Abstract
Patch exploitation strategies have received considerable attention since the development of the marginal value theorem. As an excellent biological research object, parasitoids have been extensively studied in regard to patch exploitation, including the effect of parasitoid states. Longevity and fecundity are state-dependent traits that may affect foraging decisions, oviposition behavior and patch residence time. We investigated the impact of Trichopria drosophilae (Hymenoptera: Diapriidae) states on patch exploitation. As an important endoparasitic wasp in the Drosophila pupal stage, T. drosophilae has potential as a biological control agent. Our results demonstrate that female age, food availability and mating state modulated the patch residence time of T. drosophilae. In addition, the time taken for females to enter a patch was changed by oviposition experience, age, and food availability. Our results are consistent with models that predict that the patch exploitation strategy must be fundamentally dynamic in parasitoids. Differences between patch foraging behavior in wasps with different internal state can be explained by the maximum fitness they achieved.
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Data for this paper are deposited in the Zenodo repository https://doi.org/10.5281/zenodo.6362590
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References
Abram PK, Cusumano A, Peri E, Brodeur J, Boivin G, Colazza S (2015) Thermal stress affects patch time allocation by preventing forgetting in a parasitoid wasp. Behav Ecol 26(5):1326–1334. https://doi.org/10.1093/beheco/arv084
Abram PK, Cusumano A, Abram K, Colazza S, Peri E (2017) Testing the habituation assumption underlying models of parasitoid foraging behavior. Peer J 5:e3097. https://doi.org/10.7717/peerj.3097
Bianchi FJ, Wäckers FL (2008) Effects of flower attractiveness and nectar availability in field margins on biological control by parasitoids. Biol Control 46:400–408
Boivin G, Fauvergue X, Wajnberg E (2004) Optimal patch residence time in egg parasitoids: innate versus learned estimate of patch quality. Oecologia 138:640–647
Charnov EL (1976) Optimal foraging, the marginal value theorem. Theor Popul Biol 9:129–136
Clark CW, Mangel M (2000) Dynamic state variable models in ecology: methods and applications. Oxford University Press on Demand, Oxford
Corley JC, Villacide JM, van Nouhuys S (2010) Patch time allocation by a parasitoid: the influence of con-specifics, host abundance and distance to the patch. J Insect Behav 23:431–440
Cox DR (1972) Regression models and life-tables. J R Stat Soc B 34:187–202
Daane KM, Wang X-G, Biondi A, Miller B, Miller JC, Riedl H, Shearer PW, Guerrieri E, Giorgini M, Buffington M (2016) First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J Pest Sci 89:823–835
David JR, Clavel MF (1965) Interaction entre le génotype et le milieu d’élevage. Conséquences sur les caractéristiques du développement de la Drosophile. Bull Biol Fr Belg 99:369–378
Farahani HK, Moghadassi Y, Alford L, van Baaren J (2019) Effect of interference and exploitative competition on associative learning by a parasitoid wasp: a mechanism for ideal free distribution? Anim Behav 151:157–163
Fischbein D, Bettinelli J, Bernstein C, Corley JC (2012) Patch choice from a distance and use of habitat information during foraging by the parasitoid Ibalia leucospoides. Ecol Entomol 37:161–168
Godfray HCJ, Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology, vol 67. Princeton University Press, Princeton
Goubault M, Outreman Y, Poinsot D, Cortesero AM (2005) Patch exploitation strategies of parasitic wasps under intraspecific competition. Behav Ecol 16:693–701
Hemerik LIA, Driessen G, Haccou P (1993) Effects of intra-patch experiences on patch time, search time and searching efficiency of the parasitoid Leptopilina clavipes. J Anim Ecol 62:33–44
Hirose Y, Ehler LE, Hirose Y (2003) Influence of host age on patch use by a quasi-gregarious egg parasitoid. Environ Entomol 32:789–796
Houston A, Clark C, McNamara J, Mangel M (1988) Dynamic models in behavioural and evolutionary ecology. Nature 332:29–34
Iranipour S, BenaMoleai P, Asgari S, Michaud JP (2020) Foraging egg parasitoids, Trissolcus vassilievi (Hymenoptera: Platygastridae), respond to host density and conspecific competitors in a patchy laboratory environment. J Econ Entomol 113:760–769
Jamont M, Dubois-Pot C, Jaloux B (2014) Nectar provisioning close to host patches increases parasitoid recruitment, retention and host parasitism. Basic Appl Ecol 15:151–160
Kaçar G, Wang X-G, Biondi A, Daane KM (2017) Linear functional response by two pupal Drosophila parasitoids foraging within single or multiple patch environments. PLoS One 12:e0183525
Keeling CI, Plettner E, Slessor KN (2004) Hymenopteran semiochemicals. In: Schulz S (ed) The chemistry of pheromones and other semiochemicals I. Springer Berlin Heidelberg, Berlin, pp 133–177
King BH, Grimm KM, Reno HE (2000) Effects of mating on female locomotor activity in the parasitoid wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). Environ Entomol 29:927–933
Konopka JK, Poinapen D, Gariepy T, McNeil JN (2018) Understanding the mismatch between behaviour and development in a novel host-parasitoid association. Sci Rep 8:1–11
Krebs JR, Davies NB (2009) Behavioural ecology: an evolutionary approach. Blackwall, Oxford
Lanteigne M-E, Brodeur J, Jenni S, Boivin G (2015) Patch experience changes host acceptance of the aphid parasitoid aphidius ervi. J Insect Behav 28:436–446
Le Lann C, Visser B, Mériaux M, Moiroux J, van Baaren J, van Alphen JJM, Ellers J (2014) Rising temperature reduces divergence in resource use strategies in coexisting parasitoid species. Oecologia 174:967–977
Louapre P, van Baaren J, Pierre JS, van Alphen JJM (2011) Information gleaned and former patch quality determine foraging behavior of parasitic wasps. Behav Ecol 22:1064–1069
Mazzetto F, Marchetti E, Amiresmaeili N, Sacco D, Francati S, Jucker C, Dindo ML, Lupi D, Tavella L (2016) Drosophila parasitoids in northern Italy and their potential to attack the exotic pest Drosophila suzukii. J Pest Sci 89:837–850
Moiroux J, Abram PK, Louâpre P, Barrette M, Brodeur J, Boivin G (2016) Influence of temperature on patch residence time in parasitoids: physiological and behavioural mechanisms. Sci Nat 103(3–4):1–10. https://doi.org/10.1007/s00114-016-1357-0
Nonacs P (2001) State dependent behavior and the marginal value theorem. Behav Ecol 12:71–83
Olson D, Fadamiro H, Lundgren JG, Heimpel GE (2000) Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp. Physiol Entomol 25:17–26
Outreman Y, Le Ralec A, Wajnberg E, Pierre JS (2005) Effects of within- and among-patch experiences on the patch-leaving decision rules in an insect parasitoid. Behav Ecol Sociobiol 58:208–217
Rivero A, West SA (2005) The costs and benefits of host feeding in parasitoids. Anim Behav 69:1293–1301
Smid HM, Wang G, Bukovinszky T, Steidle JLM, Bleeker MAK, van Loon JJA, Vet LEM (2007) Species-specific acquisition and consolidation of long-term memory in parasitic wasps. P Roy Soc B-Biol Sci 274:1539–1546
Stacconi MVR, Buffington M, Daane KM, Dalton DT, Grassi A, Kaçar G, Miller B, Miller JC, Baser N, Ioriatti C (2015) Host stage preference, efficacy and fecundity of parasitoids attacking Drosophila suzukii in newly invaded areas. Biol Control 84:28–35
Stephens DW, Krebs JR (1986) Foraging theory, vol 1. Princeton University Press, Princeton
Turlings TCL, Wäckers FL, Vet LEM, Lewis WJ, Tumlinson JH (1993) Learning of host-finding cues by hymenopterous parasitoids. In: Insect learning. Springer, Boston, MA, pp 51–78
van Alphen JJM, Bernstein C, Driessen G (2003) Information acquisition and time allocation in insect parasitoids. Trends Ecol Evol 18:81–87
van Baaren J, Boivin G, Outreman Y (2005) Patch exploitation strategy by an egg parasitoid in constant or variable environment. Ecol Entomol 30:502–509
Waage JK (1979) Foraging for patchily-distributed hosts by the parasitoid, Nemeritis canescens. J Anim Ecol:353–371
Wajnberg É (2006) Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioral mechanisms. Behav Ecol Sociobiol 60:589–611
Wajnberg E, Bernhard P, Hamelin F, Boivin G (2006) Optimal patch time allocation for time-limited foragers. Behav Ecol Sociobiol 60:1–10
Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee J, Bruck DJ, Walton VM, O'Neal SD, Zalom FG (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:G1–G7
Wang X-G, Kaçar G, Biondi A, Daane KM (2016) Foraging efficiency and outcomes of interactions of two pupal parasitoids attacking the invasive spotted wing drosophila. Biol Control 96:64–71
Yamada Y (1988) Optimal use of patches by parasitoids with a limited fecundity. Res Popul Ecol 30(2):235–249. https://doi.org/10.1007/BF02513247
Zang L-S, Liu T-X (2010) Effects of food deprivation on host feeding and parasitism of whitefly parasitoids. Environ Entomol 39:912–918
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National Natural Science Foundation of China (31672351, 31172145).
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SZ, BQ, JX, and XG conduct the experiments. SZ contributed to data curation and statistical analysis, and first drafted the writing. Ilyas A contributed to comments and revisions. PL and HH contributed to idea and design of the study, and comments and revisions; All authors contributed critically to the drafts. All authors read and approved the final manuscript.
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Zhang, S., Qian, B., Ilyas, A. et al. Influence of Parasitoid States on the Propensity to Enter and the Stay in a Patch. J Insect Behav 35, 56–64 (2022). https://doi.org/10.1007/s10905-022-09799-z
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DOI: https://doi.org/10.1007/s10905-022-09799-z