Abstract
Appreciation for the role of cryptofauna in ecological systems has increased dramatically over the past decade. The impacts blood-feeding arthropods, such as ticks and mosquitos, have on terrestrial communities are the subject of hundreds of papers annually. However, blood-feeding arthropods have been largely ignored in marine environments. Gnathiid isopods, often referred to as “ticks of the sea”, are temporary external parasites of fishes. They are found in all marine environments and have many consequential impacts on host fitness. Because they are highly mobile and only associated with their hosts while obtaining a blood meal, their broader trophic connections are difficult to discern. Conventional methods rely heavily on detecting gnathiids on wild-caught fishes. However, this approach typically yields few gnathiids and does not account for hosts that avoid capture. To overcome this limitation, we sequenced blood meals of free-living gnathiids collected in light traps to assess the host range and community-dependent exploitation of Caribbean gnathiid isopods. Using fish-specific COI (cox1) primers, sequencing individual blood meals from 1060 gnathiids resulted in the identification of 70 host fish species from 27 families. Comparisons of fish assemblages to blood meal identification frequencies at four collection sites indicated that fishes within the families Haemulidae (grunts) and Lutjanidae (snappers) were exploited more frequently than expected based on their biomass, and Labrid parrotfishes were exploited less frequently than expected. The broad host range along with the biased exploitation of diel-migratory species has important implications for the role gnathiid isopods play in Caribbean coral reef communities.
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Data availability
These data were contributed to the Biological & Chemical Oceanography Data Management Office (BCO-DMO) database under the project title “Beyond Cleaning Symbiosis: Ecology of ‘Ticks of the Sea’ on Coral Reefs” (https://www.bco-dmo.org/project/562115).
Code availability
Not applicable.
References
Alcaide M, Rico C, Ruiz S, Soriguer R, Muñoz J, Figuerola J (2009) Disentangling vector-borne transmission networks: a universal DNA barcoding method to identify vertebrate hosts from arthropod bloodmeals. PLoS One 4:e7092. https://doi.org/10.1371/journal.pone.0007092
Allan BJM, Illing B, Fakan EP, Narvaez P, Grutter AS, Sikkel PC, McClure EC, Rummer JL, McCormick MI (2020) Parasite infection directly impacts escape response and stress levels in fish. J Exp Biol 223:1–8. https://doi.org/10.1242/jeb.230904
Artim JM, Sikkel PC (2016) Comparison of sampling methodologies and estimation of population parameters for a temporary fish ectoparasite. Int J Parasitol Parasites Wildl 5:145–157. https://doi.org/10.1016/j.ijppaw.2016.05.003
Artim JM, Sellers JC, Sikkel PC (2015) Micropredation by gnathiid isopods on settlement-stage reef fish in the eastern Caribbean Sea. Bull Mar Sci 91:479–487. https://doi.org/10.5343/bms.2015.1023
Artim JM, Hook A, Grippo RS, Sikkel PC (2017) Predation on parasitic gnathiid isopods on coral reefs: a comparison of Caribbean cleaning gobies with non-cleaning microcarnivores. Coral Reefs 36:1213–1223. https://doi.org/10.1007/s00338-017-1613-6
Artim JM, Nicholson MD, Hendrick GC, Brandt M, Smith TB, Sikkel PC (2020) Abundance of a cryptic generalist parasite reflects degradation of an ecosystem. Ecosphere 11:1–8. https://doi.org/10.1002/ecs2.3268
Bakhoum MT, Fall M, Seck MT, Gardès L, Fall AG, Diop M, Mall I, Balenghien T, Baldet T, Gimonneau G, Garros C, Bouyer J (2016) Foraging range of arthropods with veterinary interest: New insights for Afrotropical Culicoides biting midges (Diptera: Ceratopogonidae) using the ring method. Acta Trop 157:59–67. https://doi.org/10.1016/j.actatropica.2016.01.023
Bellwood DR (1996) The Eocene fishes of Monte Bolca: the earliest coral reef fish assemblage. Coral Reefs 15:11–19. https://doi.org/10.1007/s003380050025
Bhattacharya M, Sharma AR, Patra BC, Sharma G, Seo EM, Nam JS, Chakraborty C, Lee SS (2016) DNA barcoding to fishes: Current status and future directions. Mitochondrial DNA 27:2744–2752. https://doi.org/10.3109/19401736.2015.1046175
Borland EM, Kading RC (2021) Modernizing the toolkit for arthropod bloodmeal identification. InSects 12:37. https://doi.org/10.3390/insects12010037
Boucek RE, Ellis RD, Forauer AR, Adams AJ (2022) A decade-long connectivity study of Permit (Trachinotus falcatus) in Florida supports a spatial management approach. Environ Biol Fishes. https://doi.org/10.1007/s10641-022-01302-z
Brandl SJ, Casey JM, Knowlton N, Duffy JE (2017) Marine dock pilings foster diverse, native cryptobenthic fish assemblages across bioregions. Ecol Evol 7:7069–7079. https://doi.org/10.1002/ece3.3288
Brandl SJ, Goatley CHR, Bellwood DR, Tornabene L (2018) The hidden half: ecology and evolution of cryptobenthic fishes on coral reefs. Biol Rev 93:1846–1873. https://doi.org/10.1111/brv.12423
Brandl SJ, Tornabene L, Goatley CHR, Casey JM, Morais RA, Côté IM, Baldwin CC, Parravicini V, Schiettekatte NMD, Bellwood DR (2019) Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science 364:1189–1192. https://doi.org/10.1126/science.aav3384
Brugman VA, Hernández-Triana LM, Prosser SWJ, Weland C, Westcott DG, Fooks AR, Johnson N (2015) Molecular species identification, host preference and detection of myxoma virus in the Anopheles maculipennis complex (Diptera: Culicidae) in southern England, UK. Parasit Vectors 8:421. https://doi.org/10.1186/s13071-015-1034-8
Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Modell 197:516–519. https://doi.org/10.1016/j.ecolmodel.2006.03.017
Caminade C, McIntyre KM, Jones AE (2019) Impact of recent and future climate change on vector-borne diseases. Ann N Y Acad Sci 1436:157–173. https://doi.org/10.1111/nyas.13950
Chen HW, Shao KT, Liu CWJ, Lin WH, Liu WC (2011) The reduction of food web robustness by parasitism: fact and artefact. Int J Parasitol 41:627–634. https://doi.org/10.1016/j.ijpara.2010.12.013
Clark RD, Pittman S, Caldow C, Christensen J, Roque B, Appeldoorn RS, Monaco ME (2009) Nocturnal fish movement and trophic flow across habitat boundaries in a coral reef ecosystem (SW Puerto Rico). Caribb J Sci 45:282–303. https://doi.org/10.18475/cjos.v45i2.a15
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Austral Ecol 18:117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
Coile AM, Sikkel PC (2013) An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology 140:888–896. https://doi.org/10.1017/S0031182013000097
Coile AM, Welicky RL, Sikkel PC (2014) Female Gnathia marleyi (Isopoda: Gnathiidae) feeding on more susceptible fish hosts produce larger but not more offspring. Parasitol Res 113:3875–3880. https://doi.org/10.1007/s00436-014-4090-7
Cook CA, Sikkel PC, Renoux LP, Smit NJ (2015) Blood parasite biodiversity of reef-associated fishes of the eastern Caribbean. Mar Ecol Prog Ser 533:1–13. https://doi.org/10.3354/meps11430
Cowman PF (2014) Historical factors that have shaped the evolution of tropical reef fishes: a review of phylogenies, biogeography, and remaining questions. Front Genet 5:1–15. https://doi.org/10.3389/fgene.2014.00394
Curtis LM, Grutter AS, Smit NJ, Davies AJ (2013) Gnathia aureamaculosa, a likely definitive host of Haemogregarina balistapi and potential vector for Haemogregarina bigemina between fishes of the Great Barrier Reef, Australia. Int J Parasitol 43:361–370. https://doi.org/10.1016/j.ijpara.2012.11.012
Dallas T, Huang S, Nunn C, Park AW, Drake JM (2017) Estimating parasite host range. Proc R Soc B Biol Sci 284:20171250. https://doi.org/10.1098/rspb.2017.1250
Davies AJ (1995) The biology of fish haemogregarines. Adv Parasitol 36:191–201. https://doi.org/10.1016/S0065-308X(08)60491-1
Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:516–519. https://doi.org/10.18637/jss.v022.i04
Esser HJ, Mögling R, Cleton NB, Van Der Jeugd H, Sprong H, Stroo A, Koopmans MPG, De Boer WF, Reusken CBEM (2019) Risk factors associated with sustained circulation of six zoonotic arboviruses: a systematic review for selection of surveillance sites in non-endemic areas. Parasit Vectors 12:1–17. https://doi.org/10.1186/s13071-019-3515-7
Farquharson C, Smit NJ, Sikkel PC (2012) Gnathia marleyi sp. nov. (Crustacea, Isopoda, Gnathiidae) from the Eastern Caribbean. Zootaxa 3381:47. https://doi.org/10.11646/zootaxa.3381.1.3
Fenton A, Streicker DG, Petchey OL, Pedersen AB (2015) Are all hosts created equal? Partitioning host species contributions to parasite persistence in multihost communities. Am Nat 186:610–622. https://doi.org/10.1086/683173
Ferreira ML, Smit NJ, Grutter AS, Davies AJ (2009) A new species of Gnathiid (Crustacea: Isopoda) parasitizing Teleosts from Lizard Island, Great Barrier Reef, Australia. J Parasitol 95:1066–1075. https://doi.org/10.1645/GE-1920.1
Floeter SR, Bender MG, Siqueira AC, Cowman PF (2018) Phylogenetic perspectives on reef fish functional traits. Biol Rev 93:131–151. https://doi.org/10.1111/brv.12336
Francois CM, Simon L, Malard F, Lefébure T, Douady CJ, Mermillod-Blondin F (2020) Trophic selectivity in aquatic isopods increases with the availability of resources. Funct Ecol 34:1078–1090. https://doi.org/10.1111/1365-2435.13530
Gibson AK, Baffoe-Bonnie H, Penley MJ, Lin J, Owens R, Khalid A, Morran LT, Baffoe-Bonnie H, Penley MJ, Lin J, Owens R, Khalid A, Morran LT (2020) The evolution of parasite host range in heterogeneous host populations. J Evol Biol 33:773–782. https://doi.org/10.1111/jeb.13608
Green AL, Maypa AP, Almany GR, Rhodes KL, Weeks R, Abesamis RA, Gleason MG, Mumby PJ, White AT (2015) Larval dispersal and movement patterns of coral reef fishes, and implications for marine reserve network design. Biol Rev 90:1215–1247. https://doi.org/10.1111/brv.12155
Grutter AS (1994) Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia. Mar Ecol Prog Ser 115:21–30. https://doi.org/10.3354/meps115021
Grutter AS (1995) Relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:51–58. https://doi.org/10.3354/meps118051
Grutter A (1996) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol Prog Ser 130:61–70. https://doi.org/10.3354/meps130061
Grutter AS, Crean AJ, Curtis LM, Kuris AM, Warner RR, Mccormick MI (2011a) Indirect effects of an ectoparasite reduce successful establishment of a damselfish at settlement. Funct Ecol 25:586–594. https://doi.org/10.1111/j.1365-2435.2010.01798.x
Grutter AS, Rumney JG, Sinclair-Taylor T, Waldie P, Franklin CE (2011b) Fish mucous cocoons: the “mosquito nets” of the sea. Biol Lett 7:292–294. https://doi.org/10.1098/rsbl.2010.0916
Hasle G (2013) Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front Cell Infect Microbiol 4:1–6. https://doi.org/10.3389/fcimb.2013.00048
Hayes PM, Smit NJ, Grutter AS, Davies AJ (2011) Unexpected response of a captive blackeye thicklip, Hemigymnus melapterus (Bloch), from Lizard Island, Australia, exposed to juvenile isopods Gnathia aureamaculosa Ferreira & Smit. J Fish Dis 34:563–566. https://doi.org/10.1111/j.1365-2761.2011.01261.x
Hendrick GC, Dolan MC, McKay T, Sikkel PC (2019) Host DNA integrity within blood meals of hematophagous larval gnathiid isopods (Crustacea, Isopoda, Gnathiidae). Parasit Vectors 12:316. https://doi.org/10.1186/s13071-019-3567-8
Hendrick GC, Nicholson MD, Narvaez P, Sun D, Packard A, Grutter AS, Sikkel PC (2023) Diel fish migration facilitates functional connectivity of coral reef and seagrass habitats via transport of ectoparasites. Mar Ecol Prog Ser. https://doi.org/10.3354/meps14339
Heupel MR, Bennett MB (1999) The occurrence, distribution and pathology associated with gnathiid isopod larvae infecting the epaulette shark, Hemiscyllium ocellatum. Int J Parasitol 29:321–330. https://doi.org/10.1016/S0020-7519(98)00218-5
Jenkins WG, Demopoulos AWJ, Sikkel PC (2018) Effects of host injury on susceptibility of marine reef fishes to ectoparasitic gnathiid isopods. Symbiosis 75:113–121. https://doi.org/10.1007/s13199-017-0518-z
Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, Poulin R, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371. https://doi.org/10.1016/j.tree.2010.01.005
Jones CM, Grutter AS (2005) Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. J Fish Biol 66:860–864. https://doi.org/10.1111/j.0022-1112.2005.00640.x
Jones CM, Nagel L, Hughes GL, Cribb TH, Grutter AS (2007) Host specificity of two species of Gnathia (Isopoda) determined by DNA sequencing blood meals. Int J Parasitol 37:927–935. https://doi.org/10.1016/j.ijpara.2007.01.011
Kent RJ (2009) Molecular methods for arthropod bloodmeal identification and applications to ecological and vector-borne disease studies. Mol Ecol Resour 9:4–18. https://doi.org/10.1111/j.1755-0998.2008.02469.x
Kilpatrick HJ, Labonte AM, Stafford KC (2014) The relationship between deer density, tick abundance, and human cases of lyme disease in a residential community. J Med Entomol 51:777–784. https://doi.org/10.1603/ME13232
Kimirei IA, Nagelkerken I, Trommelen M, Blankers P, van Hoytema N, Hoeijmakers D, Huijbers CM, Mgaya YD, Rypel AL (2013) What drives ontogenetic niche shifts of fishes in coral reef ecosystems? Ecosystems 16:783–796. https://doi.org/10.1007/s10021-013-9645-4
Kirkim F, Gozler AM, Kopuz U, Agirbas E (2011) New records of two species of Gnathiid Isopods, Paragnathia Formica (Hesse, 1864) and Gnathia Maxillaris (Montagu, 1804) (Isopoda, Gnathiidae) from the Black Sea. Crustaceana 84:1719–1725. https://doi.org/10.1163/156854011X607088
Knowlton N, Brainard RE, Fisher R, Moews M, Plaisance L, Caley MJ (2010) Coral Reef Biodiversity. Life World’s Ocean Divers Distrib Abundance 65–77
Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends Ecol Evol 17:507–513. https://doi.org/10.1016/S0169-5347(02)02615-0
Lafferty KD, Kuris AM (2009) Parasites reduce food web robustness because they are sensitive to secondary extinction as illustrated by an invasive estuarine snail. Philos Trans R Soc B Biol Sci 364:1659–1663. https://doi.org/10.1098/rstb.2008.0220
Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216. https://doi.org/10.1073/pnas.0604755103
Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546. https://doi.org/10.1111/j.1461-0248.2008.01174.x
Lassen SB, Nielsen SA, Kristensen M (2012) Identity and diversity of blood meal hosts of biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasit Vectors 5:1–10. https://doi.org/10.1186/1756-3305-5-143
McKiernan JP, Grutter AS, Davies AJ (2005) Reproductive and feeding ecology of parasitic gnathiid isopods of epaulette sharks (Hemiscyllium ocellatum) with consideration of their role in the transmission of a haemogregarine. Int J Parasitol 35:19–27. https://doi.org/10.1016/j.ijpara.2004.10.016
Nagel L, Grutter AS (2007) Host preference and specialization in Gnathia sp., a common parasitic isopod of coral reef fishes. J Fish Biol 70:497–508. https://doi.org/10.1111/j.1095-8649.2007.01320.x
Nagel L, Lougheed SC (2006) A simple molecular technique for identifying marine host fish by sequencing blood—feeding parasites. J Parasitol 92:665–668
Nagelkerken I, Dorenbosch M, Verberk W, Cocheret de la Morinière E, van der Velde G (2000) Day-night shifts of fishes between shallow-water biotopes of a Caribbean bay, with emphasis on the nocturnal feeding of Haemulidae and Lutjanidae. Mar Ecol Prog Ser 194:55–64. https://doi.org/10.3354/meps194055
Nemtzov SC (1994) Intraspecific variation in sand-diving and predator avoidance behavior of green razorfish, Xyrichtys splendens (Pisces, Labridae): effect on courtship and mating success. Environ Biol Fishes 41:403–414. https://doi.org/10.1007/BF02197856
Nicholson MD, Artim JD, Hendrick GC, Packard AJ, Sikkel PC (2019) Fish-parasitic Gnathiid isopods metamorphose following invertebrate-derived meal. J Parasitol 105:793. https://doi.org/10.1645/19-59
Nicholson MD, Hendrick GC, Packard AJ, Strobel DL, Vondriska C, Sikkel PC (2020) Vertical limits of host infestation by Gnathiid isopods (Isopoda: Gnathiidae) parasitic on Caribbean coral reef fishes. J Crustac Biol 40:866–871. https://doi.org/10.1093/jcbiol/ruaa067
Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O’Hara R, Solymos P, Stevens M, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Ribeiro Cunha E, Smith T, Stier A, Ter Braak C, Weedon J (2022) Vegan: Community Ecology Package. R package version 2.6–2. https://CRAN.R-project.org/package=vegan
Pagán JA, Veríssimo A, Sikkel PC, Xavier R (2020) Hurricane-induced disturbance increases genetic diversity and population admixture of the direct-brooding isopod, Gnathia marleyi. Sci Rep 10:8649. https://doi.org/10.1038/s41598-020-64779-7
Pagán JA, Xavier R, Sikkel PC, Veríssimo A (2022) Host-mediated dispersal shapes spatial distribution of genetic variability in marine symbionts. Bull Mar Sci 98:317–330. https://doi.org/10.5343/bms.2021.0046
Paula JR, Sun D, Pissarra V, Narvaez P, Rosa R, Grutter AS, Sikkel PC (2021) The role of corals on the abundance of a fish ectoparasite in the Great Barrier Reef. Coral Reefs 40:535–542. https://doi.org/10.1007/s00338-021-02051-8
Pearman JK, Leray M, Villalobos R, Machida RJ, Berumen ML, Knowlton N, Carvalho S (2018) Cross-shelf investigation of coral reef cryptic benthic organisms reveals diversity patterns of the hidden majority. Sci Rep 8:1–18. https://doi.org/10.1038/s41598-018-26332-5
Penfold R, Grutter A, Kuris A, McCormick M, Jones C (2008) Interactions between juvenile marine fish and gnathiid isopods: predation versus micropredation. Mar Ecol Prog Ser 357:111–119. https://doi.org/10.3354/meps07312
Quattrini AM, Demopoulos AWJ (2016) Ectoparasitism on deep-sea fishes in the western North Atlantic: In situ observations from ROV surveys. Int J Parasitol Parasites Wildl 5:217–228. https://doi.org/10.1016/j.ijppaw.2016.07.004
Raffel TR, Martin LB, Rohr JR (2008) Parasites as predators: unifying natural enemy ecology. Trends Ecol Evol 23:610–618. https://doi.org/10.1016/j.tree.2008.06.015
Reaka-Kudla ML (1997) The global biodiversity of coral reefs: a comparison with rain forests. In: Reaka-Kudla ML, Wilson DE, Wilson EO (eds) Biodiversity II: understanding and protecting our biological resources. Joseph Henry Press, Washington, pp 83–108
Reeves LE, Holderman CJ, Gillett-Kaufman JL, Kawahara AY, Kaufman PE (2016) Maintenance of host DNA integrity in field-preserved mosquito (Diptera: Culicidae) blood meals for identification by DNA barcoding. Parasit Vectors 9:1–11. https://doi.org/10.1186/s13071-016-1791-z
Saint-Béat B, Baird D, Asmus H, Asmus R, Bacher C, Pacella SR, Johnson GA, David V, Vézina AF, Niquil N (2015) Trophic networks: How do theories link ecosystem structure and functioning to stability properties? A review. Ecol Indic 52:458–471. https://doi.org/10.1016/j.ecolind.2014.12.017
Santos TRN, Sikkel PC (2019) Habitat associations of fish-parasitic gnathiid isopods in a shallow reef system in the central Philippines. Mar Biodivers 49:83–96. https://doi.org/10.1007/s12526-017-0756-6
Sellers JC, Holstein DM, Botha TL, Sikkel PC (2019) Lethal and sublethal impacts of a micropredator on post-settlement Caribbean reef fishes. Oecologia 189:293–305. https://doi.org/10.1007/s00442-018-4262-8
Shan B, Liu Y, Yang C, Zhao Y, Zhang G, Wu Q, Sun D (2021) DNA barcoding of fish in mischief reef—fish diversity of a reef fish community from Nansha Islands. Front Mar Sci 7:1–10. https://doi.org/10.3389/fmars.2020.618954
Shodipo MO, Gomez RDC, Welicky RL, Sikkel PC (2019) Apparent kleptoparasitism in fish—parasitic gnathiid isopods. Parasitol Res 118:653–655. https://doi.org/10.1007/s00436-018-6152-8
Sikkel PC, Cheney KL, Côté IM (2004) In situ evidence for ectoparasites as a proximate cause of cleaning interactions in reef fish. Anim Behav 68:241–247. https://doi.org/10.1016/j.anbehav.2003.10.023
Sikkel PC, Schaumburg CS, Mathenia JK (2006) Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish. Coral Reefs 25:683–689. https://doi.org/10.1007/s00338-006-0154-1
Sikkel PC, Ziemba RE, Sears WT, Wheeler JC (2009) Diel ontogenetic shift in parasitic activity in a gnathiid isopod on Caribbean coral reefs. Coral Reefs 28:489–495. https://doi.org/10.1007/s00338-009-0474-z
Sikkel PC, Tuttle LJ, Cure K, Coile AM, Hixon MA (2014) Low susceptibility of invasive red lionfish (Pterois volitans) to a generalist ectoparasite in both its introduced and native ranges. PLoS One 9:1–8. https://doi.org/10.1371/journal.pone.0095854
Sikkel PC, Welicky RL, Artim JM, McCammon AM, Sellers JC, Coile AM, Jenkins WG (2017) Nocturnal migration reduces exposure to micropredation in a coral reef fsh. Bull Mar Sci 93:475–489. https://doi.org/10.5343/bms.2016.1021
Sikkel PC, Pagan JA, Santos JL, Hendrick GC, Nicholson MD, Xavier R (2020) Molecular detection of apicomplexan blood parasites of coral reef fishes from free-living stages of ectoparasitic gnathiid isopods. Parasitol Res 119:1975–1980. https://doi.org/10.1007/s00436-020-06676-6
Sikkel PC, Welicky RL (2019) The ecological significance of parasitic crustaceans. pp 421–477
Smit NJ, Davies AJ (2004) The curious life-style of the parasitic stages of gnathiid isopods. Adv Parasitol 58:289–391. https://doi.org/10.1016/S0065-308X(04)58005-3
Stuart-Smith RD, Mellin C, Bates AE, Edgar GJ (2021) Habitat loss and range shifts contribute to ecological generalization among reef fishes. Nat Ecol Evol 5:656–662. https://doi.org/10.1038/s41559-020-01342-7
Tanaka K (2007) Life history of gnathiid isopods-current knowledge and future directions. Plankt Benthos Res 2:1–11. https://doi.org/10.3800/pbr.2.1
Tatom-Naecker TAM, Westneat MW (2018) Burrowing fishes: kinematics, morphology and phylogeny of sand-diving wrasses (Labridae). J Fish Biol 93:860–873. https://doi.org/10.1111/jfb.13789
Timi JT, Poulin R (2020) Why ignoring parasites in fish ecology is a mistake. Int J Parasitol 50:755–761. https://doi.org/10.1016/j.ijpara.2020.04.007
Triki Z, Grutter AS, Bshary R, Ros AFH (2016) Effects of short-term exposure to ectoparasites on fish cortisol and hematocrit levels. Mar Biol 163:187. https://doi.org/10.1007/s00227-016-2959-y
Acknowledgements
We thank E. Brill, K. Driskill, A. McCammon, S. Robles, A. Savage, T. Santos, J. Sellers, B. Velez, O. Rullan, and A. Hook for their assistance during field work. We also thank E. Babcock for insightful discussions regarding statistical analyses. We thank the staff of the MacLean Marine Science Center of University of the Virgin Islands, Arkansas State University, Arkansas Biosciences Institute, and the Isla Magueyes Marine Laboratories, University of Puerto Rico. Funding was generously provided by U.S. National Science Foundation grant OCE-1536794 (PC Sikkel, PI). This is contribution number 282 from the University of the Virgin Islands Center for Marine and Environmental Studies and is dedicated to the memory of James (Jimmy) William Buffett.
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Funding was provided by U.S. National Science Foundation Grant OCE-1536794 (PC Sikkel, PI).
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GCH, JDA, MCD, and PCS conceived the idea and designed the study. GCH, MDN, JDA, and PCS developed field methodologies. GCH and MCD developed molecular methods. GCH, MDN, JAP, JDA, and PCS conducted fieldwork. GCH performed laboratory work, data analysis, and wrote the manuscript. MDN, JAP, JDA, MCD, and PCS provided editorial advice.
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Hendrick, G.C., Nicholson, M.D., Pagan, J.A. et al. Blood meal identification reveals extremely broad host range and host-bias in a temporary ectoparasite of coral reef fishes. Oecologia 203, 349–360 (2023). https://doi.org/10.1007/s00442-023-05468-w
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DOI: https://doi.org/10.1007/s00442-023-05468-w