Length-mass allometries of the larvae of aquatic dipterans: differences between taxa, morphological traits, and methods
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články
Grantová podpora
LM2015075
MEYS CZ
University of South Bohemia
PubMed
38367014
PubMed Central
PMC10874217
DOI
10.1093/jisesa/ieae012
PII: 7609878
Knihovny.cz E-zdroje
- Klíčová slova
- Culicidae, dry mass, length–weight regression, mosquito, wet mass,
- MeSH
- Aedes * MeSH
- Culex * MeSH
- larva MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Body mass underpins many ecological processes at the level of individuals, populations, and communities. Often estimated in arthropods from linear morphological traits such as body length or head width, these relationships can vary even between closely related taxa. Length-mass relationships of mosquito (Diptera: Culicidae) larvae are poorly known despite the importance of this family to disease and aquatic ecology. To fill this gap, we measured ontogenetic changes in linear traits (body length, head width, and thorax width) and dry and wet masses and estimated length- and width-mass relationships in larvae of 3 culicid species inhabiting different niches: the tropical Aedes albopictus (Skuse, 1894), the temperate Culex pipiens (Linnaeus, 1758), and the snowmelt Ochlerotatus punctor (Kirby, 1837). We compared our results with published length-mass allometries of other aquatic dipteran larvae. We showed that thorax width and body length, but not head width, reliably predicted body mass for our 3 species. The length-mass allometry slopes in aquatic dipterans varied considerably between and within families but were independent of phylogeny, specimen handling, preservation techniques, and data fitting methods. Slope estimates became less precise with decreasing sample size and size range. To obtain reliable estimates of the allometric slopes, we have thus recommended using data on all larval stages for intraspecific allometries and a wide range of species for interspecific allometries. We also cautioned against the indiscriminate use of length-mass allometries obtained for other taxa or collected at lower taxonomic resolutions, e.g., when using length-mass relationships to estimate biomass production at a given site.
Zobrazit více v PubMed
Abouheif E. A method for testing the assumption of phylogenetic independence in comparative data. Evol Ecol Res. 1999:1:895–909.
Arnold TW. Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manage. 2010:74(6):1175–1178. 10.1111/j.1937-2817.2010.tb01236.x DOI
Banse K, Mosher S.. Adult body mass and annual production/biomass relationships of field populations. Ecol Monogr. 1980:50(3):355–379. 10.2307/2937256 DOI
Barbour MT, Gerritsen J, Snyder BD, Stribling JB.. Appendix B: regional tolerance value, functional feeding groups and habit/behavior assignments for benthic macroinvertebrates. In: Rapid bioassessment protocols for use in streams and wadeable rivers: periphyton, benthic macroinvertebrates, and fish. 2nd ed. Washington (DC): Environmental Protection Agency; Office of Water; 1999.
Bates D, Maechler M, Bolker B, Walker S.. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015:67(1):1–48. 10.18637/jss.v067.i01 DOI
Becker B, Moretti MS, Callisto M.. Length–dry mass relationships for a typical shredder in Brazilian streams (Trichoptera: Calamoceratidae). Aquat Insects. 2009:31(3):227–234. 10.1080/01650420902787549 DOI
Becker N, Petrić D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A.. Mosquitoes and their control. 2nd ed. Berlin, Heidelberg: Springer-Verlag Berlin Heidelberg; 2010.
Benke AC. Concepts and patterns of invertebrate production in running waters. SIL Proceedings 1922-2010. 1993:25(1):15–38. 10.1080/03680770.1992.11900056 DOI
Benke AC, Huryn AD.. Secondary production of macroinvertebrates. In: Hauer FR, Lamberti GA, editors. Methods in stream ecology. 2nd ed. Burlington (MA): Academic Press; 2006. p. 691–710.
Benke AC, Huryn AD, Smock LA, Wallace JB.. Length-mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States. J North Am Benthol Soc. 1999:18(3):308–343. 10.2307/1468447 DOI
Burgherr P, Meyer EI.. Regression analysis of linear body dimensions vs. dry mass in stream macroinvertebrates. Archiv für Hydrobiologie. 1997:139(1):101–112. 10.1127/archiv-hydrobiol/139/1997/101 DOI
Cardini A. Missing the third dimension in geometric morphometrics: how to assess if 2D images really are a good proxy for 3D structures? Hystrix Ital J Mammal. 2014:25(2):73–81. 10.4404/hystrix-25.2-10993 DOI
Cranston PS, Hardy NB, Morse GE.. A dated molecular phylogeny for the Chironomidae (Diptera). Syst Entomol. 2012:37(1):172–188. 10.1111/j.1365-3113.2011.00603.x DOI
Cunze S, Kochmann J, Koch LK, Klimpel S.. Aedes albopictus and its environmental limits in Europe. PLoS One. 2016:11(9):e0162116. 10.1371/journal.pone.0162116 PubMed DOI PMC
de Vienne DM. Lifemap: exploring the entire tree of life. PLoS Biol. 2016:14(12):e2001624. 10.1371/journal.pbio.2001624 PubMed DOI PMC
Dekanová V, Streberová Z, Novikmec M, Svitok M.. The effect of preservation on biomass and length estimates and its variation within and between two mayfly species. Limnology. 2023:24(3):181–191. 10.1007/s10201-023-00715-8 DOI
Dekanová V, Venarsky MP, Bunn SE.. Length–mass relationships of Australian aquatic invertebrates. Austral Ecol. 2022:47(1):120–126. 10.1111/aec.13077 DOI
Dermott RM, Paterson CG.. Determining dry weight and percentage dry matter of chironomid larvae. Can J Zool. 1974:52(10):1243–1250. 10.1139/z74-165 DOI
Dyar HG. The number of molts of Lepidopterous larvae. Psyche (Stuttg). 1890:5(175–176):23871. 10.1155/1890/23871 DOI
Edwards FK, Lauridsen RB, Armand L, Vincent HM, Jones IJ.. The relationship between length, mass and preservation time for three species of freshwater leeches (Hirudinea). Fundam Appl Limnol/Arch für Hydrobiol. 2009:173(4):321–327. 10.1127/1863-9135/2009/0173-0321 DOI
Eklöf J, Austin A, Bergström U, Donadi S, Eriksson BDHK, Hansen J, Sundblad G.. Size matters: relationships between body size and body mass of common coastal, aquatic invertebrates in the Baltic Sea. PeerJ. 2017:5:e2906. 10.7717/peerj.2906 PubMed DOI PMC
Evans CL, Adler PH.. Microsculpture and phylogenetic significance of the spermatheca of black flies (Diptera: Simuliidae). Can J Zool. 2000:78(8):1468–1482. 10.1139/z00-078 DOI
Fisher SG, Gray LJ.. Secondary production and organic matter processing by collector macroinvertebrates in a desert stream. Ecology. 1983:64(5):1217–1224. 10.2307/1937830 DOI
Gil-Azevedo LH, Coscarón S.. Comprehensive phylogeny of Simulium (Psilopelmia) Enderlein (Diptera: Simuliidae) – classification tested against comparative morphology. Arthropod Syst Phylogeny. 2020:78(3):405–425. 10.26049/ASP78-3-2020-04 DOI
Giustini M, Miccoli FP, De Luca G, Cicolani B.. Length–weight relationships for some plecoptera and ephemeroptera from a carbonate stream in central Apennine (Italy). Hydrobiologia. 2008:605(1):183–191. 10.1007/s10750-008-9353-9 DOI
González JM, Basaguren A, Pozo J.. Size-mass relationships of stream invertebrates in a northern Spain stream. Hydrobiologia. 2002:489(1):131–137. 10.1023/A:1023220501921 DOI
Helm BR, Baldwin MA, Rinehart JP, Yocum GD, Greenlee KJ, Bowsher JH.. Body and wing allometries reveal flight-fecundity tradeoff in response to larval provisioning in Osmia lignaria (Hymenoptera: Megachilidae). J Insect Sci. 2021:21(3):11. 10.1093/jisesa/ieab035 PubMed DOI PMC
Hongoh V, Berrang-Ford L, Scott ME, Lindsay LR.. Expanding geographical distribution of the mosquito, Culex pipiens, in Canada under climate change. Appl Geogr. 2012:33:53–62. 10.1016/j.apgeog.2011.05.015 DOI
Hothorn T, Bretz F, Westfall P.. Simultaneous inference in general parametric models. Biom J. 2008:50(3):346–363. 10.1002/bimj.200810425 PubMed DOI
Hubálek Z. Mosquito-borne viruses in Europe. Parasitol Res. 2008:103(S1):29–43. 10.1007/s00436-008-1064-7 PubMed DOI
Johnston TA, Cunjak RA.. Dry mass–length relationships for benthic insects: a review with new data from Catamaran Brook, New Brunswick, Canada. Freshw Biol. 1999:41(4):653–674. 10.1046/j.1365-2427.1999.00400.x DOI
Johnston TA, Mathias JA.. Length reduction and dry weight loss in frozen and formalin-preserved larval walleye, Stizostedion vitreum (Mitchill). Aquacult Res. 1993:24(3):365–371. 10.1111/j.1365-2109.1993.tb00558.x DOI
Jombart T, Balloux F, Dray S.. adephylo: new tools for investigating the phylogenetic signal in biological traits. Bioinformatics. 2010:26(15):1907–1909. 10.1093/bioinformatics/btq292 PubMed DOI
Jourdain F, Samy AM, Hamidi A, Bouattour A, Alten B, Faraj C, Roiz D, Petrić D, Pérez-Ramírez E, Velo E, et al. . Towards harmonisation of entomological surveillance in the Mediterranean area. PLoS Negl Trop Dis. 2019:13(6):e0007314. 10.1371/journal.pntd.0007314 PubMed DOI PMC
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO.. Picante: R tools for integrating phylogenies and ecology. Bioinformatics. 2010:26(11):1463–1464. 10.1093/bioinformatics/btq166 PubMed DOI
Kraus JM, Vonesh JR.. Fluxes of terrestrial and aquatic carbon by emergent mosquitoes: a test of controls and implications for cross-ecosystem linkages. Oecologia. 2012:170(4):1111–1122. 10.1007/s00442-012-2369-x PubMed DOI
Krosch MN, Cranston PS, Bryant LM, Strutt F, McCluen SR.. Towards a dated molecular phylogeny of the Tanypodinae (Chironomidae, Diptera). Invertebr Syst. 2017:31(3):302. 10.1071/IS16046 DOI
Krosch MN, Silva FL, Ekrem T, Baker AM, Bryant LM, Stur E, Cranston PS.. A new molecular phylogeny for the Tanypodinae (Diptera: Chironomidae) places the Australian diversity in a global context. Mol Phylogenet Evol. 2022:166:107324. 10.1016/j.ympev.2021.107324 PubMed DOI
Landahl CC, Nagell B.. Influence of the season and of preservation methods on wet- and dry weights of larvae of Chironomus plumosus L. Int Rev der Gesamten Hydrobiol und Hydrogr. 1978:63(3):405–410. 10.1002/iroh.19780630308 DOI
LaRue B, Gaudreau C, Bagre HO, Charpentier G.. Generalized structure and evolution of ITS1 and ITS2 rDNA in black flies (Diptera: Simuliidae). Mol Phylogenet Evol. 2009:53(3):749–757. 10.1016/j.ympev.2009.07.032 PubMed DOI
Lasenby DC, Yan ND, Futter MN.. Changes in body dimensions of larval Chaoborus in ethanol and formalin. J Plankton Res. 1994:16(12):1601–1608. 10.1093/plankt/16.12.1601 DOI
Leisnham PT, Sala LM, Juliano SA.. Geographic variation in adult survival and reproductive tactics of the mosquito Aedes albopictus. J Med Entomol. 2008:45(2):210–221. 10.1603/0022-2585(2008)45[210:gviasa]2.0.co;2 PubMed DOI PMC
Lenth R . emmeans: estimated marginal means, aka least-squares means. R package version 1.10.0; 2024.
Leuven R, Brock TCM, van Druten HAM.. Effects of preservation on dry- and ash-free dry weight biomass of some common aquatic macro-invertebrates. Hydrobiologia. 1985:127(2):151–159. 10.1007/bf00004193 DOI
López C, Corona A, Rincón JE.. Relación entre parámetros biométricos y peso seco en insectos acuáticos depredadores de Venezuela. Rev Biol Trop. 1997:44(3):641–643.
Louca V, Lucas MC, Green C, Majambere S, Fillinger U, Lindsay SW.. Role of fish as predators of mosquito larvae on the floodplain of the Gambia river. J Med Entomol. 2009:46(3):546–556. 10.1603/033.046.0320 PubMed DOI PMC
Mährlein M, Pätzig M, Brauns M, Dolman AM.. Length–mass relationships for lake macroinvertebrates corrected for back-transformation and preservation effects. Hydrobiologia. 2016:768(1):37–50. 10.1007/s10750-015-2526-4 DOI
Martinet J-P, Ferté H, Failloux A-B, Schaffner F, Depaquit J.. Mosquitoes of North-Western Europe as potential vectors of arboviruses: a review. Viruses. 2019:11(11):1059. 10.3390/v11111059 PubMed DOI PMC
Mayer SV, Tesh RB, Vasilakis N.. The emergence of arthropod-borne viral diseases: a global prospective on dengue, chikungunya and zika fevers. Acta Trop. 2017:166:155–163. 10.1016/j.actatropica.2016.11.020 PubMed DOI PMC
Mazón M, Nuñez-Penichet C, Cobos ME.. Relationship between body mass and forewing length in neotropical Ichneumonidae (Insecta: Hymenoptera). Neotrop Entomol. 2020:49(5):713–721. 10.1007/s13744-020-00784-9 PubMed DOI
Medley KA. Niche shifts during the global invasion of the Asian tiger mosquito, Aedes albopictus Skuse (Culicidae), revealed by reciprocal distribution models. Glob Ecol Biogeogr. 2010:19(1):122–133. 10.1111/j.1466-8238.2009.00497.x DOI
Merritt RW, Cummins KW, Berg MB.. An introduction to aquatic insects of North America. 4th ed. Dubuque (IA): Kendall/Hunt Publishing Company; 2008.
Meyer EI. The relationship between body length parameters and dry mass in running water in-vertebrates. Archiv für Hydrobiologie. 1989:117(2):191–203. 10.1127/archiv-hydrobiol/117/1989/191 DOI
Mills EL, Pittman K, Munroe B.. Effect of preservation on the weight of marine benthic invertebrates. Can J Fish Aquat Sci. 1982:39(1):221–224. 10.1139/f82-029 DOI
Miserendino ML. Length-mass relationships for macroinvertebrates in freshwater environments of Patagonia (Argentina). Ecol Austral. 2001:11:3–8.
Mogi M. Insects and other invertebrate predators. J Am Mosq Control Assoc. 2007:23(2 Suppl):93–109. 10.2987/8756-971X(2007)23[93:IAOIP]2.0.CO;2 PubMed DOI
Mouquet N, Daufresne T, Gray SM, Miller TE.. Modelling the relationship between a pitcher plant (Sarracenia purpurea) and its phytotelma community: mutualism or parasitism? Funct Ecol. 2008:22(4):728–737. 10.1111/j.1365-2435.2008.01421.x DOI
Nylin S, Gotthard K.. Plasticity in life-history traits. Annu Rev Entomol. 1998:43(1):63–83. 10.1146/annurev.ento.43.1.63 PubMed DOI
Oliphant ZH, Hyslop EJ.. Biomass, productivity, and biomass turnover (P/B) ratios of benthic macroinvertebrates in high elevation ponds in St. Ann, Jamaica (West Indies). Caribb J Sci. 2020:50(2):275–300. 10.18475/cjos.v50i2.a11 DOI
Paradis E, Schliep K.. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019:35(3):526–528. 10.1093/bioinformatics/bty633 PubMed DOI
Pavoine S, Ollier S, Pontier D, Chessel D.. Testing for phylogenetic signal in phenotypic traits: new matrices of phylogenetic proximities. Theor Popul Biol. 2008:73(1):79–91. 10.1016/j.tpb.2007.10.001 PubMed DOI
Pedersen TL. Patchwork: the Composer of Plots. R package version 1.2.0; 2024.
Pélabon C, Tidière M, Lemaître JF, Gaillard JM.. Modelling allometry: statistical and biological considerations – a reply to Packard. Biol J Linn Soc. 2018:125(3):664–671. 10.1093/biolinnean/bly141 DOI
Phillips N, Smith B.. New Zealand freshwater macroinvertebrate trait database. Hamilton, New Zealand: NIWA; 2018.
Quiroz-Martínez H, Rodríguez-Castro A.. Aquatic insects as predators of mosquito larvae. J Am Mosq Control Assoc. 2007:23(2 Suppl):110–117. 10.2987/8756-971X(2007)23[110:AIAPOM]2.0.CO;2 PubMed DOI
R Development Core Team. R: a language and environment for statistical computing. R Found Stat Comput, Vienna, Austria; 2019. 10.1007/978-3-540-74686-7 DOI
Reynolds SK, Benke AC.. Temperature-dependent growth rates of larval midges (Diptera: Chironomidae) from a southeastern U.S. stream. Hydrobiologia. 2005:544(1):69–75. 10.1007/s10750-004-8334-x DOI
Ribeiro GC. Phylogeny of the Limnophilinae (Limoniidae) and early evolution of the Tipulomorpha (Diptera). Invertebr Syst. 2008:22(6):627. 10.1071/IS08017 DOI
Rochlin I, Ninivaggi DV, Hutchinson ML, Farajollahi A.. Climate change and range expansion of the Asian tiger mosquito (Aedes albopictus) in Northeastern USA: implications for public health practitioners. PLoS One. 2013:8(4):e60874. 10.1371/journal.pone.0060874 PubMed DOI PMC
Romeo-Aznar V, Alem I, De Majo MS, Byttebier B, Solari HG, Fischer S.. Effects of scarcity and excess of larval food on life history traits of Aedes aegypti (Diptera: Culicidae). J Vector Ecol. 2018:43(1):117–124. 10.1111/jvec.12291 PubMed DOI
Ryan SJ, Carlson CJ, Mordecai EA, Johnson LR.. Global expansion and redistribution of Aedes-borne virus transmission risk with climate change. PLoS Negl Trop Dis. 2019:13(3):e0007213. 10.1371/journal.pntd.0007213 PubMed DOI PMC
Sabo JL, Bastow JL, Power ME.. Length–mass relationships for adult aquatic and terrestrial invertebrates in a California watershed. J North Am Benthol Soc. 2002:21(2):336–343. 10.2307/1468420 DOI
Schmidt-Kloiber A, Hering D.. www.freshwaterecology.info – an online tool that unifies, standardises and codifies more than 20,000 European freshwater organisms and their ecological preferences. Ecol Indic. 2015:53:271–282. 10.1016/j.ecolind.2015.02.007 DOI
Serra SRQ, Cobo F, Graça MAS, Dolédec S, Feio MJ.. Synthesising the trait information of European Chironomidae (Insecta: Diptera): towards a new database. Ecol Indic. 2016:61:282–292. 10.1016/j.ecolind.2015.09.028 DOI
Shahbaz-Gahroee S, Aazami J, Aghamohammadi A, Rico A, Sumon KA.. Length-mass relationships for macroinvertebrates in the Choghakhor international wetland, Iran. Biologia (Bratisl). 2021:76(2):645–653. 10.2478/s11756-020-00585-w DOI
Shinkarenko L, Hulsman K, Mottram P, Dale P, Kay BH.. Reliability of using head capsule width and body length to identify larval instars of Aedes vigilax (Diptera: Culicidae). Aust J Entomol. 1986:25(1):37–40. 10.1111/j.1440-6055.1986.tb01066.x DOI
Smith RJ. Use and misuse of the reduced major axis for line-fitting. Am J Phys Anthropol. 2009:140(3):476–486. 10.1002/ajpa.21090 PubMed DOI
Smock LA. Relationships between body size and biomass of aquatic insects. Freshw Biol. 1980:10(4):375–383. 10.1111/j.1365-2427.1980.tb01211.x DOI
Sohlström EH, Marian L, Barnes AD, Haneda NF, Scheu S, Rall BC, Brose U, Jochum M.. Applying generalized allometric regressions to predict live body mass of tropical and temperate arthropods. Ecol Evol. 2018:8(24):12737–12749. 10.1002/ece3.4702 PubMed DOI PMC
Stanford JA. A centrifuge method for determining live weights of aquatic insect larvae, with a note on weight loss in preservative. Ecology. 1973:54(2):449–451. 10.2307/1934356 DOI
Studier EH, Lavoie KH, Howarth FG.. Leg attenuation and seasonal femur length: mass relationships in cavernicolous crickets (Orthoptera: Gryllidae and Rhaphidophoridae). J Cave Karst Stud. 2002:64(2):126–131.
Tachet H, Richoux P, Bournaud M, Usseglio-Polatera P.. Invertébrés d’eau douce: systématique, biologie, écologie. Paris: CNRS Éditions; 2000.
Taskinen S, Warton DI.. Robust tests for one or more allometric lines. J Theor Biol. 2013:333:38–46. 10.1016/j.jtbi.2013.05.010 PubMed DOI
Towers DJ, Henderson IM, Veltman CJ.. Predicting dry weight of New Zealand aquatic macroinvertebrates from linear dimensions. N Z J Mar Freshw Res. 1994:28(2):159–166. 10.1080/00288330.1994.9516604 DOI
Usseglio-Polatera P, Bournaud M, Richoux P, Tachet H.. Biological and ecological traits of benthic freshwater macroinvertebrates: relationships and definition of groups with similar traits. Freshw Biol. 2000:44(3):563–568. 10.1046/j.1365-2427.2000.00535.x DOI
Walker ED, Lawson DL, Merritt RW, Morgan WT, Klug MJ.. Nutrient dynamics, bacterial populations, and mosquito productivity in tree hole ecosystems and microcosms. Ecology. 1991:72(5):1529–1546. 10.2307/1940953 DOI
Warton DI, Duursma RA, Falster DS, Taskinen S.. smatr 3 - an R package for estimation and inference about allometric lines. Methods Ecol Evol. 2012:3(2):257–259. 10.1111/j.2041-210X.2011.00153.x DOI
Warton DI, Weber NC.. Common slope tests for bivariate errors-in-variables models. Biom J. 2002:44(2):161–174. 10.1002/1521-4036(200203)44:2<161::aid-bimj161>3.0.co;2-n DOI
Warton DI, Wright IJ, Falster DS, Westoby M.. Bivariate line-fitting methods for allometry. Biol Rev Camb Philos Soc. 2006:81(2):259–291. 10.1017/S1464793106007007 PubMed DOI
Wenzel F, Meyer E, Schwoerbel J.. Morphometry and biomass determination of dominant mayfly larvae (Ephemeroptera) in running waters. Archiv für Hydrobiologie. 1990:118(1):31–46. 10.1127/archiv-hydrobiol/118/1990/31 DOI
Whitman D, Agrawal A.. What is phenotypic plasticity and why is it important? In: Whitman DW, Ananthakrishnan TN, editors. Phenotypic plasticity of insects. Science Publishers, Plymouth, NJ, USA; 2009.
Wickham H. Reshaping data with the reshape package. J Stat Softw. 2007:21(12):1–20.
Wickham H. ggplot2: elegant graphics for data analysis. Springer-Verlag New York; 2016.
Wickham H, François R, Henry L, Müller K, Vaughan D. dplyr: a grammar of data manipulation. R package version 1.1.4, https://github.com/tidyverse/dplyr, https://dplyr.tidyverse.org. 2023.
Wiegmann BM, Trautwein MD, Winkler IS, Barr NB, Kim J-W, Lambkin C, Bertone MA, Cassel BK, Bayless KM, Heimberg AM, et al. . Episodic radiations in the fly tree of life. Proc Natl Acad Sci U S A. 2011:108(14):5690–5695. 10.1073/pnas.1012675108 PubMed DOI PMC
Wiegmann BM, Yeates DK.. Phylogeny of Diptera. In: Kirk-Spriggs AH, Sinclair BJ, editors. Manual of Afrotropical Diptera. Vol. 4. SANBI Publishing, Pretoria, South Africa; 2017. p. 253–265.
Woodward G, Hildrew AG.. Differential vulnerability of prey to an invading top predator: integrating field surveys and laboratory experiments. Ecol Entomol. 2002:27(6):732–744. 10.1046/j.1365-2311.2002.00462.x DOI
Yu G, Smith DK, Zhu H, Guan Y, Lam TT.. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol. 2017:8(1):28–36. 10.1111/2041-210x.12628 DOI