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Similar host instar preferences by three sympatric parasitoids of Chielomenes sexmaculata (Coleoptera: Coccinellidae): potential host niche overlapping

Published online by Cambridge University Press:  08 January 2025

Chung-Han Cheng Open the ORCID record for Chung-Han Cheng [Opens in a new window]  and
Shaw-Yhi Hwang Open the ORCID record for Shaw-Yhi Hwang [Opens in a new window]
Chung-Han Cheng
Affiliation:
Insect-Plant Interaction Laboratory, Department of Entomology, College of Agriculture and Natural Resources, National Chung Hsing University, Taichung City, Taiwan
Shaw-Yhi Hwang*
Affiliation:
Insect-Plant Interaction Laboratory, Department of Entomology, College of Agriculture and Natural Resources, National Chung Hsing University, Taichung City, Taiwan
*
Corresponding author: Shaw-Yhi Hwang; Email: [email protected]
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Abstract

Parasitoids employ diverse oviposition strategies to enhance offspring survival and maximise fitness gains from hosts. Ladybird parasitoids, significant natural enemies of ladybirds, have the potential to disrupt biocontrol efforts, yet their biology and ecology remain poorly understood. This study investigated the host–parasitoid interaction among three sympatric larval endoparasitoids of Cheilomenes sexmaculata (Coleoptera: Coccinellidae): Homalotylus hemipterinus (Hymenoptera: Encyrtidae), Nothoserphus mirabilis (Hymenoptera: Proctotrupidae) and Oomyzus scaposus (Hymenoptera: Eulophidae). Our objective was to understand host instar preferences from five perspectives related to host profitability, handling difficulty or parasitism decision-making, and to examine the occupation rates of each parasitoid in different host instars. Host profitability was determined by development time, adult offspring dry mass, sex ratio, brood size, parasitism success rate and host handling time. Host handling difficulty was evaluated through host defensive behaviour and handling time. Parasitism decision-making was evaluated through acceptance rate and preference score that considered the first reaction of female wasp to the host. Results showed that each parasitoid responded differently to the host from various perspectives. However, the first two suitable hosts of these parasitoids overlap on the third instar host, with first to third instar hosts being ideal for H. hemipterinus, and third to fourth instar hosts being ideal for N. mirabilis and O. scaposus. In the field, the occupation rate of each parasitoid in third instar host was influenced by the population of N. mirabilis, implying its superior competitiveness. This study reveals the host instar preferences of ladybird parasitoids and highlights the potential for interspecific competition.

Keywords

biocontrol agentfourth trophic levelhost instar preferencehost qualityinterspecific competitionladybird parasitoid
Type
Research Paper
Information
Bulletin of Entomological Research , First View , pp. 1 - 11
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Copyright
Copyright © The Author(s), 2025. Published by Cambridge University Press

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References

Aartsma, Y, Cusumano, A, de Bobadilla, MF, Rusman, Q, Vosteen, I and Poelman, EH (2019) Understanding insect foraging in complex habitats by comparing trophic levels: insights from specialist host-parasitoid-hyperparasitoid systems. Current Opinion in Insect Science 32, 54–60.CrossRefGoogle ScholarPubMed
Abbas, K, Zaib, MS, Zakria, M, Hani, U-E, Zaka, SM and Ane, MN-U (2020) Cheilomenes sexmaculata (Coccinellidae: Coleoptera) as a potential biocontrol agent for aphids based on age-stage, two-sex life table. PLoS ONE 15, e0228367.CrossRefGoogle ScholarPubMed
Al Abassi, S, Birkett, MA, Pettersson, J, Pickett, JA, Wadhams, LJ and Woodcock, CM (2001) Response of the ladybird parasitoid Dinocampus coccinellae to toxic alkaloids from the seven-spot ladybird, Coccinella septempunctata. Journal of Chemical Ecology 27, 33–43.CrossRefGoogle ScholarPubMed
Andrade, TO, Krespi, L, Bonnardot, V, van Baaren, J and Outreman, Y (2016) Impact of change in winter strategy of one parasitoid species on the diversity and function of a guild of parasitoids. Oecologia 180, 877–888.CrossRefGoogle ScholarPubMed
Assour, HR and Behm, JE (2019) First occurrence of Cheilomenes sexmaculata (Coleoptera: Coccinellidae) on the Caribbean island of Curaçao. Neotropical Entomology 48, 863–865.CrossRefGoogle ScholarPubMed
Barrette, M, Wu, G-M, Brodeur, J, Giraldeau, L-A and Boivin, G (2009) Testing competing measures of profitability for mobile resources. Oecologia 158, 757–764.CrossRefGoogle ScholarPubMed
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Bayoumy, MH (2011) Foraging behavior of the coccinellid Nephus includens (Coleoptera: Coccinellidae) in response to Aphis gossypii (Hemiptera: Aphididae) with particular emphasis on larval parasitism. Environmental Entomology 40, 835–843.CrossRefGoogle ScholarPubMed
Bayoumy, MH and Michaud, JP (2012) Parasitism interacts with mutual interference to limit foraging efficiency in larvae of Nephus includens (Coleoptera: Coccinellidae). Biological Control 62, 120–126.CrossRefGoogle Scholar
Bezemer, TM and Mills, NJ (2003) Clutch size decisions of a gregarious parasitoid under laboratory and field conditions. Animal Behaviour 66, 1119–1128.CrossRefGoogle Scholar
Biranvand, A, Nedvĕd, O, Karimi, S, Vahedi, H, Hesami, S, Lotfalizadeh, H, Ajamhasani, M and Ceryngier, P (2020) Parasitoids of the ladybird beetles (Coleoptera: Coccinellidae) in Iran: an update. Annales de la Société entomologique de France (NS) 56, 106–114.CrossRefGoogle Scholar
Brown, PMJ and Roy, HE (2018) Native ladybird decline caused by the invasive harlequin ladybird Harmonia axyridis: evidence from a long-term field study. Insect Conservation and Diversity 11, 230–239.CrossRefGoogle Scholar
Canale, A, Benelli, G and Lucchi, A (2013) Female-borne cues affecting Psyttalia concolor (Hymenoptera: Braconidae) male behavior during courtship and mating. Insect Science 20, 379–384.CrossRefGoogle ScholarPubMed
Cebolla, R, Bru, P, Urbaneja, A and Tena, A (2018) Effect of host instar on host discrimination of heterospecific-parasitised hosts by sympatric parasitoids. Ecological Entomology 43, 137–145.CrossRefGoogle Scholar
Ceryngier, P, Roy, HE and Poland, RL (2012) Natural enemies of ladybird beetles. In Hodek, I, van Emden, HF and Honěk, A (eds), Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). Oxford: Blackwell Publishing Ltd, pp. 375–443.CrossRefGoogle Scholar
Ceryngier, P, Franz, K and Romanowski, J (2023) Distribution, host range and host preferences of ‘Dinocampus coccinellae’ (Hymenoptera: Braconidae): a worldwide database. European Journal of Entomology 120, 26–34. https://doi.org/10.14411/eje.2023.004CrossRefGoogle Scholar
Chavez, Y, Chirinos, DT, González, G, Lemos, N, Fuentes, A, Castro, R and Kondo, T (2017) Tamarixia radiata (Waterston) and Cheilomenes sexmaculata (Fabricius) as biological control agents of Diaphorina citri Kuwayama in Ecuador. Chilean Journal of Agricultural Research 77, 180–184.CrossRefGoogle Scholar
Chen, Z, Xu, R, Kuang, R-P and Sun, R (2016) Phototactic behaviour of the parasitoid Encarsia formosa (Hymenoptera: Aphelinidae). Biocontrol Science and Technology 26, 250–262.CrossRefGoogle Scholar
Chen, C, Gols, R, Biere, A and Harvey, JA (2019) Differential effects of climate warming on reproduction and functional responses on insects in the fourth trophic level. Functional Ecology 33, 693–702.CrossRefGoogle Scholar
Clausen, CP (1940) Entomophagous Insects. New York: McGraw-Hill book Company, Incorporated.Google Scholar
Comont, RF, Purse, BV, Phillips, W, Kunin, WE, Hanson, M, Lewis, OT, Harrington, R, Shortall, CR, Rondoni, G and Roy, HE (2014) Escape from parasitism by the invasive alien ladybird, Harmonia axyridis. Insect Conservation and Diversity 7, 334–342.CrossRefGoogle Scholar
Cusumano, A, Peri, E and Colazza, S (2016) Interspecific competition/facilitation among insect parasitoids. Current Opinion in Insect Science 14, 12–16.CrossRefGoogle ScholarPubMed
Cusumano, A, Harvey, JA, Bourne, ME, Poelman, EH and de Boer, JG (2020) Exploiting chemical ecology to manage hyperparasitoids in biological control of arthropod pests. Pest Management Science 76, 432–443.CrossRefGoogle ScholarPubMed
DaSilva, C, Morelli, R and Parra, J (2016) Effects of self-superparasitism and temperature on biological traits of two neotropical Trichogramma (Hymenoptera: Trichogrammatidae) species. Journal of Economic Entomology 109, 1555–1563.CrossRefGoogle ScholarPubMed
Davis, DS, Stewart, SL, Manica, A and Majerus, MEN (2006) Adaptive preferential selection of female coccinellid hosts by the parasitoid wasp Dinocampus coccinellae (Hymenoptera: Braconidae). European Journal of Entomology 103, 41–45.CrossRefGoogle Scholar
Duffield, SJ (1995) Crop-specific differences in the seasonal abundance of four major predatory groups on sorghum and short-duration pigeonpea. International Chickpea Newsletter 2, 74–76.Google Scholar
Fei, M, Hu, H, Gols, R, Liu, S, Wan, X, Li, B and Harvey, JA (2021) Development and oviposition strategies in two congeneric gregarious larval-pupal endoparasitoids of the seven-spot ladybird, Coccinella septempunctata. Biological Control 163, 104756.CrossRefGoogle Scholar
Fei, M, Gols, R and Harvey, JA (2023) The biology and ecology of parasitoid wasps of predatory arthropods. Annual Review of Entomology 68, 109–128.CrossRefGoogle ScholarPubMed
Firlej, A, Lucas, E, Coderre, D and Boivin, G (2007) Teratocytes growth pattern reflects host suitability in a host–parasitoid assemblage. Physiological Entomology 32, 181–187.CrossRefGoogle Scholar
Firlej, A, Lucas, E, Coderre, D and Boivin, G (2010) Impact of host behavioral defenses on parasitization efficacy of a larval and adult parasitoid. Biocontrol 55, 339–348.CrossRefGoogle Scholar
Fox, JW (2023) The existence and strength of higher order interactions is sensitive to environmental context. Ecology 104, e4156.CrossRefGoogle ScholarPubMed
Geoghegan, IE, Majerus, TMO and Majerus, MEN (1998) Differential parasitisation of adult and pre-imaginal Coccinella septempunctata (Coleoptera: Coccinellidae) by Dinocampus coccinellae (Hymenoptera: Braconidae). European Journal of Entomology 95, 571–579.Google Scholar
Godfray, HCJ (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Gols, R, Ros, VID, Ode, PJ, Vyas, D and Harvey, JA (2019) Varying degree of physiological integration among host instars and their endoparasitoid affects stress-induced mortality. Entomologia Experimentalis et Applicata 167, 424–432.CrossRefGoogle Scholar
Guo, Q, Meng, L, Fei, M and Li, B (2022) Oviposition and development of the gregarious parasitoid Homalotylus eytelweinii (Hymenoptera: Encyrtidae) in relation to host stage of predaceous ladybirds. Biocontrol Science and Technology 32, 455–466.CrossRefGoogle Scholar
Harvey, JA, Bezemer, TM, Elzinga, JA and Strand, MR (2004) Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size. Ecological Entomology 29, 35–43.CrossRefGoogle Scholar
Harvey, JA, Poelman, EH and Tanaka, T (2013) Intrinsic inter-and intraspecific competition in parasitoid wasps. Annual Review of Entomology 58, 333–351.CrossRefGoogle ScholarPubMed
Heimpel, GE, Mangel, M and Rosenheim, JA (1998) Effects of time limitation and egg limitation on lifetime reproductive success of a parasitoid in the field. The American Naturalist 152, 273–289.CrossRefGoogle ScholarPubMed
Holt, RD and Lawton, JH (1993) Apparent competition and enemy-free space in insect host-parasitoid communities. The American Naturalist 142, 623–645.CrossRefGoogle ScholarPubMed
Iperti, G (1964) The parasites of Coccinellids that attack aphids in the Alpes-Maritimes and Basses-Alpes. Entomophaga 9, 153–180.CrossRefGoogle Scholar
Iwasa, Y, Suzuki, Y and Matsuda, H (1984) Theory of oviposition strategy of parasitoids. I. Effect of mortality and limited egg number. Theoretical Population Biology 26, 205–227.CrossRefGoogle ScholarPubMed
Kassambara, A (2023) Pipe-friendly framework for basic statistical tests (R package rstatix version 0.7.2) ver R package version 0.7.2. Comprehensive R Archive Network (CRAN).Google Scholar
Khatri, D, He, XZ and Wang, Q (2016) Trade-off between fitness gain and cost determines profitability of a peach aphid parasitoid. Journal of Economic Entomology 109, 1539–1544.CrossRefGoogle ScholarPubMed
Klausnitzer, B (1969) Zur Kenntnis der Entomoparasiten mitteleuropäischer Coccinellidae. Abhandlungen und Berichte des Naturkundemuseums Görlitz 44, 1–15.Google Scholar
Knapp, M, Řeřicha, M, Maršíková, S, Harabiš, F, Kadlec, T, Nedvěd, O and Teder, T (2019) Invasive host caught up with a native parasitoid: field data reveal high parasitism of Harmonia axyridis by Dinocampus coccinellae in Central Europe. Biological Invasions 21, 2795–2802. https://doi.org/https://doi.org/10.1007/s10530-019-02027-4CrossRefGoogle Scholar
Lenth, RV (2023) Emmeans: estimated marginal means, aka least-squares means (version 1.8. 4-1). American Statistician 34, 1–5.Google Scholar
Lim, UT and Ben-Yakir, D (2020) Visual sensory systems of predatory and parasitic arthropods. Biocontrol Science and Technology 30, 728–739.CrossRefGoogle Scholar
Lin, KS (1988) Two new genera of Serphidae from Taiwan (Hymenoptera: Serphoidea). Journal of the Taiwan Museum 41, 15–33.Google Scholar
Liu, P-C, Zhao, B, Cao, D-D and Wei, J-R (2021) Oviposition decisions in an endoparasitoid under self-superparasitism conditions. Journal of Asia-Pacific Entomology 24, 443–447.CrossRefGoogle Scholar
Luna, MG, Desneux, N and Schneider, MI (2016) Encapsulation and self-superparasitism of Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae), a parasitoid of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). PLoS ONE 11, e0163196.CrossRefGoogle ScholarPubMed
Magdaraog, PM, Tanaka, T and Harvey, JA (2016) Wasp-associated factors act in interspecies competition during multiparasitism. Archives of Insect Biochemistry and Physiology 92, 87–107.CrossRefGoogle ScholarPubMed
Majerus, MEN, Geoghegan, IE and Majerus, TMO (2000) Adaptive preferential selection of young coccinellid hosts by the parasitoid wasp Dinocampus coccinellae (Hymenoptera: Braconidae). European Journal of Entomology 97, 161–164.CrossRefGoogle Scholar
Messing, RH and Wang, XG (2009) Competitor-free space mediates non-target impact of an introduced biological control agent. Ecological Entomology 34, 107–113.CrossRefGoogle Scholar
Murillo, FD, Liedo, P, Nieto-López, MG, Cabrera-Mireles, H, Barrera, JF and Montoya, P (2016) First instar larvae morphology of Opiinae (Hymenoptera: Braconidae) parasitoids of Anastrepha (Diptera: Tephritidae) fruit flies. Implications for interspecific competition. Arthropod Structure & Development 45, 294–300.CrossRefGoogle ScholarPubMed
Noyes, JS (2010) Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea), 3: subfamily Encyrtinae: Encyrtini, Echthroplexiellini, Discodini, Oobiini and Ixodiphagini, parasitoids associated with bugs (Hemiptera), insect eggs (Hemiptera, Lepidoptera, Coleoptera, Neuroptera) and ticks (Acari). Memoirs of the American Entomological Society 84, 1–848.Google Scholar
Ode, PJ, Vyas, DK and Harvey, JA (2022) Extrinsic inter-and intraspecific competition in parasitoid wasps. Annual Review of Entomology 67, 305–328.CrossRefGoogle ScholarPubMed
Pérez, J, Rojas, JC, Montoya, P, Liedo, P, González, FJ and Castillo, A (2012) Size, shape and hue modulate attraction and landing responses of the braconid parasitoid Fopius arisanus to fruit odour-baited visual targets. Biocontrol Science and Technology 57, 405–414.CrossRefGoogle Scholar
Pervez, A (2004) Predaceous coccinellids in India: predator-prey catalogue (Coleoptera: Coccinellidae). Oriental Insects 38, 27–61.CrossRefGoogle Scholar
Poelman, EH, Cusumano, A and De Boer, JG (2022) The ecology of hyperparasitoids. Annual Review of Entomology 67, 143–161.CrossRefGoogle ScholarPubMed
R, Core Team (2022) R: A Language and Environment for Statistical Computing. Vienna, Austria: Foundation for Statistical Computing.Google Scholar
Ray, DL (2010) To eat or not to eat: an easy simulation of optimal diet selection in the classroom. The American Biology Teacher 72, 40–43.CrossRefGoogle Scholar
Saeki, Y and Crowley, PH (2013) The size-number trade-off and components of fitness in clonal parasitoid broods. Entomologia Experimentalis et Applicata 149, 241–249.CrossRefGoogle Scholar
Sagarra, L, Vincent, C and Stewart, R (2001) Body size as an indicator of parasitoid quality in male and female Anagyrus kamali (Hymenoptera: Encyrtidae). Bulletin of Entomological Research 91, 363–367.CrossRefGoogle Scholar
Samková, A, Hadrava, J, Skuhrovec, J and Janšta, P (2019) Host population density and presence of predators as key factors influencing the number of gregarious parasitoid Anaphes flavipes offspring. Scientific Reports 9, 6081.CrossRefGoogle ScholarPubMed
Savino, V, Luna, MG, Gervassio, NGS and Coviella, CE (2017) Interspecific interactions between two Tuta absoluta (Lepidoptera: Gelechiidae) larval parasitoids with contrasting life histories. Bulletin of Entomological Research 107, 32–38.CrossRefGoogle ScholarPubMed
Sih, A and Christensen, B (2001) Optimal diet theory: when does it work, and when and why does it fail? Animal Behaviour 61, 379–390.CrossRefGoogle Scholar
Silva-Torres, CSA, Ramos Filho, IT, Torres, JB and Barros, R (2009) Superparasitism and host size effects in Oomyzus sokolowskii, a parasitoid of diamondback moth. Entomologia Experimentalis et Applicata 133, 65–73.CrossRefGoogle Scholar
Song, H, Meng, L and Li, B (2017) Fitness consequences of body-size-dependent parasitism in a gregarious parasitoid attacking the 7-spot ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae). Biological Control 113, 73–79.CrossRefGoogle Scholar
Sreedevi, K, Verghese, A, Vasudev, V and Devi, KS (2006) Species composition and abundance of predators with reference to the pomegranate aphid, Aphis punicae Passerini. Pest Management in Horticultural Ecosystems 12, 93–97.Google Scholar
Tamò, C, Roelfstra, L-L, Guillaume, S and Turlings, TCJ (2006) Odour-mediated long-range avoidance of interspecific competition by a solitary endoparasitoid: a time-saving foraging strategy. Journal of Animal Ecology 75, 1091–1099.CrossRefGoogle ScholarPubMed
Thierry, M, Hrček, J and Lewis, OT (2019) Mechanisms structuring host–parasitoid networks in a global warming context: a review. Ecological Entomology 44, 581–592.CrossRefGoogle Scholar
Tirunagaru, K, Sagadai, M and Kumar, A (2016) Five new species of Homalotylus Mayr (Hymenoptera: Encyrtidae) – from India with a key to Indian species. Journal of Natural History 50, 2369–2387.CrossRefGoogle Scholar
Van Baaren, J, Héterier, V, Hance, T, Krespi, L, Cortesero, A-M, Poinsot, D, Le Ralec, A and Outreman, Y (2004) Playing the hare or the tortoise in parasitoids: could different oviposition strategies have an influence in host partitioning in two Aphidius species? Ethology Ecology & Evolution 16, 231–242.CrossRefGoogle Scholar
van Baaren, J, Le Lann, C and van Alphen, JM (2010) Consequences of climate change for aphid-based multi-trophic systems. In Kindlmann, P, Dixon, A and Michaud, J (eds), Aphid Biodiversity under Environmental Change. Dordrecht: Springer, pp. 55–68.CrossRefGoogle Scholar
Vinson, SB and Iwantsch, GF (1980) Host suitability for insect parasitoids. Annual Review of Entomology 25, 397–419.CrossRefGoogle Scholar
Zhu, F, Lammers, M, Harvey, JA and Poelman, EH (2016) Intrinsic competition between primary hyperparasitoids of the solitary endoparasitoid Cotesia rubecula. Ecological Entomology 41, 292–300.CrossRefGoogle Scholar