Abstract
Plant-host-parasitoid assemblages can be extremely variable, involving highly specialized trophic interactions. In this regard, Neotropical host-parasitoid networks remain poorly known due to a lack of studies and rearing programs. Here we describe and quantify for the first time the parasitoid network associated with Diaethria anna and Theritas lisus. Both butterfly species were exclusively feeding on Trema micrantha in cloud forest habitats in Southern Mexico. We reared caterpillars and pupae to determine the associated parasitoids, attack proportions and the trophic relations for each butterfly species. Eight parasitic hymenopterans and four dipteran species emerged from the reared pupae. Parasitoid richness and abundance significantly varied among lepidopterans. Species specificity and partner diversity also differed between butterfly species. The Anna’s Eighty-eight was parasitized by ten different species, resulting in 44% of death. In contrast, T. lisus was attacked by two natural enemies but caused higher mortality (85%). Our results suggest a trade-off between the diversity of parasitoids and mortality for both butterfly species. Quantitative observations of trophic relationships can help us understand the biological processes and changes occurring in complex but fragile networks.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmad F, Aslam M, Razaq M (2003) Chemical ecology of insects and tritrophic interactions. J Res Sci 15:181–190
Arnaud PH (1978) A host-parasite catalog of North American Tachinidae (Diptera). USDA Miscellaneous Publications Hyattsville, MD
Barbosa EP, Kamisnki LA, Freitas AVL (2010) Immature stages of the butterfly Diaethria clymena janeira (Lepidoptera: Nymphalidae: Biblidinae). Zoologia 27:696–702. https://doi.org/10.1590/S1984-46702010000500005
Beccaloni GW, Viloria AL, Hall SK, Robinson GR (2008) Catalogue of the hostplants of the Neotropical butterflies. Monografías 3er Milenio. Zaragoza, Spain
Boggs CL, Watt WB, Ehrlich P (2003) Butterflies. University of Chicago Press, Chicago, IL, Ecology and evolution taking flight
Caldas A, Passos FC (1996) Comments on plant-herbivore-parasitoid interactions in two cerrado areas of southern Brazil. Rev Bras Zool 13:405–410. https://doi.org/10.1590/S0101-81751996000200010
Cagnolo L, Valladares G, Salvo A, Cabido M, Zak M (2009) Habitat fragmentation and species loss across three interacting trophic levels: effects of life-history and food-web traits. Conserv Biol 23:1167–2117. https://doi.org/10.1111/j.1523-1739.2009.01214.x
Cusumano A, Zhu F, Volkoff AN, Verbaaschot P, Bloem J, Vogel H, Dicke M, Poelman EH (2018) Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores. Ecol Lett 21:957–967. https://doi.org/10.1111/ele.12952
De la Maza J (1977) Estudio sobre el género Diaethria Billb. (Lepidoptera: Nymphalidae) en México. Revista De La Sociedad Mexicana De Lepidopterología 3:5–15
De Morales CM, Lewis WJ, Tumlison JH (2000) Examining plant-parasitoid interactions in tritrophic systems. An Soc Entomol Bras 29:189–203. https://doi.org/10.1590/S0301-80592000000200001
Dormann C (2011) How to be a specialist? Quantifying specialisation in pollination networks. Netw Biol 1:1–20
Dormann C, Gruber B, Fruend J (2008) Introducing the bipartite Package: analysing ecological networks. R News 8:8–11
Dyer LA, Wagner DL, Greeney HF et al (2011) Novel insights into tritrophic interaction diversity and chemical ecology using 16 years of volunteer-supported research. Am Entomol 58:15–19. https://doi.org/10.1093/ae/58.1.0015
Fernández F, Sharkey MJ (2006) Introducción a los Hymenoptera de la región Neotropical. Sociedad Colombiana de Entomología y Universidad Nacional de Colombia, Bogotá, Colombia
Fontaine C, Guimaraes PRJr, Kéfi S, Loeuille N, Memmott J, van der Putten WH, van Veen FJ, Thébault E, (2011) The ecological and evolutionary implications of merging different types of networks. Ecol Lett 14:1170–1181. https://doi.org/10.1111/j.1461-0248.2011.01688.x
Gauld ID, Gaston KJ, Janzen DH (1992) Plant allelochemicals, tritrophic interactions and the anomalous diversity of tropical parasitoids: the ‘nasty’ host hypothesis. Oikos 65:53–57. https://doi.org/10.2307/3545032
GBIF (2020a) Theritas lisus (Stoll, 1790). https://www.gbif.org/occurrence/search?q=Theritas%20lisus. Accessed Oct 2020
GBIF (2020b) Diaethria anna Guérin-Meneville, 1844. https://www.gbif.org/occurrence/search?q=Diaethria%20anna. Accessed Oct 2020
Geest EA, Wolfenbarger LL, McCarty JP (2019) Recruitment, survival, and parasitism of monarch butterflies (Danaus plexippus) in milkweed gardens and conservation areas. J Insect Conserv 23:211–224
Gibson GAP, Huber JT, Woolley JB (1997) Annotated keys to the genera of Nearctic Chalcidoidea (Hymenoptera): National Research Council Research Press. Canada, Ottawa
Giunti G, Canale A, Messing RH, Donati E, Stefanini C, Michaud JP, Benelli G (2015) Parasitoid learning: current knowledge and implications for biological control. Biol Control 90:208–219. https://doi.org/10.1016/j.biocontrol.2015.06.007
Glassberg J (2018) A swift guide to butterflies of Mexico and Central America, 2nd edn. Princeton University Press, Princeton, Oxon
Godfray HCJ (1994) Parasitoids: behavioural and evolutionary ecology. Princeton University Press, Princeton, Oxon
Godfray HCJ, Lewis OT, Memmott J (1999) Studying insect diversity in the tropics. Philos Trans R Soc Lond B Biol Sci 354:1811–1824. https://doi.org/10.1098/rstb.1999.0523
Gomina M, Vayssières JF, Kasseney BD, Glitho AI, Amevoin A (2020) Diversity of parasitoids associated with fruit flies on cultivated and wild plants in southern Togo. Int J Trop Insect Sci 40:887–898. https://doi.org/10.1007/s42690-020-00147-2
Hall AR, Scanlan PD, Morgan AW, Buckling A (2011) Host–parasite coevolutionary arms races give way to fluctuating selection. Ecol Lett 14:635–642. https://doi.org/10.1111/j.1461-0248.2011.01624.x
Hassell MP (1985) Insect natural enemies as regulating factors. J Anim Ecol 54:323–334. https://doi.org/10.2307/4641
Hawkins BA (1990) Global patterns of parasitoid assemblage size. J Anim Ecol 59:57–72. https://doi.org/10.2307/5158
Hawkins BA (2005) Pattern and process in host-parasitoid interactions. Cambridge University Press, Cambridge, UK
Henry LM, Roitberg BD (2019) Parasitoids. In: Choe J (ed) Encyclopedia of animal behavior. Academic Press. Seoul, Korea, pp 407–412
Heppner JB (2002) Mexican Lepidoptera biodiversity. Insecta Mundi 16:170–190
Janzen DH, Hallwachs W (2009) Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservación Guanacaste (ACG), northwestern Costa Rica. Available from: http://janzen.sas.upenn.edu/caterpillars/database.lasso. Accessed Oct 2020
Jost L (2006) Entropy and diversity. Oikos 113:363–375. https://doi.org/10.1111/j.2006.0030-1299.14714.x
Julliard R, Clavel J, Devictor V, Jiguet F, Couvet D (2006) Spatial segregation of specialists and generalists in bird communities. Ecology Letters 9: 1237–1244. https://doi.org/10.1111/j.1461-0248.2006.00977.x
Kendall RO, McGuire WW (1984) Some new and rare records of Lepidoptera found in Texas. Bull Allyn Mus 86:1–50
Koul O, Dhaliwal GS (2003) Predators and parasitoids. Taylor & Francis, New York, NY
Krizek GO (1991) Neotropical Nymphalidae in photography. Trop Lepid Res 2:85–102
Krenn HW, Zulka KP, Gatschnegg T (2001) Proboscis morphology and food preferences in nymphalid butterflies (Lepidoptera: Nymphalidae). J Zool 254:17–26. https://doi.org/10.1017/S0952836901000528
Lamas G (2004) Atlas of Neotropical Lepidoptera. Association for Tropical Lepidoptera. Scientific Publishers, Gainesville, FL
La Salle J, Gauld ID (1992) Parasitic Hymenoptera and the biodiversity crisis. Redia (firenze) 74:315–334
Lei GC, Vikberg V, Kuussaari M (2007) The parasitoid complex attacking Finnish populations of the Glanville fritillary Melitaea cinxia (Lep: Nymphalidae), and endangered butterfly. J Nat Hist 31:635–648. https://doi.org/10.1080/00222939700770301
Llorente-Bousquets J, Vargas-Fernández I, Luis-Martínez A, Trujano-Ortega M, Hernández-Mejía BC, Warren AW (2014) Biodiversidad de Lepidoptera en México. Revista Mexicana De Biodiversidad 85:353–371. https://doi.org/10.7550/rmb.31830
Martins ARP, Faynel C, Robbins RK (2016) Variation of male secondary sexual structures and the taxonomy of Theritas lisus and relatives (Lepidoptera, Lycaenidae, Eumaeini). Proc Entomol Soc Wash 118:555–573. https://doi.org/10.4289/0013-8797.118.4.555
McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (1981) Manual of nearctic diptera. Research Branch, Agriculture Canada, Quebec, Canada
Mullen GR, Zaspel JM (2019) Moths and butterflies (Lepidoptera). In Mullen GR, Durden LA, L. A. (eds) Medical and veterinary entomology. Academic Press. San Diego, CA, pp 439–458
Muyshondt A (1973) Notes on the life cycle and natural history of butterflies of El Salvador. I Prepona omphale octavia (Nymphalidae). J Lepid Soc 27: 210-219
Muyshondt A (2005) Notas sobre el ciclo y la historia natural de algunas mariposas de El Salvador. Imprenta universitaria, Universidad de El Salvador, Ciudad universitaria, San Salvador
Naranjo SE, Ellsworth PC, Frisvold GB (2015) Economic value of biological control in integrated pest management of managed plant systems. Annu Rev Entomol 60:32.1–32.25. https://doi.org/10.1146/annurev-ento-010814-021005
New TR (2014) Lepidoptera and conservation. Wiley Blackwell, Melbourne, Australia
O’Hara JE (2013) Taxonomic and host catalogue of the Tachinidae of America north of Mexicohttp://www.nadsdiptera.org/Tach/Nearctic/CatNAmer/Home/CatNAmerhome.html. Accessed Oct 2020
Opedal OH, Ovaskainen O, Saastamoinen M, Laine AL, van Nouhuys S (2020) Host-plant availability drives the spatiotemporal dynamics of interacting metapopulations across a fragmented landscape. Ecology 101:e03186. https://doi.org/10.1002/ecy.3186
Owen DF, Chanter DO (1970) Species diversity and seasonal abundance in tropical Ichneumonidae. Oikos 21:142–144. https://doi.org/10.2307/3543849
Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA (2002) The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu Rev Entomol 47(1):733–771. https://doi.org/10.1146/annurev.ento.47.091201.145257
Quicke DL, Butcher BA (2015) Description of a new Betylobraconini-like parasitoid wasp genus and species (Hymenoptera: Braconidae: Rogadinae) from Chile. Zootaxa 4021(3):459–466. https://doi.org/10.11646/zootaxa.4021.3.5
Rodríguez A, Pohjoismäki JLO, Kouki J (2019) Diversity of forest management promotes parasitoid functional diversity in boreal forests. Biol Conserv 238:108205. https://doi.org/10.1016/j.biocon.2019.108205
Samways MJ (1988) Classical biological control and insect conservation: are they compatible? Environ Conserv 15:349–354. https://doi.org/10.1017/S0376892900029842
Sermeño-Chicas JM, Pérez D, Pérez-Rodríguez CS (2016) Theritas lisus (Stoll, 1790) (Lepidoptera: Lycaenidae) en árboles de paterno (Inga paterno Harms) y almendro de río (Andira inermis (Wright)) en El Salvador. BIOMA 39:7–16
Shaw MR, Hochberg ME (2001) The neglect of parasitic Hymenoptera in insect conservation strategies: the British fauna as a prime example. J Insect Conserv 5:253–263. https://doi.org/10.1023/A:1013393229923
Shaw MR, Stefanescu C, Van Nouhuys S (2009) Parasitoids of European butterflies, 130–156. In J. Settele, T. Shreeve, M. Konvicka, and H. Van Dyck (Eds.), Ecology of butterflies in Europe. Cambridge University Press. UK
Smith MA, Wood DM, Janzen DH, Hallwachs W, Hebert PND (2007) DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. PNAS 104:4967–4972. https://doi.org/10.1073/pnas.0700050104
Smith MA, Rodriguez JJ, Whitfield JM, Deans AR, Janzen DH, Hallwachs W, Hebert PND (2008) Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. PNAS 105:12359–12364. https://doi.org/10.1073/pnas.0805319105
Sow A, Brévault T, Benoit L, Chapuis MP, Galan M, d’acier AC, Delvare G, Sembène M, Harta J (2019) Deciphering host-parasitoid interactions and parasitism rates of crop pests using DNA metabarcoding. Sci Rep 9:3646. https://doi.org/10.1038/s41598-019-40243-z
Stireman JO, Singer MS (2003) What determines host range in parasitoids? An analysis of a tachinid parasitoid community. Oecologia 135:629–638. https://doi.org/10.1007/s00442-003-1235-2
Stireman JO, Dyer LA, Janzen DH et al (2005) Climatic unpredictability and parasitism of caterpillars: implications of global warming. PNAS 102:17384–17387. https://doi.org/10.1073/pnas.0508839102
Stireman JO, O’Hara JE, Wood DM (2006) Tachinidae: evolution, behavior, and ecology. Annu Rev Entomol 51:525–555. https://doi.org/10.1146/annurev.ento.51.110104.151133
Stolarski OC, Gorenstein MR, Lubke M, Lubke L, O’Connor PHP, Campanha BF (2018) Trema micrantha (L.) Blume in plantations for ecological restoration: early development in the Brazilian subtropical forest. Ciência Florestal 28:1217–1229. https://doi.org/10.5902/1980509833351
Team RC (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Townes H (1969) The genera of Ichneumonidae, Part 1. Mem Am Entomol Inst 11:1–300
Townes H (1970a) The genera of Ichneumonidae, Part 2. Mem Am Entomol Inst 12:1–537
Townes H (1970b) The genera of Ichneumonidae, Part 3. Mem Am Entomol Inst 13:1–307
Ueda S, Komatsu T, Itino T, Arai R, Sakamoto H (2016) Host-ant specificity of endangered large blue butterflies (Phengaris spp., Lepidoptera: Lycaenidae) in Japan. Sci Rep 6(1):1–5
Vázquez-Yanes C (1998) Trema micrantha (L.) Blume (Ulmaceae): a promising Neotropical tree for site amelioration of deforested land. Agrofor Syst 40:97–104. https://doi.org/10.1023/A:1006063010677
Vázquez-Yanes C, Batis Muñoz AI, Alcocer-Silva MI, Gual Díaz M, Sánchez-Dirzo C (1999) Árboles y arbustos potencialmente valiosos para la restauración ecológica y la reforestación. Reporte técnico del proyecto J084. CONABIO-Instituto de Ecología, UNAM. CDMX, Mexico
Wajnberg E, Colazza S (2013) Chemical ecology of insect parasitoids. Wiley-Blackwell, Oxford, UK
Wäschke N, Meiners T, Rostás M (2013) Foraging strategies of parasitoids in complex chemical environments, pp. 37–63. In E. Wajnberg, and S. Colazza. (Eds.), Chemical ecology of insect parasitoids. Wiley-Blackwell. Oxford, UK
Williams-Linera G (2002) Tree species richness complementarity, disturbance and fragmentation in a Mexican tropical montane cloud forest. Biodivers Conserv 11:1825–1843. https://doi.org/10.1023/A:1020346519085
Zhang ZQ (2011) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148:1–237. https://doi.org/10.11646/zootaxa.3148.1.2
Acknowledgements
We thank Euridice Tinoco and Avril Manrique, who kindly helped with plant species identification.
Funding
During this work, the authors individually received graduate scholarships from CONACyT. RBM at INECOL (scholarship number 700191) and AFB at CIBNOR (273254) as Ph.D. students.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Appendix
Appendix
Color variation in parasitized pupae of Diaetria anna
Rights and permissions
About this article
Cite this article
Badillo-Montaño, R., Amancio, G., Falcón-Brindis, A. et al. Trophic host-parasitoid interactions of two Neotropical butterfly species in southeastern Mexico. Int J Trop Insect Sci 42, 1865–1875 (2022). https://doi.org/10.1007/s42690-021-00714-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42690-021-00714-1