. 21-25.

[22] Normann C, Tscharntke T, Scherber C. Interacting effects of forest stratum, edge and tree diversity on beetles. For. Ecol. Manage. 2016, 361, 421-431. doi:10.1016/j.foreco.2015.11.002.

[23] Weiss M, Didham RK, Procházka J, Schlaghamerský J, Basset Y, Odegaard F, et al. Saproxylic beetles in tropical and temperate forests-A standardized comparison of vertical stratification patterns. For. Ecol. Manag. 2019, 444, 50-58. doi:10.1016/j.foreco.2019.04.021.

[24] Ulyshen MD, Hanula JL. A Comparison of the Beetle (Coleoptera) Fauna Captured at Two Heights Above the Ground in a North American Temperate Deciduous Forest. Am. Midl. Nat. 2007, 158, 260-278.

[25] Hardersen S, Curletti G, Leseigneur L, Platia G, Liberti G, Leo P, et al. Spatio-temporal analysis of beetles from the canopy and ground layer in an Italian lowland forest. Bull. Insectology 2014, 67, 87-97.

[26] Lawrence E. Henderson’s Dictionary of Biology; Pearson Benjamin Cummings: Harlow, UK, 2008.

[27] King DA, Wright SJ, Connell JH. The contribution of interspecific variation in maximum tree height to tropical and temperate diversity. J. Trop. Ecol. 2006, 221, 11e24.

[28] Yamakura T. An empirical approach to the analysis of forest stratification. I. Proposed graphical method derived by using an empirical distribution function. Bot. Mag. Tokyo 1987, 100, 109e128. doi:10.1007/BF02488317.

[29] LaFrankie JV, Ashton PS, Chuyong GB, Co L, Condit R, Davies SJ, et al.Contrasting structure and composition of the understory in species-rich tropical rain forests. Ecology 2006, 87, 2298-2305.

[30] Draper FC, Costa FRC, Arellano G, Phillips OL, Duque A, Macía MJ, et al. Amazon tree dominance across forest strata. Nat. Ecol. Evol. 2020, 5, 757-767.

[31] Laurans M, Hérault B, Vieilledent G, Vincent G. Vertical stratification reduces competition for light in dense tropical forests. Ecol. Manag. 2014, 329, 79-88.

[32] Wesenberg J. Blühphänologie im Kronenraum eines tropischen Tieflandregenwaldes am Oberen Orinoco, Amazonas, Venezuela. Doctoral Dissertation, Fakultät für Biowissenschaften, Pharmazie und Psychologie, Universität Leipzig, Leipzig, Germany, 2004.

[33] Prance GT. Notes on the vegetation of Amazonia III. The terminology of Amazonian forest types subject to inundation. Brittonia 1979, 31, 26-38.

[34] Grimbacher PS, Stork NE. Vertical stratification of feeding guilds and body size in beetle assemblages from an Australian tropical rainforest. Austral Ecol. 2007, 32, 77-85. doi:10.1111/j.1442-9993.2007.01735.x.

[35] Sobek S, Tscharntke T, Scherber C, Schiele S, Steffan-Dewenter I. Canopy vs. understory: Does tree diversity affect bee and wasp communities and their natural enemies across forest strata? For. Ecol. Manag. 2009, 258, 609-615. doi:10.1016/j.foreco.2009.04.026.

[36] Berkov A, Tavakilian G. Host utilization of the Brazil nut family (Lecythidaceae) by sympatric woodboring species of Palame (Coleoptera, Cerambycidae, Lamiinae, Acanthocinini). Biol. J. Linn. Soc. 1999, 67, 181-198.

[37] Floren A. Sampling arthropods from the canopy by insecticidal knockdown. In Manual on Field Recording Techniques and Protocols for All Taxa Biodiversity Inventories, Part 1, Vol. 8; Eymann J, Degref J, Häuser C, Monje JC, Samyn Y, VandenSpiegel D,Eds.; ABC Taxa: Bruselles, Belgium, 2010; pp. 158-172.

[38] Watanabe M, Nagamitsu T, Itioka T, Meleng P, Kojima H. Species Diversity and Vertical Distributions of Weevils (Coleoptera, Curculionidae) Collected by Collision Traps with Floral-fragrance Attractants in a Bornean Rainforest. Elytra 2017, 7, 491-498.

[39] Medianero E, Valderrama A, Barrios H. Diversidad de insectos minadores y formadores de agallas en el dosel y sotobosque del bosque tropical. Acta Zool. Mex. 2003, 1, 153-168.

[40] Barrios H. Insect herbivores feeding on conspecific seedlings and trees. In Arthropods of Tropical Forests. Spatio-Temporal Dynamics and Resource Use in the Canopy; Basset Y, Novotny V, Miller SE, Kitching RL,Eds.; Cambridge University Press: Cambridge, UK, 2003; pp. 282-290.

[41] Nagamitsu T, Momose K, Inoue T, Roubik DW. Preference in flower visits and partitioning in pollen diets of stingless bees in an Asian tropical rain forest. Res. Popul. Ecol. 1999, 41, 195-202. doi:10.1007/s101440050023.

[42] Ramalho M. Stingless bees and mass flowering trees in the canopy of Atlantic forest: a tight relationship. Acta Bot. Bras. 2004, 18, 37-47. doi:10.1590/s0102-33062004000100005.

[43] Ulyshen MD, Soon V, Hanula JL. On the vertical distribution of bees in a temperate deciduous forest. Insect Conserv. Diver. 2010, 3, 222-228. doi:10.1111/j.1752-4598.2010.00092.x.

[44] Oliveira BF, Scheffers BR. Vertical stratification influences global patterns of biodiversity. Ecography 2019, 42, 249-249. doi:10.1111/ecog.03636.

[45] Schleuning M, Blüthgen N, Flörchinger M, Braun J, Schaefer H, Böhning-Gaese K. Specialization and interaction strength in a tropical plant-frugivore network differ among forest strata. Ecology 2011, 92, 26-36.

[46] Kirmse S. Diel activity patterns of a canopy-inhibiting beetle community (Coleoptera) in a Neotropical rainforest. Fron. For. Glob. Chang. 2024, 7, 1370044. doi:10.3389/ffgc.2024.1370044.

[47] Anhuf D, Motzer T, Rollenbeck R, Schröder B, Scarzynski J. Water budget of the Surumoni crane site (Venezuela). Selbyana 1999, 20, 179-185.

[48] Anhuf D, Winkler H. Geographical and ecological settings of the Surumoni-Crane-Project 784 (Upper Orinoco, Estado Amazonas, Venezuela). Anz. Akad. Wiss. Wien, Math. Naturwiss. Kl. I 1999, 135, 3-23.

[49] Morrone JJ. Monograph biogeographical regionalisation of the Neotropical region. Zootaxa 2014, 3782, 1-110. doi:10.11646/zootaxa.3782.1.1.

[50] Kirmse S. Beetle diversity (Coleoptera) in the canopy of a tropical lowland rainforest in Venezuela. PeerJ 2024, accepted.

[51] Lamarre GPA, Molto Q, Fine PVA, Baraloto C. A comparison of two common flight interception traps to survey tropical arthropods. ZooKeys 2012, 216, 43-55.

[52] Riley KNP, Browne RA, Erwin TL. Carabid beetle (Coleoptera, Carabidae) richness, diversity, and community structure in the understory of temporarily flooded and non-flooded Amazonian forests of Ecuador. ZooKeys 2021, 1044, 831-876. doi:10.3897/zookeys.1044.62340.

[53] Russo L, Stehouwer R, Heberling JM, Shea K. The composite insect trap: an innovative combination trap for biologically diverse sampling. PLoS ONE 2011, 6, e21079. doi:10.1371/journal.pone.0021079.

[54] Arndt E, Kirmse S. Seed-feeding ground beetle communities (Coleoptera: Carabidae: Harpalini) on fruit falls of Miconia and Goupia in South Venezuela. Stud. Neotrop. Fauna Environ. 2002, 37, 151-157.

[55] Paarmann W, Adis J, Stork N, Gutzmann B, Stumpe P, Staritz B, et al. The structure of ground beetle assemblages (Coleoptera: Carabidae) at fig fruit falls (Moraceae) in a terra firme rain forest near Manaus (Brazil). Ecotropica 2001, 17, 549-561.

[56] Hoekman D, LeVan KE, Ball GE, Browne RA, Davidson RL, Erwin TL, et al. Design for ground beetle abundance and diversity sampling within the National Ecological Observatory Network. Ecosphere 2017, 8, e01744. doi:10.1002/ecs2.1744.

[57] Jarosík V. Pitfall trapping and species abundance relationships: a value for carabid beetles (Coleoptera: Carabidae). Acta Entomol. Bohemoslov. 1992, 89, 1-12.

[58] Mommertz S, Schauer C, Kösters N, Lang A, Filser J. A comparison of D-vacsuction, fenced and unfenced pitfall trap sampling of epigeal arthropods in agroecosystems. Ann. Zool. Fennici 1996, 33, 117-124.

[59] Kirmse S. Structure and composition of a canopy-beetle community (Coleoptera) in a Neotropical lowland rainforest in southern Venezuela. R. Soc. Open Sci. 2024, 11, 240478. doi:10.1098/rsos.240478.

[60] Reichardt H. A synopsis of the genera of neotropical Carabidae (Insecta: Coleoptera). Quaest. Entomol. 1977, 13, 346-493.

[61] Bouchard P, Bousquet Y, Davies AE, Alonso-Zarazaga MA, Lawrence JF, Lyal CHC, et al. Family-group names in Coleoptera (Insecta). ZooKeys 2011, 88, 1-972.

[62] Kirmse S. Beetle diversity on 23 canopy-tree species in the Amazonas (dataset). Dryad Digit. Repos. 2024. doi:10.5061/dryad.kprr4xhc7.

[63] Hammer Ø, Harper DAT, Ryan PD. PAST: Palaeontological statistics software package for education and data analysis. Palaeontol. Electron. 2001, 4, 9.

[64] Hammond PM, Stork NE, Brendell MJD. Treecrown beetles in context:A comparison of canopy and other ecotone assemblages in a lowland tropical forest in Sulawesi. In Canopy Arthropods; Stork NE, Adis J, Didham RK,Eds.; Chapman & Hall: London, UK, 1997; pp. 184-223.

[65] Davis AJ, Sutton SL, Brendell MJD. Vertical distribution of beetles in a tropical rainforest in Sulawesi: The role of the canopy in contributing to biodiversity. Sepilok Bull. 2011, 13, 59-83.

[66] McCaig T, Sam L, Nakamura A, Stork NE. Is insect vertical distribution in rainforests better explained by distance from the canopy top or distance from the ground? Biodiv. Conserv. 2019, 29, 1081-1103. doi:10.1007/s10531-019-01927-0.

[67] Kirmse S, Chaboo CS. Flowers are essential to maintain high beetle diversity (Coleoptera) in a Neotropical rainforest canopy. J. Nat. Hist. 2020, 54, 1661-1696. doi:10.1080/00222933.2020.1811414.

[68] Wolda H, OBrien CW, Stockwell HP. Weevil Diversity and Seasonality in Tropical Panama as Deduced from Light-Trap Catches (Coleoptera: Curculionoidea). Smithson. Contrib. Zool. 1998, 590, 79.

[69] Charles E, Basset Y. Vertical stratification of leaf beetle assemblages (Coleoptera: Chrysomelidae) in two forest types in Panama. J. Trop. Ecol. 2005, 21, 329-336.

[70] Arndt E, Beutel RG, Will KW.7.8. Carabidae Latreille, 1802. In Handbook of Zoology, Vol. IV Arthropoda:Insecta. Part 38: Coleoptera, Vol. 1:Morphology and Systematics ( Polyphaga Partim; Kristensen NP, Beutel RG, Leschen RAB,Eds.; Walter De Gruyter: Berlin, Germany; New York, NY, USA, 2005; pp. 119-146.

[71] Bellamy CL, Nelson GH. Chapter 41. Buprestidae (Leach, 1815). In American Beetles: Polyphaga:Scarabaeoidea through Curculionidea; 2; Arnett RH, Thomas RMC, Skelly PE, Frank JL,Eds.; CRC Press LLC: Boca Raton, FL, USA, 2002; pp. 98-112.

[72] Bezark LG, Monné MA. Checklist of the Oxypeltidae, Vesperidae, Disteniidae and Cerambycidae, (Coleoptera) of the Western Hemisphere. 2013. Available online: https://apps2.cdfa.ca.gov/publicApps/plant/bycidDB/wdocuments.asp?w=n. (accessed on 30 August 2024).

[73] Liljeblad E. Monograph of the Family Mordellidae (Coleoptera) of North America, North of Mexico; University of Michigan Press: Ann Arbor, MI, USA, 1945.

[74] Pokon R, Novotny V, Samuelson GA. Host specialization and species richness of root-feeding chrysomelid larvae (Chrysomelidae, Coleoptera) in a New Guinea rain forest. J. Trop. Ecol. 2005, 21, 595-604.

[75] Scholz CH, Chown SL. The evolution of habitat use and diet in Scarabaeoidea:A phylogenetic approach. In Biology, Phylogeny, and Classification of Coleoptera. Papers Celebrating the 80th Birthday of Roy A. Crowson; Pakaluk J, Ślipiński SA,Eds.; Muzeum i Instytut Zoologii PAN: Warszawa, Poland, 1995; pp. 355-374.

[76] Johnson PJ. Elateridae. In American Beetles: Polyphaga: Scarabaeoidea through Curculionidea; Arnett RH, Jr., Thomas MC, Skelley PE, Frank JH,Eds.; CRC Press LLC: Boca Raton, FL, USA, 2002; Volume 2, pp. 160-173.

[77] Jolivet PHAH, Cox ML, Petitpierre E. Novel Aspects of the Biology of Chrysomelidae; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1994.

[78] Kirmse S, Chaboo CS. Polyphagy and florivory prevail in a leaf-beetle community (Coleoptera: Chrysomelidae) inhabiting the canopy of a tropical lowland rainforest in southern Venezuela. J. Nat. Hist. 2018, 52, 2677-2721. doi:10.1080/00222933.2018.1548666.

[79] Erber D. Biology of Camptostomata Clytrinae-Cryptocephalinae-Chlamisinae-Lamprostomatinae. In Biology of Chrysomelidae; Jolivet PA, Petitpierre E, Hsiao TH,Eds.; Kluwer Academic: Dordrecht, The Netherlands; Boston, MA, USA; London, UK, 1988; pp. 513-552.

[80] Jolivet P. Food habits and food selection of Chrysomelidae. Bionomic and evolutionary perspectives. In Biology of Chrysomelidae; Jolivet PA, Petitpierre E, Hsiao TH,Eds.; Springer: Dordrecht, The Netherlands, 1988; pp. 1-24.

[81] Anderson RS. Curculionidae. In American Beetles. Polyphaga: Scarabaeoidea through Curculionoidea; Arnett RH, Jr., Thomas MC, Skelley P,Eds.; CRC Press LLC: Boca Raton, FL, USA, 2002; pp. 722-815.

[82] Berkov A. Chapter 16. Seasonality and Stratification: Neotropical Saproxylic Beetles Respond to a Heat and Moisture Continuum with Conservatism and Plasticity. Saproxylic Insects:Divers. Ecol. Conserv. 2018, 547-578. doi:10.1007/978-3-319-75937-1_16.

[83] Erwin TL. Forest Canopies, Animal Diversity. In Encyclopedia of Biodiversity; Levin SA, Ed.; Academic Press: Waltham, MA, USA, 2013; pp. 511-515.