A Holistic Approach to Parasitoid-Host Interaction Along an Elevational Gradient Revealed Coevolution Driven by Host Foraging Strategy
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
40225882
PubMed Central
PMC11991926
DOI
10.1002/ece3.71227
PII: ECE371227
Knihovny.cz E-zdroje
- Klíčová slova
- elevation, host range, mid‐domain effect, parasitism rate, parasitoid distribution, parasitoid–host interaction,
- Publikační typ
- časopisecké články MeSH
The evolutionary processes that shape host-parasitoid coexistence in a changing environment are poorly understood. We examined the large-scale distribution of highly specialised polysphinctine Darwin wasps associated with spiders along an elevational gradient and tested the hypothesis that distribution and parasitism rates depend on elevation, habitat type and the species and age composition of the host community. Further, on the basis of a large-scale dataset, we examined the hypothesis that three-dimensional webs in spiders may be an evolutionary adaptation against polysphinctine parasitoids. We found significant variation in parasitoid distribution and parasitism rates along a 1500 m elevational gradient in central Europe. The optimal model showed a humped shape for the parasitism rate on an elevational gradient. Overall, we found relatively low parasitism rates (4%) on spiders, with the highest parasitism rates in non-forested riparian vegetation and the lowest in agroecosystems. Rates of parasitism varied significantly among spiders forming different types of webs (foraging guilds). Spiders spinning 3D webs were dominant in the spider community, but parasitism on them was lower compared to spiders spinning 2D webs, probably because of the defensive function of the 3D web architecture. The bottom-up approach, in which the entire spider host community is analysed for parasitism rate, supports the hypothesis that 3D webs are evolutionarily novel and could have arisen as a result of the need for defence against enemies such as parasitoids.
Crop Research Institute Prague Czech Republic
Institute of Forest Ecology Slovak Academy of Sciences Zvolen Slovak Republic
Institute of Landscape Ecology Bratislava Slovak Academy of Sciences Nitra Slovak Republic
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Aguirre, H. , Shaw S. R., and Rodríguez‐Jiménez A.. 2018. “Contrasting Patterns of Altitudinal Distribution Between Parasitoid Wasps of the Subfamilies Braconinae and Doryctinae (Hymenoptera: Braconidae).” Insect Conservation and Diversity 11, no. 3: 219–229. 10.1111/icad.12265. DOI
Askew, R. R. , and Shaw M. R.. 1986. “Parasitoid Communities: Their Size, Structure and Development.” In Insect Parasitoids, edited by Waage J. and Greathead D., 225–229. Academic Press.
Barrantes, G. , Eberhard W. G., and Weng J. L.. 2008. “Seasonal Patterns of Parasitism of the Tropical Spiders Theridion evexum (Araneae, Theridiidae) and Allocyclosa bifurca (Araneae, Araneidae) by the Wasps Zatypota petronae and Polysphincta gutfreundi (Hymenoptera, Ichneumonidae).” Revista de Biología Tropical 56, no. 2: 749–754. PubMed
Benamú, M. , García L. F., Viera C., Lacava M., and Korenko S.. 2020. “Koinobiont Lifestyle of the Spider Wasp Minagenia (Hymenoptera, Pompilidae) and Its Consequences for Host Selection and Sex Allocation.” Zoology 140: 125797. PubMed
Blackledge, T. A. , Coddington J. A., and Gillespie R. G.. 2003. “Are Three‐Dimensional Spider Webs Defensive Adaptations?” Ecology Letters 6, no. 1: 13–18. 10.1046/j.1461-0248.2003.00384.x. DOI
Blackledge, T. A. , Scharff N., Coddington J. A., et al. 2009. “Reconstructing Web Evolution and Spider Diversification in the Molecular Era.” Proceedings of the National Academy of Sciences of the United States of America 106, no. 13: 5229–5234. PubMed PMC
Bohart, R. M. , and Menke A. S.. 1976. Sphecid Wasps of the World: A Generic Revision. University of California Press, pp. 695.
Bosmans, R. , Maelfait J.‐P., and De Kimpe A.. 1986. “Analysis of the Spider Communities in an Altitudinal Gradient in the French and Spanish Pyrénées.” Bulletin of the British Arachnological Society 7: 69–76.
Branco, V. V. , and Cardoso P.. 2020. “An Expert‐Based Assessment of Global Threats and Conservation Measures for Spiders.” Global Ecology and Conservation 24: e01290. 10.1016/j.gecco.2020.e01290. DOI
Cardoso, P. , Barton P. S., Birkhofer K., et al. 2020. “Scientists' Warning to Humanity on Insect Extinctions.” Biological Conservation 242: 108426.
Cardoso, P. , Pekár S., Jocqué R., and Coddington J. A.. 2011. “Global Patterns of Guild Composition and Functional Diversity of Spiders.” PLoS One 6: e21710. PubMed PMC
Chatzaki, M. , Lymberakis P., Markakis G., and Mylonas M.. 2005. “The Distribution of Ground Spiders (Araneae, Gnaphosidae) Along the Altitudinal Gradient of Crete, Greece: Species Richness, Activity and Altitudinal Range.” Journal of Biogeography 32, no. 5: 813–831. 10.1111/j.1365-2699.2004.01189.x. DOI
Colwell, R. K. , and Lees D. C.. 2000. “The Mid‐Domain Effect: Geometric Constraints on the Geography of Species Richness.” Trends in Ecology & Evolution 15, no. 2: 70–76. PubMed
Eberhard, W. G. 2000. “Spider Manipulation by a Wasp Larva.” Nature 406: 255–256. PubMed
Eberhard, W. G. 2019. “Hunting Behavior of the Wasp Polysphincta gutfreundi and Related Polysphinctine Wasps (Hymenoptera, Ichneumonidae).” Journal of the Kansas Entomological Society 91, no. 3: 177. 10.2317/0022-8567-91.3.177. DOI
Eberhard, W. G. , and Gonzaga M. O.. 2019. “Evidence That Polysphincta‐Group Wasps (Hymenoptera: Ichneumonidae) use Ecdysteroids to Manipulate the Web‐Construction Behaviour of Their Spider Hosts.” Biological Journal of the Linnean Society 127: 429–471.
Fitton, M. G. , Shaw M. R., and Austin A. D.. 1987. “The Hymenoptera Associated With Spiders in Europe.” Zoological Journal of the Linnean Society 90, no. 1: 65–93. 10.1111/j.1096-3642.1987.tb01348.x. DOI
Fitton, M. G. , Shaw M. R., and Gauld I. D.. 1988. Pimpline Ichneumonflies‐ Handbooks for the Identification British Insects. Vol. 7, 1–110. Royal Entomological Society.
Flinte, V. , Pádua D. G., Durand E. M., et al. 2023. “Variation in a Darwin Wasp (Hymenoptera: Ichneumonidae) Community Along an Elevation Gradient in a Tropical Biodiversity Hotspot: Implications for Ecology and Conservation.” Insects 14: 861. PubMed PMC
Fritzén, N. R. , and Shaw M. R.. 2014. “On the Spider Parasitoids Polysphincta longa Kasparyan and P. boops Tschek (Hymenoptera, Ichneumonidae, Pimplinae), With the First Host Records of P. longa .” Journal of Hymenoptera Research 39: 71–82. 10.3897/jhr.39.7591. DOI
Godfray, H. C. J. 1994. Parasitoids: Behavioral and Evolutionary Ecology, 473. Princeton University Press.
Gonzaga, M. O. , Kloss T. G., and Sobczak J. F.. 2017. “Host Behavioural Manipulation of Spiders by Ichneumonid Wasps.” In Behaviour and Ecology of Spiders, edited by Viera C. and Gonzaga M., 417–437. Springer International Publishing.
González‐Reyes, A. X. , Corronca J. A., and Rodriguez‐Artigas S. M.. 2017. “Changes of Arthropod Diversity Across an Altitudinal Ecoregional Zonation in Northwestern.” PeerJ 5: e4117. PubMed PMC
Hassell, M. P. 2000. “Host‐Parasitoid Population Dynamics.” Journal of Animal Ecology 69: 543–566. PubMed
Hoedjes, K. M. , Kruidhof H. M., Huigens M. E., Dicke M., Vet L. E., and Smid H. M.. 2011. “Natural Variation in Learning Rate and Memory Dynamics in Parasitoid Wasps: Opportunities for Converging Ecology and Neuroscience.” Proceedings of the Royal Society B: Biological Sciences 278: 889–897. PubMed PMC
Holen, O. H. , and Johnstone R. A.. 2004. “The Evolution of Mimicry Under Constraints.” American Naturalist 164, no. 5: 598–613. 10.1086/424972. PubMed DOI
Hunter, M. L. , and Yonzon P.. 1993. “Altitudinal Distributions of Birds, Mammals, People, Forests, and Parks in Nepal.” Conservation Biology 7, no. 2: 420–423. 10.1046/j.1523-1739.1993.07020420.x. DOI
Kloss, T. G. , Gonzaga M. O., Roxinol J. A. M., and Spelber C. F.. 2016. “Attack Behavior of Two Wasp Species of the Polysphincta Genus Group (Hymenoptera, Ichneumonidae) on Their Orb‐Weaver Spider Hosts (Araneae, Araneidae).” Journal of Insect Behavior 29, no. 3: 315–324. 10.1007/s10905-016-9560-6. DOI
Korenko, S. , Isaia M., Satrapová J., and Pekár S.. 2014. “Parazitoid Genus‐Specific Manipulation of Orb‐Web Host Spiders (Araneae, Araneidae).” Ecological Entomology 39: 30–38.
Korenko, S. , Korenková B., Satrapová J., Hamouzová K., and Belgers D.. 2015. “Modification of Tetragnatha montana (Araneae,Tetragnathidae) web Architecture Induced Bylarva of the Parasitoid Acrodactyla quadrisculpta (Hymenoptera, Ichneumonidae, Polysphincta Genus‐Group).” Zoological Studies 54: 40. PubMed PMC
Korenko, S. , Kysilková K., and Černecká L.. 2017. “Further Records of Two Spider‐Parasitoids of the Genus Polysphincta (Hymenoptera, Ichneumonidae, Ephialtini) From Central Europe, With Notes on Their Host Interactions.” Arachnologische Mitteilungen 54: 28–32.
Korenko, S. , Michalková V., Zwakhals K., and Pekár S.. 2011. “Host Specificity and Temporal and Seasonal Shifts in Host Preference of a Web‐Spider Parasitoid Zatypota percontatoria .” Journal of Insect Science 11: 101. 10.1673/031.011.10101. PubMed DOI PMC
Korenko, S. , Sýkora J., Černecká Ľ., et al. 2022. “Elevation Gradient Affects the Distribution and Host Utilisation of Zatypota Anomala (Hymenoptera, Ichneumonidae) Associated With Mesh Web Weaving Spiders (Araneae, Dictynidae).” Journal of Hymenoptera Research 93: 89–100. 10.3897/jhr.93.91513. DOI
Körner, C. 2007. “The Use of ‘Altitude’ in Ecological Research.” Trends in Ecology & Evolution 22, no. 11: 569–574. 10.1016/j.tree.2007.09.006. PubMed DOI
Lenoir, J. , Gégout J.‐C., Marquet P. A., de Ruffray P., and Brisse H.. 2008. “A Significant Upward Shift in Plant Species Optimum Elevation During the 20th Century.” Science 20: 1768–1771. PubMed
Li, L. , Huang Z., Ye W., et al. 2009. “Spatial Distributions of Tree Species in a Subtropical Forest of China.” Oikos 118, no. 4: 495–502. 10.1111/j.1600-0706.2009.16753.x. DOI
Lomolino, M. V. 2001. “Elevational Gradients of Species‐Density: Historical and Prospective Views.” Global Ecology and Biogeography 10: 3–13.
Matsumoto, R. 2016. “Molecular Phylogeny and Systematics of the Polysphincta Group of Genera (Hymenoptera, Ichneumonidae, Pimplinae).” Systematic Entomology 41, no. 4: 854–864. 10.1111/syen.12196. DOI
Maunsell, S. C. , Kitching R. L., Burwell C. J., and Morris R. J.. 2015. “Changes in Host‐Parasitoid Food Web Structure With Elevation.” Journal of Animal Ecology 84: 353–363. PubMed
McCain, C. M. 2007. “Could Temperature and Water Availability Drive Elevational Species Richness Patterns? A Global Case Study for Bats.” Global Ecology and Biogeography 16, no. 1: 1–13. 10.1111/j.1466-8238.2006.00263.x. DOI
McCain, C. M. , and Grytnes J.‐A.. 2010. “Elevational Gradients in Species Richness.” In Encyclopedia of Life Sciences, 1–8. John Wiley & Sons, Ltd.
Michalko, R. , Pekár S., and Entling M. H.. 2019. “An Updated Perspective on Spiders as Generalist Predators in Biological Control.” Oecologia 189: 21–36. PubMed
Miller, J. 2010. “Species Distribution Modelling.” Geography Compass 4: 490–509.
Natural History Museum . 2024. “World Spider Catalog, Version 25.” https://wsc.nmbe.ch/.
Nentwig, W. , Blick T., Gloor D., Hänggi A., and Kropf C.. 2024. “Araneae – Spiders of Europe, Version 1.2024.” www.araneae.unibe.ch.
Pekár, S. , and Brabec M.. 2019. Modern Analysis of Biological Data 3. Non‐Linear Models in R. Muni Press, 218 pp.
Penney, D. , and Selden P. A.. 2002. “The Oldest Linyphiid Spider, in Lower Cretaceous Lebanese Amber (Araneae, Linyphiidae, Linyphiinae).” Journal of Arachnology 30, no. 3: 487–493. 10.1636/0161-8202(2002)030[0487:TOLSIL]2.0.CO;2. DOI
Péré, C. , Jactel H., and Kenis M.. 2013. “Response of Insect Parasitism to Elevation Depends on Host and Parasitoid Life‐History Strategies.” Biology Letters 9: 20130028. PubMed PMC
Peters, M. K. , Hemp A., Appelhans T., et al. 2016. “Predictors of Elevational Biodiversity Gradients Change From Single Taxa to the Multi‐Taxa Community Level.” Nature Communications 7, no. 1: 13736. 10.1038/ncomms13736. PubMed DOI PMC
Petráková, L. , Líznarová E., Pekár S., Haddad C. R., Sentenská L., and Symondson W. O.. 2015. “Discovery of a Monophagous True Predator, a Specialist Termite‐Eating Spider (Araneae: Ammoxenidae).” Scientific Reports 5: 14013. 10.1038/srep14013. PubMed DOI PMC
Plath, E. , Rischen T., Mohr T., and Fischer K.. 2021. “Biodiversity in Agricultural Landscapes: Grassy Field Margins and Semi‐Natural Fragments Both Foster Spider Diversity and Body Size.” Agriculture, Ecosystems and Environment 316: 107457.
Rahbek, C. 1995. “The Elevational Gradient of Species Richness – A Uniform Pattern.” Ecography 18: 200–205.
Read, D. P. , Feeny P. P., and Root R. B.. 1970. “Habitat Selection by the Aphid Parasite Diaeretiella rapae (Hymenoptera: Braconidae) and Hyperparasite Charips brassicae (Hymenoptera: Cynipidae).” Canadian Entomologist 102: 1567–1578.
RobledoOspina, L. E. , and Rao D.. 2022. “Dangerous Visions: A Review of Visual Antipredator Strategies in Spiders.” Evolutionary Ecology 36, no. 2: 163–180. 10.1007/s10682-022-10156-x. DOI
Roslin, T. , Hardwick B., Novotny V., et al. 2017. “Higher Predation Risk for Insect Prey at Low Latitudes and Elevations.” Science 356, no. 6339: 742–744. PubMed
Sánchez‐Cordero, V. 2001. “Elevation Gradients of Diversity for Rodents and Bats in Oaxaca, Mexico.” Global Ecology and Biogeography 10, no. 1: 63–76. 10.1046/j.1466-822x.2001.00235.x. DOI
Salt, G. 1935. “Experimental Studies in Insect Parasitism. III – Host Selection.” Proceedings of the Royal Society B: Biological Sciences 117: 413–435.
Schulz, S. 2004. “Semiochemistry of Spiders.” In Advances in Insect Chemical Ecology, edited by Cardé R. T. and Millar J. F., 110–150. Cambridge University Press.
Sivinski, J. , Piñero J., and Aluja M.. 2000. “The Distributions of Parasitoids (Hymenoptera) of Anastrepha Fruit Flies (Diptera: Tephritidae) Along an Altitudinal Gradient in Veracruz, Mexico.” Biological Control 18, no. 3: 258–269. 10.1006/bcon.2000.0836. DOI
Souza, H. S. , Messas Y. F., Masago F., dos Santos E. F., and Vasconcellos‐Neto J.. 2015. “ Paracyphononyxs Capulatus (Hymenoptera, Pompilidae), a Koinobiontecto Parasitoid of Trochosa sp. (Araneae, Lycosidae).” Journal of Hymenoptera Research 46: 165–172. 10.3897/jhr.46.5833. DOI
Spasojevic, T. , Broad G. B., Sääksjärvi I. E., et al. 2021. “Mind the Outgroup and Bare Branches in Total‐Evidence Dating: A Case Study of Pimpliform Darwin Wasps (Hymenoptera, Ichneumonidae).” Systematic Biology 70, no. 2: 322–339. 10.1093/sysbio/syaa079. PubMed DOI PMC
Speed, J. D. M. , Skjelbred I. Å., Barrio I. C., et al. 2019. “Trophic Interactions and Abiotic Factors Drive Functional and Phylogenetic Structure of Vertebrate Herbivore Communities Across the Arctic Tundra Biome.” Ecography 42: 1152–1163.
Stanová, V. , and Valachovič M.. 2002. Katalóg Biotopov Slovenska. DAPHNE – Inštitút aplikovanej ekológie, pp. 225.
Stevens, G. C. 1992. “The Elevational Gradient in Altitudinal Range: An Extension of Rapport's Latitudinal Rule to Altitude.” American Naturalist 140, no. 6: 893–911. 10.1086/285447. PubMed DOI
Takasuka, K. , Fritzén N. R., Tanaka Y., Matsumoto R., Maeto K., and Shaw M. E.. 2018. “The Changing Use of the Ovipositor in Host Shifts by Ichneumonid Ectoparasitoids of Spiders (Hymenoptera, Ichneumonidae, Pimplinae).” Parasite 25: 17. 10.1051/parasite/2018011. PubMed DOI PMC
Takasuka, K. , and Matsumoto R.. 2011. “Lying on the Dorsum: Unique Host‐Attacking Behaviour of Zatypota Albicoxa (Hymenoptera, Ichneumonidae).” Journal of Ethology 29, no. 2: 203–207. 10.1007/s10164-010-0263-8. DOI
Takasuka, K. , Matsumoto R., and Ohbayashi N.. 2009. “Oviposition Behavior of Zatypota Albicoxa (Hymenoptera, Ichneumonidae), an Ectoparasitoid of Achaearanea Tepidariorum (Araneae, Theridiidae).” Entomological Science 12, no. 3: 232–237. 10.1111/j.1479-8298.2009.00338.x. DOI
Terborgh, J. , and Weske J. S.. 1975. “The Role of Competition in the Distribution of Andean Birds.” Ecology 56, no. 3: 562–576. 10.2307/1935491. DOI
Townes, H. 1958. “Some Biological Characteristics of the Ichneumonidae (Hymenoptera) in Relation to Biological Control.” Journal of Economic Entomology 51, no. 5: 650–652. 10.1093/jee/51.5.650. DOI
Uma, D. B. , and Weiss M. R.. 2010. “Chemical Mediation of Prey Recognition by Spider‐Hunting Wasps.” Ethology 116, no. 1: 85–95. 10.1111/j.1439-0310.2009.01715.x. DOI
van der Ent, L. J. , and Shaw S. R.. 1998. “Species Richness of Costa Rican Cenocoeliini (Hymenoptera: Braconidae): Anomalous Diversity.” Journal of Hymenoptera Research 7: 15–24.
Vet, L. E. M. 1983. “Host‐Habitat Location Through Olfactory Cues by Leptopilina clavipes (Hartig) (Hym.: Eucoilidae), A Parasitoid of Fungivorous Drosophila: The Influence of Conditioning.” Netherlands Journal of Zoology 33: 225–248.
Vinson, S. B. 1976. “Host Selection by Insect Parasitoids.” Annual Review of Entomology 21: 109–133.
Virtanen, T. , and Neuvonen S.. 1999. “Performance of Moth Larvae on Birch in Relation to Altitude, Climate, Host Quality and Parasitoids.” Oecologia 120: 92–101. PubMed
Vollrath, F. , and Selden P.. 2007. “The Role of Behavior in the Evolution of Spiders, Silks, and Webs.” Annual Review of Ecology, Evolution, and Systematics 38, no. 1: 819–846. 10.1146/annurev.ecolsys.37.091305.110221. DOI
Waichert, C. , Rodriguez J., Wasbauer M. S., von Dohlen C. D., and Pitts J. P.. 2015. “Molecular Phylogeny and Systematics of Spider Wasps (Hymenoptera: Pompilidae): Redefining Subfamily Boundaries and the Origin of the Family.” Zoological Journal of the Linnean Society 175, no. 2: 271–287. 10.1111/zoj.12272. DOI
Wisz, M. S. , Pottier J., Kissling W. D., et al. 2013. “The Role of Biotic Interactions in Shaping Distributions and Realised Assemblages of Species: Implications for Species Distribution Modelling.” Biological Reviews and Biological Proceedings of the Cambridge Philosophical Society 88, no. 1: 15–30. 10.1111/j.1469-185X.2012.00235.x. PubMed DOI PMC
Yanoviak, S. P. , Kragh G., and Nadkarni N. M.. 2003. “Spider Assemblages of Costa Rican Cloud Forests: Effects of Forest Level and Forest Age.” Studies on Neotropical Fauna and Environment 38, no. 2: 145–154.
Zuur, A. F. , Hilbe J. M., and Ieno E. N.. 2015. A Beginner's Guide to GLM and GLMM With R. A Frequentist and Bayesian Perspective for Ecologists. Highland Statistics Ltd, pp. 256.
Zwakhals, K. 2006. “The European Species of the Genera Zatypota and Sinarachna (Hymenoptera: Ichneumonidae, Pimplinae, Polysphinctini).” Entomologische Berichten 66: 34–37.
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