Abstract
Ferns and lycophytes are the second and third largest lineages of vascular plants, yet our understanding of their interactions with phytophagous insects is very limited. In this study, we reviewed herbivorous insects, their feeding habits and host preferences on these two plant groups, searched for any evidence of coevolution, and discussed possible biases of our current knowledge on fern–insect interactions. We analyzed 2318 records of fern–insect interactions from 122 literature sources, based on the feeding habit of insects, fern taxa, and geographic location. We report interactions comprising 809 insect species (mainly Hemiptera, Lepidoptera, and Coleoptera) and 382 fern species (mainly Dennstaedtiaceae, Dryopteridaceae, and Pteridaceae). Leaf-chewers comprised over 50% of the species, followed by sap-sucking insects (29.1%) and spore feeders (6.5%). The overall interaction analyses revealed that the entire network was not significantly nested and had relatively low levels of specialization (H2′ = 0.24). The interaction networks of Coleoptera were the most specialized at family (H2′ = 0.40) and genus level (H2′ = 0.65), whereas six out of 10 most specialized insect families were Lepidoptera (d′ ≥ 0.44). At the genus level, all networks had a plant-biased asymmetry. Although insect specialists were common, few cases of coevolutionary radiation have been documented. We discuss the possible biases of our dataset, which also highlight gaps to fill in future research and suggest that many more fern-feeding insects remain to be discovered, especially sap-sucking, gall-forming, and spore-feeding insects on modern fern groups.
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Data availability
All used references are given in appendix 1 as a supplementary file. The data set is available online https://doi.org/10.6084/m9.figshare.16606580.
References
Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302. https://doi.org/10.1016/j.tplants.2012.02.006
Almeida-Neto M, Guimarães P, Guimarães PR, Loyola RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239. https://doi.org/10.1111/j.0030-1299.2008.16644.x
ARPR, Sharpe JM, Moran RC, Ferguson DL, Mehltreter K, Hooper EA, Canfield JM (1994–2018) Annual review of pteridological research. International Association of Pteridologists, vol 8–32
Balick MJ, Furth DG, Cooper-Driver G (1978) Biochemical and evolutionary aspects of arthropod predation on ferns. Oecologia 35:55–89. https://doi.org/10.1007/BF00345541
Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci U S A 100:9383–9387. https://doi.org/10.1073/pnas.1633576100
Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. https://doi.org/10.1126/science.1123412
Bernal R, Gradstein SR, Celis M (2016) Catálogo de plantas y líquenes de Colombia volumen I. Universidad Nacional de Colombia, Bogotá
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. https://doi.org/10.1186/1472-6785-6-9
Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol 17:341–346. https://doi.org/10.1016/j.cub.2006.12.039
Blüthgen N, Fründ J, Vázquez DP, Menzel F (2008) What do interaction network metrics tell us about specialization and biological traits? Ecology 89:3387–3399. https://doi.org/10.1890/07-2121.1
Brues CT (1920) The selection of food-plants by insects, with special reference to lepidopterous larvae. Am Nat 54:313–332. https://doi.org/10.1086/279763
Cagnolo L, Salvo A, Valladares G (2011) Network topology: patterns and mechanisms in plant-herbivore and host-parasitoid food webs. J Anim Ecol 80:342–351. https://doi.org/10.1111/j.1365-2656.2010.01778.x
Chapman RF (1982) Chemoreception: the significance of receptor numbers. Adv Insect Phys 16:247–356. https://doi.org/10.1016/S0065-2806(08)60155-1
Christenhusz MJM, Byng JW (2016) The number of known plants species in the world and its annual increase. Phytotaxa 261:201–217. https://doi.org/10.11646/phytotaxa.261.3.1
Cooper-Driver GA (1978) Insect-fern associations. Entomol Exp Appl 24:310–316. https://doi.org/10.1111/j.1570-7458.1978.tb02787.x
Cyr H, Face ML (1993) Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148–150. https://doi.org/10.1038/361148a0
de Araújo WS (2016) Global patterns in the structure and robustness of plant-herbivore networks. Front Biogeogr. https://doi.org/10.21425/f58331053
Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11
Farias R, Costa LEN, Oliveira AFM, Barros ICL, Mehltreter K (2020) Leaf defense syndromes in tropical ferns. Plant Ecol 221:853–865. https://doi.org/10.1007/s11258-019-00983-4
Flora do Brasil 2020 (2021) Jard. Botânico do Rio Janeiro. http://floradobrasil.jbrj.gov.br/. Accessed 18 Feb 2021
Fuentes-Jacques LJ, Hanson-Snortum P, Hernández-Ortiz V, Díaz-Castelazo C, Mehltreter K (2021) Data set. Figshare. https://doi.org/10.6084/m9.figshare.16606580
Gerson U (1979) The association between pteridophytes and arthropods. Fern Gaz 12:29–45
Gómez-Zurita J, Hunt T, Kopliku F, Vogler AP (2007) Recalibrated tree of leaf beetles (Chrysomelidae) indicates independent diversification of angiosperms and their insect herbivores. PLoS ONE 2:e360. https://doi.org/10.1371/journal.pone.0000360
Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, New York
Hay L, Brown JMM (1992) Plant chemical defence: plant response to physical damage. Comp Biochem Physiol Part C Comp 101:537–539. https://doi.org/10.1016/0742-8413(92)90083-J
Hendrix SD (1980) An evolutionary and ecological perspective of the insect fauna of ferns. Am Nat 115:171–196. https://doi.org/10.1086/283554
Isaka Y, Sato T (2014) Molecular phylogenetic and divergence time estimation analyses of the sawfly subfamily Selandriinae (Hymenoptera: Tenthredinidae). Entomol Sci 17:435–439. https://doi.org/10.1111/ens.12080
Isaka Y, Sato T (2015) Was species diversification in Tenthredinoidea (Hymenoptera: Symphyta) related to the origin and diversification of angiosperms? Can Entomol 147:443–458. https://doi.org/10.4039/tce.2014.60
Jørgensen PM, León-Yánez S (1999) Catalogue of the vascular plants of Ecuador. Monographs in Systematic Botany from the Missouri Botanical Garden, Missouri
Konstantinov FV, Knyshov AA (2015) The tribe Bryocorini (Insecta: Heteroptera: Miridae: Bryocorinae): phylogeny, description of a new genus, and adaptive radiation on ferns. Zool J Linn Soc 175:441–472. https://doi.org/10.1111/zoj.12283
Labandeira C (2007) The origin of herbivory on land: initial patterns of plant tissue consumption by arthropods. Insect Sci 14:259–275. https://doi.org/10.1111/j.1744-7917.2007.00141.x-i1
López-Carretero A, Díaz-Castelazo C, Boege K, Rico-Gray V (2014) Evaluating the spatio-temporal factors that structure network parameters of plant-herbivore interactions. PLoS ONE 9:e110430. https://doi.org/10.1371/journal.pone.0110430
Markham K, Chalk T, Stewart CN (2006) Evaluation of fern and moss protein-based defenses against phytophagous insects. Int J Plant Sci 167:111–117. https://doi.org/10.1086/497651
Mehltreter K (2010) Interactions of ferns with fungi and animals. In: Mehltreter K, Walker LR, Sharpe JM (eds) Fern ecology, 1st edn. Cambridge University Press, Cambridge, pp 221–254
Mehltreter K, García-Franco JG (2008) Leaf phenology and trunk growth of the deciduous tree fern Alsophila firma (Baker) D. S. Conant in a lower montane Mexican forest. Am Fern J 98:1–13
Mehltreter K, Tolome J (2003) Herbivory on three tropical fern species of a Mexican cloud forest. In: Chandra S, Srivastava M (eds) Pteridology in the New Millennium. Springer, Netherlands, Dordrecht, pp 375–381
Mehltreter K, Hülber K, Hietz P (2006) Herbivory on epiphytic ferns of a Mexican cloud forest. Fern Gaz 17:303–309
Mehltreter K, Walker LR, Sharpe JM (2010) Fern ecology. Cambridge University Press, Cambridge
Misof B, Liu S, Meusemann K et al (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–767. https://doi.org/10.1126/science.1257570
Moran RC, Labiak PH (2015) Phylogeny of the polybotryoid fern clade (Dryopteridaceae). Int J Plant Sci 176:880–891. https://doi.org/10.1086/683393
Morin NR, Brouillet L, Levin GA (2015) Flora of North America north of Mexico. Rodriguesia 66:973–981. https://doi.org/10.1590/2175-7860201566416
Muggleston SJ (1989) Rearing and the effects of photoperiod and temperature on diapause in Stathmopoda aposema (Lepidoptera: Oecophoridae: Stathmopodinae). New Zeal J Zool 16:199–204. https://doi.org/10.1080/03014223.1989.10422569
Mukhopadhyay A, Thapa D (1994) Species richness of ferns and associated insects from Darjeeling plains. J Bombay Nat Hist Soc 91:86–90
Nel P, Bertrand S, Nel A (2018) Diversification of insects since the Devonian: a new approach based on morphological disparity of mouthparts. Sci Rep 8:1–10. https://doi.org/10.1038/s41598-018-21938-1
Novotny V, Basset Y (1999) Body size and host plant specialization: a relationship from a community of herbivorous insects on Ficus from Papua New Guinea. J Trop Ecol 15:315–328. https://doi.org/10.1017/S026646749900084X
Novotny V, Miller SE, Baje L et al (2010) Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest. J Anim Ecol 79:1193–1203. https://doi.org/10.1111/j.1365-2656.2010.01728.x
O’Brien CW (2009) New Notiodes semiaquatic weevil (Curculionidae) from sporocarps of Marsilea mollis (Marsileaceae) in Southern Arizona, USA. West North Am Nat 69:421–425. https://doi.org/10.3398/064.069.0401
Park KT, Cho S, Na S, Shin YM, Kim S (2018) Genus Stathmopoda Herrich-Shäffer (Lepidoptera, Stathmopodidae) from the Korean Peninsula with two new species. J Asia-Pacific Biodivers 11:259–266. https://doi.org/10.1016/j.japb.2018.04.004
Patra B, Bera S (2007) Herbivore damage to ferns caused by a Chrysomelid beetle from lower Gangetic plains of West Bengal, India. Am Fern J 97:19–29. https://doi.org/10.1640/0002-8444(2007)97[19:HDTFCB]2.0.CO;2
Poinar G (2014) Insect herbivores of horsetails: bionomics, dispersal, and co-evolution. Am Entomol 60:235–240. https://doi.org/10.1093/ae/60.4.235
PPG I (2016) A community-derived classification for extant lycophytes and ferns. J Syst Evol 54:563–603. https://doi.org/10.1111/jse.12229
R Core Team (2021) R: a language and environment for statistical computing. R Foundation of Statistical Computing, Vienna, Austria. https://www.R-project.org
Richardson SJ, Walker LR (2010) Nutrient ecology of ferns. Fern ecology. Cambridge University Press, Cambridge, pp 111–139
Santos MG, Hanson P, Maia VC, Mehltreter K (2019) A review of galls on ferns and lycophytes. Environ Entomol 48:53–60. https://doi.org/10.1093/ee/nvy172
Sawamura M, Kawakita A, Kato M (2009) Fern–spore-feeder interaction in temperate forests in Japan: sporing phenology and spore-feeding insect community. Am J Bot 96:594–604
Schneider H (2016) The ghost of the Cretaceous terrestrial revolution in the evolution of fern-sawfly associations. J Syst Evol 54:93–103. https://doi.org/10.1111/jse.12194
Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallón S, Lupia R (2004) Ferns diversified in the shadow of angiosperms. Nature 428:553–557. https://doi.org/10.1038/nature02361
Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology, 2nd edn. Oxford University Press, Oxford
Sedio BE, Rojas Echeverri JC, Boya PCA, Wright SJ (2017) Sources of variation in foliar secondary chemistry in a tropical forest tree community. Ecology 98:616–623. https://doi.org/10.1002/ecy.1689
Shen ZY, Hsu YF (2020) The fern-feeding genus Cuprina Sinev, 1988 (Lepidoptera, Stathmopodidae), new for Taiwan, with descriptions of two new species. Zookeys 2020:117–126. https://doi.org/10.3897/zookeys.915.46980
Sugiura S, Yamazaki K (2004) Moths boring into Ficus syconia on Iriomote Island, south-western Japan. Entomol Sci 7:113–118. https://doi.org/10.1111/j.1479-8298.2004.00056.x
Testo W, Sundue M (2016) A 4000-species dataset provides new insight into the evolution of ferns. Mol Phylogenet Evol 105:200–211. https://doi.org/10.1016/j.ympev.2016.09.003
Tree of Life Web Project (2002) Hexapoda. http://tolweb.org/Hexapoda/2528/2002.01.01. Accessed 4 Feb 2021
Wang A, Guan W, Wang S (2020) Genus Stathmopoda Herrich-Schäffer, 1853 (Lepidoptera: Stathmopodidae) from China: descriptions of thirteen new species. Zootaxa 4838:358–380. https://doi.org/10.11646/zootaxa.4838.3.3
Web of Science (2021) Web of Science [v.5.35] - Colección principal de Web of ScienceBúsqueda básica. http://apps.webofknowledge.com. Accessed 22 Feb 2021
Whitney HM, Glover BJ (2013) Coevolution: plant-insect. In: eLS. John Wiley and Sons, Ltd, Chichester, UK
Wieczorek H (2009) Zur Kenntnis der Adlerfarninsekten: Ein Beitrag zum Problem der biologischen Bekämpfung von Pteridium aquilinum (L.) Kuhn in Mitteleuropa. Zeitschrift Für Angew Entomol 72:337–358. https://doi.org/10.1111/j.1439-0418.1972.tb02252.x
Wiens JJ, Lapoint RT, Whiteman NK (2015) Herbivory increases diversification across insect clades. Nat Commun 6:1–7. https://doi.org/10.1038/ncomms9370
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
Ximenes Pinho B, Dáttilo W, Leal IR (2017) Structural breakdown of specialized plant-herbivore interaction networks in tropical forest edges. Glob Ecol Conserv 12:1–8. https://doi.org/10.1016/j.gecco.2017.08.007
Zvereva EL, Lanta V, Kozlov MV (2010) Effects of sap-feeding insect herbivores on growth and reproduction of woody plants: a meta-analysis of experimental studies. Oecologia 163:949–960. https://doi.org/10.1007/s00442-010-1633-1
Acknowledgements
We thank Elda Catalina Flores-Galván for her assistance in data capture. We acknowledge two anonymous reviewers who provided constructive feedback that improved considerably the manuscript.
Funding
Research was funded by the Instituto de Ecología A.C. (Projects 20030-10796 to KM and 20030-10128 to VHO). JFJ thanks CONACyT for his doctorate scholarship (No. 589325).
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Fuentes-Jacques, L.J., Hanson-Snortum, P., Hernández-Ortiz, V. et al. A global review and network analysis of phytophagous insect interactions with ferns and lycophytes. Plant Ecol 223, 27–40 (2022). https://doi.org/10.1007/s11258-021-01187-5
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DOI: https://doi.org/10.1007/s11258-021-01187-5