Abstract
Resource specialization is a key concept in ecology, but it is unexpectedly difficult to parameterize. Differences in resource availability, sampling effort and abundances preclude comparisons of incompletely sampled biotic interaction webs. Here, we extend the distance-based specialization index (DSI) that measures trophic specialization by taking resource phylogenetic relatedness and availability into account into a rescaled version, DSI*. It is a versatile metric of specialization that expands considerably the scope and applicability, hence the usefulness, of DSI. The new metric also accounts for differences in abundance and sampling effort of consumers, which enables robust comparisons among distinct guilds of consumers. It also provides an abundance threshold for the reliability of the metric for rare species, a very desirable property given the difficulty of assessing any aspect of rare species accurately. We apply DSI* to an extensive dataset on interactions between insect herbivores from four folivorous guilds and their host plants in Papua New Guinean rainforests. We demonstrate that DSI*, contrary to the original DSI, is largely independent of sample size and weakly and non-linearly related with several host specificity measures that do not adjust for plant phylogeny. Thus, DSI* provides further insights into host specificity patterns; moreover, it is robust to the number and phylogenetic diversity of plant species selected to be sampled for herbivores. DSI* can be used for a broad range of comparisons of distinct feeding guilds, geographical locations and ecological conditions. This is a key advance in elucidating the interaction structure and evolution of highly diversified systems.
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References
Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. doi:10.1126/science.1123412
Bélisle CJP (1992) Convergence theorems for a class of simulated annealing algorithms on ℝd. J Applied Probability 29:885–895. doi:10.1017/S002190020004376X
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 289–300
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9
Chernomor O, Minh BQ, Forest F et al (2015) Split diversity in constrained conservation prioritization using integer linear programming. Methods Ecol Evol 6:83–91. doi:10.1111/2041-210X.12299
Colwell RK, Futuyma DJ (1971) On the measurement of niche breadth and overlap. Ecology 52:567–576. doi:10.2307/1934144
Craft KJ, Pauls SU, Darrow K et al (2010) Population genetics of ecological communities with DNA barcodes: an example from New Guinea Lepidoptera. Proc Natl Acad Sci 107:5041–5046. doi:10.1073/pnas.0913084107
Dyer LA, Singer MS, Lill JT et al (2007) Host specificity of Lepidoptera in tropical and temperate forests. Nature 448:696–699. doi:10.1038/nature05884
Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 586–608
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. doi:10.1016/0006-3207(92)91201-3
Forister ML, Novotny V, Panorska AK et al (2015) The global distribution of diet breadth in insect herbivores. Proc Natl Acad Sci 112:442–447. doi:10.1073/pnas.1423042112
Hulcr J, Mogia M, Isua B, Novotny V (2007) Host specificity of ambrosia and bark beetles (Col., Curculionidae: Scolytinae and Platypodinae) in a New Guinea rainforest. Ecol Entomol 32:762–772. doi:10.1111/j.1365-2311.2007.00939.x
Jorge LR, Prado PI, Almeida-Neto M, Lewinsohn TM (2014) An integrated framework to improve the concept of resource specialisation. Ecol Lett 17:1341–1350. doi:10.1111/ele.12347
Kembel SW (2009) Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12:949–960. doi:10.1111/j.1461-0248.2009.01354.x
Lewinsohn TM, Roslin T (2008) Four ways towards tropical herbivore megadiversity. Ecol Lett 11:398–416
Lewinsohn TM, Novotny V, Basset Y (2005) Insects on plants: diversity of herbivore assemblages revisited. Annu Rev Ecol Evol Syst 36:597–620. doi:10.1146/annurev.ecolsys.36.091704.175520
Manly BFJ, McDonald L, Thomas D (1993) Resource selection by animals: Statistical design and analysis for field studies. Springer
Miller SE, Novotny V, Basset Y (2003) Studies on New Guinea moths. 1. Introduction (Lepidoptera). Proc Entomol Soc Wash 105:1034–1042
Novotny V, Basset Y, Miller SE et al (2002) Low host specificity of herbivorous insects in a tropical forest. Nature 416:841–844. doi:10.1038/416841a
Novotny V, Drozd P, Miller SE et al (2006) Why are there so many species of herbivorous insects in tropical rainforests? Science 313:1115–1118. doi:10.1126/science.1129237
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. doi:10.1111/j.1365-2656.2010.01728.x
Novotny V, Miller SE, Hrcek J et al (2012) Insects on plants: explaining the paradox of low diversity within specialist herbivore guilds. Am Nat 179:351–362. doi:10.1086/664082
Pellissier L, Fiedler K, Ndribe C et al (2012) Shifts in species richness, herbivore specialization, and plant resistance along elevation gradients. Ecol Evol 2:1818–1825. doi:10.1002/ece3.296
Poulin R, Krasnov BR, Mouillot D (2011) Host specificity in phylogenetic and geographic space. Trends Parasitol 27:355–361. doi:10.1016/j.pt.2011.05.003
Strong DR, Southwood R, Lawton JH (1984) Insects on plants: community patterns and mechanisms. Blackwell Scientific, Oxford
Symons FB, Beccaloni GW (1999) Phylogenetic indices for measuring the diet breadths of phytophagous insects. Oecologia 119:427–434. doi:10.1007/s004420050804
Szefer P, Carmona CP, Chmel K et al (2017) Determinants of litter decomposition rates in a tropical forest: functional traits, phylogeny and ecological succession. Oikos. doi:10.1111/oik.03670
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. doi:10.1146/annurev.ecolsys.33.010802.150448
Weiblen GD, Webb CO, Novotny V et al (2006) Phylogenetic dispersion of host use in a tropical insect herbivore community. Ecology 87:S62–S75. doi:10.1890/0012-9658(2006)87[62:PDOHUI]2.0.CO;2
Acknowledgements
This study is part of VN’s visit to the University of Campinas, supported by Fapesp (grant #14/16006-0). LRJ was supported by a postdoc scholarship from Fapesp (grant #14/16082-9). VN acknowledges financial support by The Grant Agency of the Czech Republic (14-04258S), the European Research Foundation (669609) and the National Science Foundation (DEB-841885, -9628840, -9707928, -0211591, and -0515678). STS acknowledges funding from a Univ. of South Bohemia Postdoc project (reg.no. CZ.1.07/2.3.00/30.0006) (funded by the EU Education for Competitiveness Operational Programme, the European Social Fund and the Czech State Budget). TML received a research grant from CNPq (311800/215-7). We thank the very careful reading and insightful suggestions made by the reviewers, which greatly improved the manuscript.
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LRJ co-developed the idea of the paper, led the analysis and writing; VN contributed to idea of the paper, insect data set, and manuscript writing; STS and GDW developed plant phylogeny data and analysis, commented on the manuscript; SEM led taxonomic analysis of insects, commented on the manuscript; YB contributed to the insect data, commented on the manuscript; TML co-developed the idea of the paper, contributed to writing.
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Communicated by Andreas Prinzing.
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Jorge, L.R., Novotny, V., Segar, S.T. et al. Phylogenetic trophic specialization: a robust comparison of herbivorous guilds. Oecologia 185, 551–559 (2017). https://doi.org/10.1007/s00442-017-3980-7
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DOI: https://doi.org/10.1007/s00442-017-3980-7