Metazoan parasite communities: support for the biological invasion of Barbus barbus and its hybridization with the endemic Barbus meridionalis
Language English Country Great Britain, England Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
27855708
PubMed Central
PMC5114731
DOI
10.1186/s13071-016-1867-9
PII: 10.1186/s13071-016-1867-9
Knihovny.cz E-resources
- Keywords
- Biological invasion, Cyprinid fish, Hybridization, Metazoan parasite communities,
- MeSH
- Biodiversity * MeSH
- Chimera classification genetics growth & development parasitology MeSH
- Cyprinidae classification genetics growth & development parasitology MeSH
- Microsatellite Repeats MeSH
- Parasite Load MeSH
- Parasites classification isolation & purification MeSH
- Rivers MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- France MeSH
BACKGROUND: Recently, human intervention enabled the introduction of Barbus barbus from the Rhône River basin into the Barbus meridionalis habitats of the Argens River. After an introduction event, parasite loss and lower infection can be expected in non-native hosts in contrast to native species. Still, native species might be endangered by hybridization with the incomer and the introduction of novel parasite species. In our study, we aimed to examine metazoan parasite communities in Barbus spp. populations in France, with a special emphasis on the potential threat posed by the introduction of novel parasite species by invasive B. barbus to local B. meridionalis. METHODS: Metazoan parasite communities were examined in B. barbus, B. meridionalis and their hybrids in three river basins in France. Microsatellites were used for the species identification of individual fish. Parasite abundance, prevalence, and species richness were compared. Effects of different factors on parasite infection levels and species richness were tested using GLM. RESULTS: Metazoan parasites followed the expansion range of B. barbus and confirmed its introduction into the Argens River. Here, the significantly lower parasite number and lower levels of infection found in B. barbus in contrast to B. barbus from the Rhône River supports the enemy release hypothesis. Barbus barbus × B. meridionalis hybridization in the Argens River basin was confirmed using both microsatellites and metazoan parasites, as hybrids were infected by parasites of both parental taxa. Trend towards higher parasite diversity in hybrids when compared to parental taxa, and similarity between parasite communities from the Barbus hybrid zone suggest that hybrids might represent "bridges" for parasite infection between B. barbus and B. meridionalis. Risk of parasite transmission from less parasitized B. barbus to more parasitized B. meridionalis indicated from our study in the Argens River might be enhanced in time as higher infection levels in B. barbus from the Rhône River were revealed. Hybrid susceptibility to metazoan parasites varied among the populations and is probably driven by host-parasite interactions and environmental forces. CONCLUSIONS: Scientific attention should be paid to the threatened status of the endemic B. meridionalis, which is endangered by hybridization with the invasive B. barbus, i.e. by genetic introgression and parasite transmission.
See more in PubMed
Qiu YX, Hong DY, Fu CHX, Cameron KM. Genetic variation in the endangered and endemic species Changium smyrnioides (Apiaceae) Biochem Sys Ecol. 2004;32:583–596. doi: 10.1016/j.bse.2003.08.004. DOI
Juan A, Crespo MB, Cowan RS, Lexer C, Fay MF. Patterns of variability and gene flow in Medicago citrina, an endangered endemic of islands in the western Mediterranean, as revealed by amplified fragment length polymorphism (AFLP) Mol Ecol. 2004;13:2679–2690. doi: 10.1111/j.1365-294X.2004.02289.x. PubMed DOI
Ogutu-Ohwayo R. The effects of predation by nile perch, Lates niloticus L., on the fish of Lake Nabugabo, with suggestions for conservation of endangered endemic cichlids. Conserv Biol. 1993;7:701–711. doi: 10.1046/j.1523-1739.1993.07030701.x. DOI
Ogutu-Ohwayo R. Nile perch in Lake Victoria: the balance between benefits and negative impacts of aliens. In: Sanlund OT, Schei PJ, editors. Invasive species and biodiversity management. Dordrecht: Kluwer Academic Publishers; 1999. pp. 47–63.
Fisher RN, Bradley SH. The decline of amphibians in California's Great Central Valley. Conserv Biol. 1996;1:1387–1397. doi: 10.1046/j.1523-1739.1996.10051387.x. DOI
Vilà M, Weiner J. Are invasive plant species better competitors than native plant species? Evidence from pair-wise experiments. Oikos. 2004;105:229–238. doi: 10.1111/j.0030-1299.2004.12682.x. DOI
Perry WL, Lodge DM, Feder JL. Importance of hybridization between indigenous and nonindigenous freshwater species: an overlooked threat to North American biodiversity. Syst Biol. 2002;51:255–275. doi: 10.1080/10635150252899761. PubMed DOI
De la Rúa P, Jaffé R, Dall'Olio R, Muñoz I, Serrano J. Biodiversity, conservation and current threats to European honeybees. Apidologie. 2009;40:263–284. doi: 10.1051/apido/2009027. DOI
Biedrzycka A, Solarz W, Okarma H. Hybridization between native and introduced species of deer in Eastern Europe. J Mammal. 2012;93:1331–1341. doi: 10.1644/11-MAMM-A-022.1. DOI
Knopf K, Mahnke M. Differences in susceptibility of the European eel (Anguilla anguilla) and the Japanese eel (Anguilla japonica) to the swimbladder nematode Anguillicola crassus. Parasitology. 2004;129:491–496. doi: 10.1017/S0031182004005864. PubMed DOI
Woodworth BL, Atkinson CT, LaPointe DA, Hart PJ, Spiegel CS, Tweed EJ, et al. Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria. Proc Natl Acad Sci U S A. 2005;102:1531–1536. doi: 10.1073/pnas.0409454102. PubMed DOI PMC
Kirk RS. The impact of Anguillicola crassus on European eels. Fish Manag Ecol. 2003;10:385–394. doi: 10.1111/j.1365-2400.2003.00355.x. DOI
Egusa S. Nematode diseases. In: Egusa S, editor. Infectious Diseases of Fish. Rotterdam/Brookfield: A.A. Balkema; 1992. pp. 643–657.
van Banning P, Haenen OLM. Effects of the swimbladder nematode Anguillicola crassus in wild and farmed eel, Anguilla anguilla. In: Perkins FO, Cheng TC, editors. Pathology in Marine Science. 1990. pp. 317–330.
Molnár K, Székely C, Baska F. Mass mortality of eel in Lake Balaton due to Anguillicola crassus infection. Bull Eur Assoc Fish Pathol. 1991;11:211–212.
Molnár K, Baska F, Csaba G, Glávits R, Székely C. Pathological and histopathological studies of the swimbladder of eels Anguilla anguilla infected by Anguillicola crassus (Nematoda: Dracunculoidea) Dis Aquat Organ. 1993;15:41–50. doi: 10.3354/dao015041. DOI
Baruš V, Moravec F, Prokeš M. Anguillicolosis of the European eel (Anguilla anguilla) in the Czech Republic. Czech J Anim Sci. 1999;44:423–431.
Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM. Introduced species and their missing parasites. Nature. 2003;421:628–630. doi: 10.1038/nature01346. PubMed DOI
Keane RM, Crawley MJ. Exotic plant invasions and the enemy release hypothesis. Trends Ecology Evol. 2002;27:164–170. doi: 10.1016/S0169-5347(02)02499-0. DOI
Blakeslee AMH, Altman I, Whitman Miller A, Byers JE, Hamer CE, Ruiz GM. Parasites and invasions: a biogeographic examination of parasites and hosts in native and introduced ranges. J Biogeogr. 2012;39:609–622. doi: 10.1111/j.1365-2699.2011.02631.x. DOI
Torchin ME, Lafferty KD, Kuris AM. Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions. 2001;3:333–345. doi: 10.1023/A:1015855019360. DOI
Ondračková M, Valová Z, Hudcová I, Michálková V, Šimková A, Borcherding J, Jurajda P. Temporal effects on host-parasite associations in four naturalized goby species living in sympatry. Hydrobiologia. 2015;746:233–243. doi: 10.1007/s10750-014-1967-5. DOI
Poulin R, Mouillot D. Host introductions and the geography of parasite taxonomic diversity. J Biogeogr. 2003;30:837–845. doi: 10.1046/j.1365-2699.2003.00868.x. DOI
Dupont F, Crivelli AJ. Do parasites confer a disadvantage to hybrids? A case study of Alburnus alburnus × Rutilus rubilio, a natural hybrid of Lake Mikri Prespa, Northern Greece. Oecologia. 1988;75:587–592. doi: 10.1007/BF00776424. PubMed DOI
Šimková A, Dávidová M, Papoušek I, Vetešník L. Does interspecies hybridization affect the host specificity of parasites in cyprinid fish? Parasit Vectors. 2013;6:95. doi: 10.1186/1756-3305-6-95. PubMed DOI PMC
Floate KD, Whitham TG. The "hybrid bridge" hypothesis: host shifting via plant hybrid swarms. Am Nat. 1993;141:651–662. doi: 10.1086/285497. PubMed DOI
Persat H, Berrebi P. Relative ages of present populations of Barbus barbus and Barbus meridionalis (Cyprinidae) in southern France: preliminary considerations. Aquat Living Resour. 1990;3:253–263. doi: 10.1051/alr:1990027. DOI
Kotlík P, Berrebi P. Phylogeography of the barbel (Barbus barbus) assessed by mitochondrial DNA variation. Mol Ecol. 2001;10:2177–2186. doi: 10.1046/j.0962-1083.2001.01344.x. PubMed DOI
Berrebi P, Lamy G, Cattaneo-Berrebi G, Renno JF. Variabilité génétique de Barbus meridionalis Risso (Cyprinidae): une espèce quasi monomorphe. B Fr Peche Piscic. 1988;310:77–84. doi: 10.1051/kmae:1988007. DOI
Crespin L, Berrebi P. L’hybridation naturelle entre le barbeau commun et le barbeau méridional en France. Compte rendu de dix années de recherche. B Fr Peche Piscic. 1994;334:177–189. doi: 10.1051/kmae:1994020. DOI
Agence de l'eau Rhône Méditerranée et Corse. Etude de détermination des volumes prélevables. Bassin versant de l’Argens. Phases 4, 5 et 6. 2013. http://www.rhone-mediterranee.eaufrance.fr/docs/gestion-quantitative/EEVPG/argens/EVP_argens_rapport_ph4%265%266_juin2013.pdf. Accessed 27 Feb 2016.
BIOTOPE – Agence Paca. Document d'objectifs du site Natura FR9301627 « Embouchure de L´Argens » Tome 1, Fiches Espèces. 2011. http://embouchure-argens.n2000.fr/sites/embouchure-argens.n2000.fr/files/documents/page/DOCOB20-20Fiches20especes.pdf. Accessed 01 Mar 2016.
Kiener A, Delize A, Belkior P. Aspects piscicoles du flevue Argens (Var) Bull Fr Piscic. 1981;282:43–74. doi: 10.1051/kmae:1981014. DOI
Molecular Ecology Resources Database. http://tomato.bio.trinity.edu/manuscripts/13-5/mer-13-0090.pdf. Accessed 27 Feb 2016.
Agostini C, Albaladejo RG, Aparicio A, Arthofer W, Berrebi P, Boag PT, et al. Permanent genetic resources added to molecular ecology resources database 1 April 2013–31 May 2013. Mol Ecol Resour. 2013;13:966–968. doi: 10.1111/1755-0998.12140. PubMed DOI
Chenuil A, Desmarais E, Pouyaud L, Berrebi B. Does polyploidy lead to fewer and shorter microsatellites in Barbus (Teleostei: Cyprinidae)? Mol Ecol. 1997;6:169–178. doi: 10.1046/j.1365-294X.1997.00170.x. PubMed DOI
Van Oosterhout C, Hutchinson WF, Derek P, Wills M, Shipley P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes. 2004;4:535–539. doi: 10.1111/j.1471-8286.2004.00684.x. DOI
Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–959. PubMed PMC
Gompert Z, Buerkle CA. Introgress: a software package for mapping components of isolation in hybrids. Mol Ecol Resour. 2010;10:378–384. doi: 10.1111/j.1755-0998.2009.02733.x. PubMed DOI
Andrés JA, Larson EL, Bogdanowicz SM, Harrison RG. Patterns of transcriptome divergence in the male accessory gland of two closely related species of field crickets. Genetics. 2013;193:501–513. doi: 10.1534/genetics.112.142299. PubMed DOI PMC
Ergens R, Lom J. Causative agents of fish diseases. Prague: Academia; 1970.
Lamková K, Šimková A, Palíková M, Jurajda P, Lojek A. Seasonal changes of immunocompetence and parasitism in chub (Leuciscus cephalus), a freshwater cyprinid fish. Parasitol Res. 2007;101:775–789. doi: 10.1007/s00436-007-0546-3. PubMed DOI
Pugachev ON, Gerasev PI, Gussev AV, Ergens R, Khotenowsky I. Guide to Monogenoidea of freshwater fish of Palearctic and Amur regios. Milan: Ledizione-Ledi Publishing; 2009.
Špakulová M, Perrot-Minnot MJ, Neuhaus B. Resurrection of Pomphorhynchus tereticollis (Rudolphi, 1809) (Acanthocephala: Pomphorhynchidae) based on new morphological and molecular data. Helminthologia. 2011;48:268–277.
Moravec F. Parasitic nematodes of freshwater fishes of Europe. Prague: Academia; 2013.
Barčák D, Oros M, Hanzelová V, Scholz T. Phenotypic plasticity in Caryophyllaeus brachycollis Janiszewska, 1953 (Cestoda: Caryophyllidea): does fish host play a role? Syst Parasitol. 2014;88:153–166. doi: 10.1007/s11230-014-9495-2. PubMed DOI
Bush AO, Lafferty KD, Lotz JM, Shostack AW. Parasitology meets ecology on its own terms: Margolis et al. revised. J Parasitol. 1997;83:575–583. doi: 10.2307/3284227. PubMed DOI
Chao A. Species estimation and applications. In: Kotz S, Balakrishnan N, Read CB, Vidakovic B, editors. Encyclopedia of Statistical Sciences. 2. New York: Wiley; 2005. pp. 7907–7916.
Colwell RK, Elsensohn JE. EstimateS turns 20: statistical estimation of species richness and shared species from samples, with non-parametric extrapolation. Ecography. 2014;37:609–613. doi: 10.1111/ecog.00814. DOI
Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica. 2001;4:1–9.
Ebert D. The effects of Daphnia parasites on host fitness. In: Ebert D, editor. Ecology, epidemiology, and evolution of parasitism in Daphnia. Bethesda: National Center for Biotechnology Information; 2005. pp. 41–48.
Johnson PT, Hoverman JT. Parasite diversity and coinfection determine pathogen infection success and host fitness. Proc Natl Acad Sci U S A. 2012;109:9006–9011. doi: 10.1073/pnas.1201790109. PubMed DOI PMC
Elton CS. The Ecology of invasions by animals and plants. London: Methuen; 1958.
De Bach P. Biological control by natural enemies. London: Cambridge University Press; 1974.
Dobson AP. Restoring island ecosystems: the potential of parasites to control introduced mammals. Conserv Biol. 1998;2:31–39. doi: 10.1111/j.1523-1739.1988.tb00333.x. DOI
Kennedy CR, Bush AO. The relationship between pattern and scale in parasite communities: a stranger in a strange land. Parasitology. 1994;109:187–196. doi: 10.1017/S0031182000076290. PubMed DOI
Rohde K. A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. Am Nat. 1979;114:648–671. doi: 10.1086/283514. DOI
Lucas MC, Batley E. Seasonal movements and behaviour of adult barbel Barbus barbus, a riverine cyprinid fish: implications for river management. J Appl Ecol. 1996;33:1345–1358. doi: 10.2307/2404775. DOI
Gandon S, Michalakis Y. Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. J Evol Biol. 2002;15:451–62. doi: 10.1046/j.1420-9101.2002.00402.x. DOI
Kaltz O, Shykoff JA. Local adaptation in host-parasite systems. Heredity. 1998;81:361–70. doi: 10.1046/j.1365-2540.1998.00435.x. DOI
Francová K, Ondračková M. Host-parasite interactions in sympatric and allopatric populations of European bitterling. Parasitol Res. 2011;109:801–808. doi: 10.1007/s00436-011-2326-3. PubMed DOI
Moravec F, Konečný R, Baska F, Rydlo M, Scholz T, Molnár K, Schiemer F. Endohelminth fauna of barbel, Barbus barbus (L.), under ecological conditions of the Danube basin in Central Europe. Prague: Academia; 1997.
Moravec F. Checklist of metazoan parasites of fishes of the Czech Republic and the Slovak Republic (1873–2000) Prague: Academia; 2001.
Molnár K, Eszterbauer E, Marton S, Székely C, Eiras JC. Comparison of the Myxobolus fauna of common barbel from Hungary and Iberian barbel from Portugal. Dis Aquat Organ. 2012;100:231–248. doi: 10.3354/dao02469. PubMed DOI
Guttiérrez-Galindo JF, Lacasa-Millán MI, Castellá-Espuny J, Muñoz-López E. Helminths of Barbus meridionalis meridionalis Risso, 1826 in northeastern Spain. Acta Parasitol. 1995;40:140–141.
Ergens R. A survey of the results of studies on Gyrodactylus katharineri Malmberg, 1964 (Gyrodactylidae: Monogenea) Folia Parasitol. 1983;30:319–327. PubMed
Gelnar M, Sebelova S, Dusek L, Koubkova B, Jurajda P, Zahradkova S. Biodiversity of parasites in freshwater environment in relation to pollution. Parassitologia. 1997;39:189–199. PubMed
Angelescu N. Contribution to the knowledge of the parasitofauna of the Danube fishes from the reservoir of Iron Gates. Trav Mus Nat His Nat Gr Antipa. 1974;XV:13–22.
Le Brun N, Renaud F, Berrebi P, Lambert A. Hybrid zones and host-parasite relationships: effect on the evolution of parasitic specificity. Evolution. 1992;46:56–61. doi: 10.2307/2409804. PubMed DOI
Matejusová I, Koubková B, Gelnar M, Cunningham CO. Paradiplozoon homoion Bychowsky & Nagibina, 1959 versus P. gracile Reichenbach-Klinke, 1961 (Monogenea): two species or phenotypic plasticity? Syst Parasitol. 2002;53:39–47. doi: 10.1023/A:1019945921143. PubMed DOI
Mastisky SE, Veres JK. Field evidence for parasite spillback caused by exotic mollusc Dreissena polymorpha in an invaded lake. Parasitol Res. 2010;106:667–675. doi: 10.1007/s00436-010-1730-4. PubMed DOI
Šimková A, Navrátilová P, Dávidová M, Ondračková M, Sinama M, Chappaz R, Gilles A, Costedoat C. Does invasive Chondrostoma nasus shift the parasite community structure of endemic Parachondrostoma toxostoma in sympatric zones? Parasit Vectors. 2012;5:200. doi: 10.1186/1756-3305-5-200. PubMed DOI PMC
Moulia C, Le Brun N, Loubes C, Marin R, Renaud F. Hybrid vigor in parasites of interspecific crosses between two mice species. Heredity. 1995;74:48–52. doi: 10.1038/hdy.1995.6. PubMed DOI
Philippart JC, Berrebi P. Experimental hybridization of Barbus barbus and Barbus meridionalis: physiological, morphological, and genetic aspects. Aquat Living Resour. 1990;3:325–332. doi: 10.1051/alr:1990033. DOI
Boots M, Roberts KE. Maternal effects in disease resistance: poor maternal environment increases offspring resistance to an insect virus. Proc R Soc Lond B Biol Sci. 2012;279:4009–4014. doi: 10.1098/rspb.2012.1073. PubMed DOI PMC
Mitchell SE, Rogers ES, Little TJ, Read AF. Host‐parasite and genotype‐by‐environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution. 2005;59:70–80. doi: 10.1111/j.0014-3820.2005.tb00895.x. PubMed DOI
Grech K, Watt K, Read AF. Host-parasite interactions for virulence and resistance in a malaria model system. J Evol Biol. 2006;19:1620–30. doi: 10.1111/j.1420-9101.2006.01116.x. PubMed DOI
Wolinska J, Keller B, Manca M, Spaak P. Parasite survey of a Daphnia hybrid complex: host-specificity and environment determine infection. J Anim Ecol. 2007;76:191–200. doi: 10.1111/j.1365-2656.2006.01177.x. PubMed DOI
Sures B, Streit B. Eel parasite diversity and intermediate host abundance in the River Rhine, Germany. Parasitology. 2001;123:185–191. PubMed