Abstract
Trophic networks can have architectonic configurations influenced by historical and ecological factors. The objective of this study was to analyze the architecture of networks between lizards, their endoparasites, diet, and micro-habitat, aiming to understand which factors exert an influence on the composition of the species of parasites. All networks showed a compartmentalized pattern. There was a positive relation between diet and the diversity of endoparasites. Our analyses also demonstrated that phylogeny and the use of micro-habitat influenced the composition of species of endoparasites and diet pattern of lizards. The principal factor that explained the modularity of the network was the foraging strategy, with segregation between the “active foragers” and “sit-and-wait” lizards. Our analyses also demonstrated that historical (phylogeny) and ecological factors (use of micro-habitat by the lizards) influenced the composition of parasite communities. These results corroborate other studies with ectoparasites, which indicate phylogeny and micro-habitat as determinants in the composition of parasitic fauna. The influence of phylogeny can be the result of coevolution between parasites and lizards in the Caatinga, and the influence of micro-habitat should be a result of adaptations of species of parasites to occupy the same categories of micro-habitats as hosts, thus favoring contagion.
Similar content being viewed by others
References
Allesina S, Pascual M (2007) Network structure, predator–prey modules, and stability in large food webs. Theor Ecol 1:55–64
Andrade-Lima D (1981) The Caatingas dominium. Rev Bras Bot 4:149–153
Bascompte J (2010) Structure and dynamics of ecological networks. Science 329:765–766
Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci U S A 100:9383–9387
Brooks DR, León-Règagnon V, McLennan DA, Zelmer D (2006) Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87:76–85
Brose U, Jonsson T, Berlow EL, Warren P, Banasek-Richter C, Bersier LF, Blanchard JL, Brey T, Carpenter SR, Blandenier MFC, Cushing L, Dawah HA, Dell T, Edwards F, Harper-Smith S, Jacob U, Ledger ME, Martinez ND, Memmott J, Mintenbeck K, Pinnegar JK, Rall BC, Rayner TS, Reuman DC, Ruess L, Ulrich W, Williams RJ, Woodward G, Cohen JE (2006) Consumer–resource body-size relationships in natural food webs. Ecology 87:2411–2417
Bush AO, Lafferty KD, Lotz JM, Shostaki AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583
Cattin MF, Bersier LF, Banašek-Richter C, Baltensperger R, Gabriel JP (2004) Phylogenetic constraints and adaptation explain food-web structure. Nature 427:835–839
Chen HW, Liu WC, Davis AJ, Jordán F, Hwang MJ, Shao KT (2008) Network position of hosts in food webs and their parasite diversity. Oikos 117:1847–1855
Clayton DH, Bush SE, Johnson KP (2004) Ecology of congruence: past meets present. Syst Biol 53:165–173
Cohen JE, Jonsson T, Müller CB, Godfray HCJ, Savage VM (2005) Body sizes of hosts and parasitoids in individual feeding relationships. Proc Natl Acad Sci U S A 102:684–689
Dormann CF, Gruber B, Frund (2008) The bipartite package, version 0.5. R Project for Statistical Computing, Vienna, Austria
Fletcher RJ, Revell A, Reichert BE, Kitchens WM, Dixon JD, Austin JD (2013) Network modularity reveals critical scales for connectivity in ecology and evolution. Nat Commun 4:1–7
Gamble T, Colli GR, Rodrigues MT, Werneck FP, Simons AM (2011) Phylogeny and cryptic diversity in geckos (Phyllopezus; Phyllodactylidae; Gekkota) from South America’s open biomes. Mol Phylogenet Evol 62:943–953
Genini J, Côrtes MC, Guimarães PR Jr, Galetti M (2011) Mistletoes play different roles in a modular host–parasite network. Biotropica 44:171–178
Giannini NP (2003) Canonical phylogenetic ordination. Syst Biol 52:684–695
Giugliano LG, Collevatti RG, Colli GR (2007) Molecular dating and phylogenetic relationships among Teiidae (Squamata) inferred by molecular and morphological data. Mol Phylogenet Evol 45:168–179
Gotelli NJ and Entsminger GL (2001) EcoSim: null models software for ecology. Version 7.44. Acquired Intelligence Inc. & Kesey Bear. Available from the Internet URL http://homepages.together.net/~gentsmin/ecosim.htm
Graham SP, Hassan HK, Burkett-Cadena ND, Guyer C, Unnasch TR (2009) Nestedness of ectoparasite-vertebrate host networks. Plos One 4:e7873
Guimarães PR Jr, Rico-Gray V, Dos Reis SF, Thompson JN (2006) Asymmetries in specialization in ant–plant mutualistic networks. Proc R Soc B 273:2041–2047
Ings TC, Montoya JM, Bascompte J, Blüthgen N, Brown L, Dormann CF, Edwards F, Figueroa D, Jacob U, Jones JI (2009) Review: ecological networks–beyond food webs. J Anim Ecol 78:253–269
Kerr GD, Bull CM (2006) Interactions between climate, host refuge use, and tick population dynamics. Parasitol Res 99:214–222
Krasnov BR, Fortuna MA, Mouillot D, Khokhlova IS, Shenbrot GI, Poulin R (2012) Phylogenetic signal in module composition and species connectivity in compartmentalized host-parasite networks. Am Nat 179:501–511
Krause AE, Frank KA, Mason DM, Ulanowicz RE, Taylor WW (2003) Compartments revealed in food-web structure. Nature 426:282–285
Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. P Natl Acad Sci-Biol 103:11211–11216
Leu ST, Kappeler PM, Bull CM (2010) Refuge sharing network predicts ectoparasite load in a lizard. Behav Ecol Sociobiol 64:1495–1503
Lewinsohn TM, Prado PI, Jordano P, Bascompte J, Olesen JM (2006) Structure in plant–animal interaction assemblages. Oikos 113:174–184
Lima DP Jr, Giacomini HC, Takemoto RM, Agostinho AA, Bini LM (2012) Patterns of interactions of a large fish–parasite network in a tropical floodplain. J Anim Ecol 81:905–913
Marcogliese DJ (2002) Food webs and the transmission of parasites to marine fish. Parasitology 124:83–99
Martin JE, Llorente GA, Roca V, Carretero MA, Montori A, Santos X, Romeu R (2005) Relationship between diet and helminths in Gallotia caesaris (Sauria: Lacertidae). Zoology 108:121–130
McLaughlin RL (1989) Search modes of birds and lizards—evidence for alternative movement patterns. Am Nat 133:654–670
Morand S (2000) Wormy world: comparative tests of theoretical hypotheses on parasite species richness. In: Poulin R, Morand S, Skorping A (eds) Evolutionary Biology of host-parasite relationships: theory meets reality. Elsevier, Amsterdam, pp 63–79
Newman MEJ (2004) Fast algorithm for detecting community structure in networks. Phy Rev E 69:066133
Olesen JM, Jordano P (2002) Geographic patterns in plant-pollinator mutualistic networks. Ecology 83:2416–2424
Pascual M, Dunne JA (2006) Ecological networks: linking structure to dynamics in food webs. Oxford University Press, USA
Pedersen AB, Fenton A (2007) Emphasizing the ecology in parasite community ecology. Trends Ecol Evol 22:133–139
Perry G (1999) The evolution of search modes: ecological versus phylogenetic perspectives. Am Nat 153:98–109
Pianka ER (1973) The structure of lizard communities. Annu Rev Ecol Syst 4:53–74
Pimm SL, Lawton JH (1980) Are food webs divided into compartments? J Anim Ecol 49:879–898
Pough FH, Janis CM, Heiser JB (2003) A vida dos vertebrados. Editora Ateneu, São Paulo
Price PW (1980) Evolutionary biology of parasites. Princeton University Press, Princeton
R (2012) A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria
Rezende EL, Albert EM, Fortuna MA, Bascompte J (2009) Compartments in a marine food web associated with phylogeny, body mass, and habitat structure. Ecol Lett 12:779–788
Sites JW Jr, Reeder TW, Wiens JJ (2011) Phylogenetic insights on evolutionary novelties in lizards and snakes: sex, birth, bodies, niches, and venom. Annu Rev Ecol Evol Syst 11:227–244
Teng J, McCann KS (2004) Dynamics of compartmented and reticulate food webs in relation to energetic flows. Am Nat 164:85–100
Ter Braak CJF, Smilauer P (1998) CANOCO reference manual and user’s guide to Canoco for windows: software for canonical community ordination (version 4.5) Cajo JF ter Braak and Petr Smilauer. Centre for Biometry
Thébault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–856
Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445:202–205
Van Valen L (1973) A new evolutionary law. Evol Theor 1:1–30
Vázquez DP, Aizen MA (2004) Asymmetric specialization: a pervasive feature of plant-pollinator interactions. Ecology 85:1251–1257
Vázquez DP, Poulin R, Krasnov BR, Shenbrot GI (2005) Species abundance and the distribution of specialization in host–parasite interaction networks. J Anim Ecol 74:946–955
Velloso AL, Sampaio EVSB, Giulietti AM, Barbosa MRV, Castro AAJF, Queiroz LP, Fernandes A, Oren DC, Cestaro LA, Carvalho AJE, Pareyn FGC, Silva FBR, Miranda EE, Keel S, and Gondim RS (2001) Ecorregiões: propostas para o bioma caatinga; resultados do seminário de planejamento ecorregional da caatinga. Page 76 in Seminário de Planejamento Ecorregional da Caatinga. TNC/APNE Recife, Aldeia-Pernambuco
Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM (1993) Nematóides do Brasil. Parte III: Nematóides de Répteis. Rev Bras Zool 10:19–168
Vitt LJ (1991) An introduction to the ecology of Cerrado lizards. J Herpetol 25:79–90
Vitt LJ (1995) The ecology of tropical lizards in the Caatinga of Northeast Brazil. Occas pap Okla Mus nat hist 1:1–29
Vitt LJ, Carvalho CM (1995) Niche partitioning in a tropical wet season: lizards in the lavrado area of northern Brazil. Copeia 2:305–329
Wiens JJ, Hutter CR, Mulcahy DG, Noonan BP, Townsend TM, Sites JW Jr, Reeder TW (2012) Resolving the phylogeny of lizards and snakes (Squamata) with extensive sampling of genes and species. Biol Lett 1:1–4
Winemiller KO (1990) Spatial and temporal variation in tropical fish trophic networks. Ecol Monogr 60:331–367
Woodward G, Ebenman B, Emmerson ME, Montoya JM, Olesen JM, Valido A, Warren PH (2005) Body size in ecological networks. Trends Ecol Evol 20:402–409
Acknowledgments
This work was supported by a Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico–FUNCAP postdoctoral fellowship to SVB and FSF, a research fellowship from–CNPq to AV and WOA, and a Universal CNPq fellowship to DOM. Instituto Brasileiro de Meio Ambiente e Recursos Naturais Renováveis–IBAMA provided the license to capture lizards. Dr. A. Leyva helped with the English translation and editing of the manuscript. DOM thanks the University of Texas and Eric Pianka for providing conditions to finalize this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Brito, S.V., Corso, G., Almeida, A.M. et al. Phylogeny and micro-habitats utilized by lizards determine the composition of their endoparasites in the semiarid Caatinga of Northeast Brazil. Parasitol Res 113, 3963–3972 (2014). https://doi.org/10.1007/s00436-014-4061-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-014-4061-z