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Ecological release in lizard endoparasites from the Atlantic Forest, northeast of the Neotropical Region

Published online by Cambridge University Press:  22 January 2020

Adonias A. Martins Teixeira Open the ORCID record for Adonias A. Martins Teixeira [Opens in a new window] ,
Pablo Riul ,
Samuel Vieira Brito ,
João A. Araujo-Filho ,
Diêgo Alves Teles ,
Waltécio de Oliveira Almeida  and
Daniel Oliveira Mesquita
Adonias A. Martins Teixeira*
Affiliation:
Departamento de Sistemática e Ecologia, Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, Campus I, CEP 58059-900, João Pessoa, PB, Brazil
Pablo Riul
Affiliation:
Departamento de Sistemática e Ecologia, Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, Campus I, CEP 58059-900, João Pessoa, PB, Brazil
Samuel Vieira Brito
Affiliation:
Centro de Ciências Agrárias e Ambientais, Universidade Federal do Maranhão, BR-222, Km 04, S/N, Boa Vista, CEP 65500-000, Chapadinha, MA, Brazil
João A. Araujo-Filho
Affiliation:
Departamento de Sistemática e Ecologia, Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, Campus I, CEP 58059-900, João Pessoa, PB, Brazil
Diêgo Alves Teles
Affiliation:
Departamento de Sistemática e Ecologia, Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, Campus I, CEP 58059-900, João Pessoa, PB, Brazil
Waltécio de Oliveira Almeida
Affiliation:
Departamento de Ciências Biológicas, Universidade Regional do Cariri, Rua Cel. Antônio Luiz, 1161, Campus Pimenta, CEP 63105-000, Crato, CE, Brazil
Daniel Oliveira Mesquita
Affiliation:
Departamento de Sistemática e Ecologia, Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, Campus I, CEP 58059-900, João Pessoa, PB, Brazil
*
Author for correspondence: Adonias A. Martins Teixeira, E-mail: [email protected]
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Abstract

We compared lizard endoparasite assemblages between the Atlantic Forest and naturally isolated forest enclaves to test the ecological release hypothesis, which predicts that host specificity should be lower (large niche breadth) and parasite abundance should be greater for parasites from isolated forest enclaves (poor assemblages) than for parasites from the coastal Atlantic Forest (rich assemblages). Parasite richness per specimen showed no difference between the isolated and non-isolated areas. Parasite abundance did not differ between the isolated and non-isolated areas but showed a positive relationship with parasite richness considering all areas (isolated and non-isolated). Furthermore, host specificity was positively related to parasite richness. Considering that host specificity is inversely proportional to the host range infected by a parasite, our results indicate that in assemblages with greater parasite richness, parasites tend to infect a smaller range of hosts than do those in simple assemblages. In summary, our study partially supports the ecological release hypothesis: in assemblages with greater parasite richness, lizard parasites from Atlantic Forest are able to increase their parasite abundance (per host), possibly through facilitated infection; however, the amplitude of infected hosts only expands in poor assemblages (lower parasite richness).

Keywords

Density compensationecological opportunitiesfacilitated infectionhost specificityniche expansion
Type
Research Article
Information
Parasitology , Volume 147 , Issue 4 , April 2020 , pp. 491 - 500
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Adamson, ML and Noble, S (1992) Structure of the pinworm (Oxyurida: Nematoda) guild in the hindgut of the American cockroach, Periplaneta americana. Parasitology 104, 497–507.CrossRefGoogle ScholarPubMed
Adamson, ML and Caira, JN (1994) Evolutionary factors influencing the nature of parasite specificity. Parasitology 109, S85–S95.CrossRefGoogle ScholarPubMed
Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the Nematode Parasites of Vertebrates: Archival Volume. London, UK: CABI.CrossRefGoogle Scholar
Andrade-Lima, D (1960) Estudos fitogeográficos de Pernambuco. Arquivo do Instituto de Pesquisas Agronômicas de Pernambuco 5, 305–341.Google Scholar
Andrade-Lima, D (1982) Present day forest refuges in Northeastern Brazil. In Prance, GT (ed.), Biological Diversification in the Tropics. New York, USA: Columbia University Press, pp. 245–254.Google Scholar
Apanius, V, Yorinks, N, Bermingham, E and Ricklefs, RE (2000) Island and taxon effects in parasitism and resistance of Lesser Antillean birds. Ecology 81, 1959–1969.CrossRefGoogle Scholar
Araújo, FS, Gomes, VS, Silveira, AP, Figueiredo, MA, Oliveira, RS, Bruno, MMA, Lima-Verde, LW, Silva, EF, Otutumi, AT and Ribeiro, KA (2007) Efeito da variação topo climática e estrutura da vegetação da serra de Baturité, Ceará. In Oliveira, TS and Araújo, FS (eds), Diversidade e Conservação da Biota da Serra de Baturité, Ceará. Fortaleza, Brazil: Edições UFC, pp. 139–162.Google Scholar
Bates, D, Mächler, M, Bolker, BM and Walker, SC (2014) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Bellocq, GJ, Morand, S and Feliu, C (2002) Patterns of parasite species richness of Western Palaeartic micro-mammals: island effects. Ecography 25, 173–183.CrossRefGoogle Scholar
Blondel, J (2000) Evolution and ecology of birds on islands: trends and prospects. Vie et Milieu 50, 205–220.Google Scholar
Bolker, BM, Brooks, ME, Clark, CJ, Geange, SW, Poulsen, JR, Stevens, MHH and White, J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127–135.CrossRefGoogle ScholarPubMed
Brunet, AK and Medellín, RA (2001) The species–area relationship in bat assemblages of tropical caves. Journal of Mammalogy 82, 1114–1122.2.0.CO;2>CrossRefGoogle Scholar
Bush, AO and Holmes, JC (1986) Intestinal helminths of lesser scaup ducks: an interactive community. Canadian Journal of Zoology 64, 142–152.CrossRefGoogle Scholar
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis, et al. Revisited. The Journal of Parasitology 83, 575–583.CrossRefGoogle ScholarPubMed
Carnaval, AC and Bates, JM (2007) Amphibian DNA shows marked genetic structure and tracks Pleistocene climate change in northeastern Brazil. Evolution 61, 2942–2957.CrossRefGoogle ScholarPubMed
Case, TJ (1975) Species numbers, density compensation, and colonizing ability of lizards on islands in the Gulf of California. Ecology 56, 3–18.CrossRefGoogle Scholar
Cavalcanti, D and Tabarelli, M (2004) Distribuição das plantas amazônico-nordestinas no centro de endemismo Pernambuco: brejos de altitude vs. florestas de terras baixas. In Pôrto, KC, Cabral, JJP and Tabarelli, M (eds), Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Brasília, DF, Brasil: Ministério do Meio Ambiente, pp. 285–296.Google Scholar
Crowell, KL (1962) Reduced interspecific competition among the birds of Bermuda. Ecology 43, 75–88.CrossRefGoogle Scholar
Des Roches, S, Robertson, JM, Harmon, LJ and Rosenblum, EB (2011) Ecological release in White Sands lizards. Ecology and Evolution 1, 571–578.CrossRefGoogle Scholar
Dobson, AP and Pacala, SW (1992) The parasites of Anolis lizards the northern lesser Antilles. II. the structure of the parasite community. Oecologia 91, 118–125.CrossRefGoogle ScholarPubMed
Dobson, AP, Pacala, SV, Roughgarden, JD, Carper, ER and Harris, EA (1992) The parasites of Anolis lizards in the northern Lesser Antilles I. Patterns of distribution and abundance. Oecologia 91, 110–117.CrossRefGoogle ScholarPubMed
Eaton, JM, Larimer, SC, Howard, KG, Powell, R and Parmerlee, JS (2002) Population densities and ecological release of the solitary lizard Anolis gingivinus in Anguilla, West Indies. Caribbean Journal of Science 38, 27–36.Google Scholar
Ehrlich, PR and Raven, PH (1964) Butterflies and plants: a study in coevolution. Evolution 18, 586–608.CrossRefGoogle Scholar
Emlen, JT (1979) Land bird densities on Baja California islands. The Auk 96, 152–167.Google Scholar
Faeth, SH (1984) Density compensation in vertebrates and invertebrates: a review and an experiment. In Strong, JDR, Simberloff, D, Abele, LG and Thistle, AB (eds), Ecological Communities: Conceptual Issues and the Evidence. Princeton, New Jersey, USA: Princeton University Press, pp. 491–509.Google Scholar
Fromont, E, Morvilliers, L, Artois, M and Pontier, D (2001) Parasite richness and abundance in insular and mainland feral cats: insularity or density? Parasitology 123, 143–151.CrossRefGoogle ScholarPubMed
Gregory, GG and Munday, BL (1976) Internal parasites of feral cats from the Tasmanian Midlands and King Island. Australian Veterinary Journal 52, 317–320.CrossRefGoogle ScholarPubMed
Hart, SP and Marshall, DJ (2013) Environmental stress, facilitation, competition, and coexistence. Ecology 94, 2719–2731.CrossRefGoogle ScholarPubMed
Hechinger, RF and Lafferty, KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society of London B: Biological Sciences 272, 1059–1066.Google ScholarPubMed
Holmes, JC (1973) Site selection by parasitic helminths: interspecific interactions, site segregation, and their importance to the development of helminth communities. Canadian Journal of Zoology 51, 333–347.CrossRefGoogle ScholarPubMed
Holmes, JC and Price, PW (1986) Communities of parasites. In Anderson, DJ and Kikkawa, J (eds), Community Ecology: Pattern and Process. Oxford, UK: Blackwell Scientific Publications, pp. 187–213.Google Scholar
Kennedy, CR (1978) The parasite fauna of resident char Salvelinus alpinus from Arctic islands, with special reference to Bear Island. Journal of Fish Biology 13, 457–466.CrossRefGoogle Scholar
Kennedy, CR (1990) Helminth communities in freshwater fish: structured communities or stochastic assemblages? In Esch, GW, Bush, AO and Aho, J (eds), Parasite Communities: Patterns and Processes. London, England: Chapman & Hall, pp. 131–156.CrossRefGoogle Scholar
Kennedy, CR, Laffoley, DDA, Bishop, G, Jones, P and Taylor, M (1986) Communities of parasites of freshwater fish of Jersey, Channel Islands. Journal of Fish Biology 29, 215–226.CrossRefGoogle Scholar
Kodric-Brown, A and Brown, JH (1993) Highly structured fish communities in Australian desert springs. Ecology 74, 1847–1855.CrossRefGoogle Scholar
Krasnov, BR, Khokhlova, IS, Oguzoglu, I and Burdelova, NV (2002) Host discrimination by two desert fleas using an odour cue. Animal Behaviour 64, 33–40.CrossRefGoogle Scholar
Kuris, AM, Blaustein, AR and Alio, JJ (1980) Hosts as islands. The American Naturalist 116, 570–586.CrossRefGoogle Scholar
Lewis, JW (1968a) Studies on the helminth parasites of the long-tailed field mouse, Apodemus sylvaticus sylvaticus from Wales. Journal of Zoology 154, 287–312.CrossRefGoogle Scholar
Lewis, JW (1968b) Studies on the helminth parasites of voles and shrews from Wales. Journal of Zoology 154, 313–331.CrossRefGoogle Scholar
Löfgren, A and Jerling, L (2002) Species richness, extinction and immigration rates of vascular plants on islands in the Stockholm Archipelago, Sweden, during a century of ceasing management. Folia Geobotanica 37, 297–308.CrossRefGoogle Scholar
Losos, JB (1994) Historical contingency and lizard community ecology. In Vitt, LJ and Pianka, ER (eds), Lizard Ecology: Historical and Experimental Perspectives. Princeton, USA: Princeton University Press, pp. 319–333.Google Scholar
Losos, JB and Queiroz, K (1997) Evolutionary consequences of ecological release in Caribbean Anolis lizards. Biological Journal of the Linnean Society 61, 459–483.Google Scholar
MacArthur, RH and Wilson, EO (1967) The Theory of Island Biogeography. Princeton, USA: Princeton University Press.Google Scholar
MacArthur, RH, Diamond, JM and Karr, JR (1972) Density compensation in island faunas. Ecology 53, 330–342.CrossRefGoogle Scholar
Mesquita, DO, Colli, GR and Vitt, LJ (2007) Ecological release in lizard assemblages of neotropical savannas. Oecologia 153, 185–195.CrossRefGoogle ScholarPubMed
Muylaert, RL, Vancine, MH, Bernardo, R, Oshima, JEF, Sobral-Souza, T, Tonetti, VR, Niebuhr, BB and Ribeiro, MC (2018) A note on the territorial limits of the Atlantic Forest. Oecologia Australis 22, 302–311.CrossRefGoogle Scholar
Novosolov, M, Raia, P and Meiri, S (2013) The island syndrome in lizards. Global Ecology and Biogeography 22, 184–191.CrossRefGoogle Scholar
Oliveira, BHS, Teixeira, AAM, Queiroz, RNM, Araujo Filho, JA, Teles, DA, Brito, SV and Mesquita, DO (2017) Nematodes infecting Anotosaura Vanzolinia (Squamata: Gymnophthalmidae) from Caatinga, northeastern Brazil. Acta Herpetologica 12, 103–108.Google Scholar
Pafilis, P, Foufopoulos, J, Sagonas, K, Runemark, A, Svensson, E and Valakos, ED (2011) Reproductive biology of insular reptiles: marine subsidies modulate expression of the “Island Syndrome”. Copeia 2011, 545–552.CrossRefGoogle Scholar
Pianka, ER (1994) Evolutionary Ecology, 5th Edn. New York, USA: HarperCollins Publishers.Google Scholar
Poulin, R (1997) Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28, 341–358.CrossRefGoogle Scholar
Poulin, R (2007) Evolutionary Ecology of Parasites. Princeton, New Jersey: Princeton University Press.CrossRefGoogle Scholar
Poulin, R and Mouillot, D (2003) Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126, 473–480.CrossRefGoogle ScholarPubMed
Poulin, R and Mouillot, D (2004) The relationship between specialization and local abundance: the case of helminth parasites of birds. Oecologia 140, 372–378.CrossRefGoogle Scholar
Poulin, R and Mouillot, D (2005) Combining phylogenetic and ecological information into a new index of host specificity. The Journal of Parasitology 91, 511–514.CrossRefGoogle ScholarPubMed
Prance, GT (1987) Biogeography of neotropical plants. In Whitmore, TC and Prance, GT (eds), Biogeography and Quaternary History in Tropical America. Oxford: Clarendon Press, pp. 46–65.Google Scholar
Price, PW (1977) General concepts on the evolutionary biology of parasites. Evolution 31, 405–420.CrossRefGoogle ScholarPubMed
Ricklefs, RE and Miller, GL (1999) Ecology, 4th Edn. New York, USA: W.H. Freeman Publishers.Google Scholar
Rocha, CFD and Vrcibradic, D (2003) Nematode assemblages of some insular and continental lizard hosts of the genus Mabuya Fitzinger (Reptilia, Scincidae) along the eastern Brazilian coast. Revista Brasileira de Zoologia 20, 755–759.CrossRefGoogle Scholar
Santos, AMM, Cavalcanti, DR, Silva, JMC and Tabarelli, M (2007) Biogeographical relationships among tropical forests in north-eastern Brazil. Journal of Biogeography 34, 437–446.CrossRefGoogle Scholar
Silva, RJ, Ferreira, VL and Strüssmann, C (2007) New species of Haplometroides (Digenea: Plagiorchiidae) from Phalotris nasutus (Gomes, 1915) (Serpentes, Colubridae). Journal of Parasitology 93, 917–921.CrossRefGoogle Scholar
Smith, CC and Fretwell, SD (1974) The optimal balance between size and number of offspring. The American Naturalist 108, 499–506.CrossRefGoogle Scholar
Tabarelli, M and Santos, AMM (2004) Uma breve descrição sobre a história natural dos brejos nordestinos. In Pôrto, KC, Cabral, JJP and Tabarelli, M (eds), Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Brasília, DF, Brasil: Ministério do Meio Ambiente, pp. 17–24.Google Scholar
Veloso, HP, Rangel-Filho, ALR and Lima, JCA (1991) Classificação da Vegetação Brasileira, Adaptada a um Sistema Universal. Rio de Janeiro, Brasil: IBGE.Google Scholar
Wilson, K and Grenfell, BT (1997) Generalized linear modelling for parasitologists. Parasitology Today 13, 33–38.CrossRefGoogle ScholarPubMed
Wootten, R (1973) The metazoan parasite-fauna of fish from Hanningfield Reservoir, Essex in relation to features of the habitat and host populations. Journal of Zoology 171, 323–331.CrossRefGoogle Scholar
Yoder, JB, Clancey, E, Des Roches, S, Eastman, JM, Gentry, L, Godsoe, W, Hagey, TJ, Jochimsen, D, Oswald, BP and Robertson, J (2010) Ecological opportunity and the origin of adaptive radiations. Journal of Evolutionary Biology 23, 1581–1596.CrossRefGoogle ScholarPubMed