Helminths infecting Dryadosaura nordestina (Squamata: Gymnophthalmidae) from Atlantic Forest, northeastern Brazil

Open access

Abstract

We analyzed the patterns of infection by helminths in populations of the Gymnophthalmidae lizard Dryadosaura nordestina from three Atlantic Forest fragments in Northeast Brazil. Prevalence and mean intensity of infection by location showed the following results: ARIE Mata de Goiamunduba (60.8 % and 10.4 ± 8), RPPN Engenho Gargaú (83.3 % and 20.8 ± 19.7) and Benjamim Maranhão Botanical Garden (70.4 % and 7.78 ± 5.8). We provide the first records of helminth infection for the lizard D. nordestina, in which three species of nematodes, Aplectana sp., Cosmocerca sp. and Physaloptera lutzi and one trematode Haplometroides odhneri were recovered. Trematodes of the genus Haplometroides were previously known as parasites only in snake and amphisbaenian hosts in South America. Now, our study provides the first record of a species belonging to this genus parasitizing lizards. In conclusion, our study shows that D. nordestina have a depleted helminth fauna (three species at maximum), similar to other studies with lizards of this family in Brazil and that its parasite abundance is related to host snout-vent length, but not to the sex.

Amorim, D.M., Silva, L.A.F., Morais, D.H., Silva, R.J., Ávila, R.W. (2017): Aplectana Nordestina N. Sp. (Nematoda: Cosmocercidae) Parasitizing Leposternon Polystegum (Squamata: Amphisbaenidae) From Northeastern, Brazil. Zootaxa, 4247, 83 - 88. Doi: 10.11646/Zootaxa.4247.1.12

Anderson, R.C . (2000): Nematode Parasites Of Vertebrates: Their Development And Transmission, 2nd Edition Edn. New York, Cabi Publishing, 650pp.

Anderson, R.C ., Chabaud, A.G., Willmott, S. (2009): Keys To The Nematode Parasites Of Vertebrates: Archival Volume, Cabi.

Anjos, L.A., Ávila, R.W., Ribeiro, S.C., Almeida, W.O., Silva, R.J. (2012): Gastrointestinal Nematodes Of The Lizard Tropidurus Hispidus (Squamata: Tropiduridae) From A Semi-Arid Region Of Northeastern Brazil. J. Helminthol., 81, 443 - 449. Doi: 10.1017/S0022149x12000491

Araujo Filho, J.A., Ribeiro, S.C., Brito, S.V., Teles, D.A., Sousa, J.G.G., Ávila, R.W., Almeida, W.O. (2014): Parasitic Nematodes Of Polychrus Acutirostris (Polychrotidae) In The Caatinga Biome, Northeastern Brazil. Braz. J. Biol., 74, 939 - 942. Doi: 10.1590/1519-6984.01313

Ávila, R.W., Anjos, L.A., Gonçalves, U., Freire, E.M.X., Almeida, W.O., Silva, R.J. (2010a): Nematode Infection In The Lizard Bogertia Lutzae (Loveridge, 1941) From The Atlantic Forest In North-Eastern Brazil. J. Helminthol., 84, 199 - 201. Doi: 0.1017/S0022149x09990538

Ávila, R.W., Silva, R.J. (2010): Checklist Of Helminths From Lizards And Amphisbaenians (Reptilia, Squamata) Of South America. J. Venom. Anim. Toxins. Incl. Trop. Dis., 16, 543 - 572. Doi: 10.1590/S1678-91992010000400005

Ávila, R.W., Silva, R.J. (2011): Helminths Of Lizards (Reptilia: Squamata) From Mato Grosso State, Brazil. Comp. Parasitol., 78, 129- 139. Doi: 10.1654/4473.1

Ávila, R.W., Souza, F.L., Silva, R.J. (2010b): Helminths From Seven Species Of Lizards (Reptilia: Squamata) At The Cerrado Of Mato Grosso Do Sul State, Brazil. Comp. Parasitol., 77, 67 - 71. Doi: 10.1654/4414.1

Barton, K. (2009): Mumin: Multi-Model Inference. R Package Version 1. 0. 0. Http://R-Forge.R-Project.Org/Projects/Mumin.

Bates, D., Mächler, M., Bolker, B.M., Walker, S.C. (2014): Fitting Linear Mixed-Effects Models Using Lme4. J. Stat. Softw., 67, 1 - 48.Doi: 10.18637/Jss.V067.I01

Brito, S.V., Corso, G., Almeida, A.M., Ferreira, F.S., Almeida, W.O., Anjos, L.A., Mesquita, D.O., Vasconcellos, A. (2014): 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. Doi: 10.1007/S00436-014-4061-Z

Bursey, C.R., Goldberg, S.R. (2004): Cosmocerca Vrcibradici N. Sp.(Ascaridida: Cosmocercidae), Oswaldocruzia Vitti N. Sp.(Strongylida: Molineoidae), And Other Helminths From Prionodactylus Eigenmanni And Prionodactylus Oshaughnessyi (Sauria: Gymnophthalmidae) From Brazil And Ecuador. J. Parasitol., 90, 140 - 145. Doi: 10.1645/Ge-3234

Bursey, C.R., Goldberg, S.R., Telford, S.R. (2006): New Species Of Aplectana (Nematoda: Cosmocercidae) And Mesocoelium Monas (Digenea: Brachycoeliidae) In Lepidophyma Fl Avimaculatum (Squamata: Xantusiidae) From Costa Rica. Caribb. J. Sci., 42, 164 - 170

Bush, A.O., L Afferty, K.D., Lotz, J.M., Shostak, A.W. (1997): Parasitology Meets Ecology On Its Own Terms: Margolis Et Al. Revisited. J. Parasitol., 83, 575 - 583. Doi: 10.2307/3284227

Dias, S.C., C Andido, D.M., Brescovit, A.D. (2006): Scorpions From Mata Do Buraquinho, João Pessoa, Paraíba, Brazil, With Ecologi Cal Notes On A Population Of Ananteris Mauryi Lourenço (Scorpiones, Buthidae). Rev. Bras. Zool., 23, 707 - 710. Doi: 10.1590/ S0101-81752006000300014

Everhart, B.A . (1957): Notes On The Helminths Of Pseudemys Scripta Elegans (Wied, 1838) In Areas Of Texas And Oklahoma. Proc. Okla. Acad. Sci., 38 - 43

Freeland, W.J ., Boulton, W.J. (1992): Coevolution Of Food Webs: Parasites, Predators And Plant Secondary Compounds. Biotropica, 24, 309 - 327. Doi: 10.2307/2388525

Garda, A.A., Medeiros, P.H.S., Lion, M.B., Brito, M.R.M., Vieira, G.H.C., Mesquita, D.O. (2014): Autoecology Of Dryadosaura Nordestina (Squamata: Gymnophthalmidae) From Atlantic Forest Fragments In Northeastern Brazil. Zoologia (Curitiba), 31, 418 - 425. Doi: 10.1590/S1984-46702014000500002

Nascimento, M .G., Munoz, G., Marquet, P.A., Poulin, R. (2004): Testing The Energetic Equivalence Rule With Helminth Endoparasites Of Vertebrates. Ecol. Lett., 7, 527 - 531. Doi: 10.1111/J.1461-0248.2004.00609.X

Goldberg, S.R ., Bursey, C., Vitt, L.J. (2007a): Parasite Communities Of Two Lizard Species, Alopoglossus Angulatus And Alopoglossus Atriventris, From Brazil And Ecuador. Herpetol. J., 17, 269 - 272

Goldberg, S.R ., Bursey, C.R., Caldwell, J.P., Vitt, L.J., Costa, G.C. (2007b): Gastrointestinal Helminths From Six Species Of Frogs And Three Species Of Lizards, Sympatric In Pará State, Brazil. Comp. Parasitol., 74, 327 - 342. Doi: 10.1654/4268.1

Gomez, M.D.P. , González, C.E., Sanabria, E.A. (2017): A New Species Of Aplectana (Nematoda: Cosmocercidae) Parasite Of Pleurodema Nebulosum (Anura: Leptodactylidae) From The Monte Desert, Argentina, With A Key To Neotropical Species Of The Genus Aplectana. Zootaxa, 4247, 121 - 130. Doi: 10.11646/Zootaxa.4247.2.3

Grizante, M.B ., Brandt, R., Kohlsdorf, T. (2012): Evolution Of Body Elongation In Gymnophthalmid Lizards: Relationships With Climate. Plos One, 7, E49772. Doi: 10.1371/Journal.Pone.0049772

Kuris, A.M., Blaustein, A.R., Alio, J.J. (1980): Hosts As Islands. Am. Nat., 116, 570 - 586

Lafferty, K.D ., Kuris, A.M. (2005): Parasitism And Environmental Disturbances. In: Thomas, F., Renaud, F., Guégan, J.F. (Eds) Parasitism And Ecosystems. New York, Usa, Oxford University Press.

Lima, V.F., B Rito, S.V., Araujo Filho, J.A., Teles, D.A., Ribeiro, S.C., Teixeira, A.A.M., Pereira, A.M.A., Almeida, W.O. (2017): Helminth Parasites Of Phyllodactylidae And Gekkonidae Lizards In A Caatinga Ecological Station, Northeastern Brazil. Biota Neotrop., 17, 1- 7. Doi: E20160263, 2017

Lyles, A.M., Dobson, A.P. (1993): Infectious Disease And Intensive Management: Population Dynamics, Threatened Hosts, And Their Parasites. J. Zoo Wildl. Med., 24, 315 - 326

Marcogliese, D.J. (2004): Parasites: Small Players With Crucial Roles In The Ecological Theater. Ecohealth, 1, 151 - 164. Doi: 10.1007/S10393-004-0028-3

Neta, A.F.S., Ávila, R.W. (2018) Helminths Of The Lizard Colobosauroides Cearensis (Squamata, G Ymnophthalmidae) In An Area Of Caatinga, Northeastern Brazil. Acta Herpetol, 13, 29 - 34

Oliveira, B.H .S., Pessanha, A.L.M. (2013): Microhabitat Use And Diet Of Anotosaura Vanzolinia (Squamata: Gymnophthalmidae) In A Caatinga Area, Brazil. Biota Neotrop., 13, 193 - 198. Doi: 10.1590/S1676-06032013000300022

Oliveira, B.H .S., Teixeira, A.A.M., Queiroz, R.N.M., Araujo Filho, J.A., Teles, D.A., Brito, S.V., Mesquita, D.O. (2017): Nematodes Infecting Anotosaura Vanzolinia (Squamata: Gymnophthalmidae) From Caatinga, Northeastern Brazil. Acta Herpetol., 12, 103 - 108. Doi: 10.13128/Acta_Herpetol-18765

Oliveira, B.H .S., Queiroz, R.N.M., Cavalcanti, L.B.Q., Mesquita, D.O. (2018): Autecology Of Neotropical Lizard Species Anotosaura Vanzolinia (Squamata, Gymnophthalmidae) In A Caatinga Region, North-Eastern Brazil. Herpetol. J., 28, 19 - 26

Pimm, S.L., R Aven, P. (2000): Biodiversity: Extinction By Numbers. Nature, 403, 843 - 845. Doi: 10.1038/35002708

Pinto, L.P., Bedê, L., Paese, A., Fonseca, M., Paglia, A., Lamas, I. (2006): Mata Atlântica Brasileira: Os Desafi Os Para Conservação Da Biodiversidade De Um Hotspot Mundial. In: Rocha, C.F.D., Bergallo, H.G., Alves, M.A.S. (Eds) Biologia Da Conservação: Essências. São Carlos, São Paulo, Brasil, Rima

Poulin, R. (1 998): Large-Scale Patterns Of Host Use By Parasites Of Freshwater Fi Shes. Ecol. Lett., 1, 118 - 128

Poulin, R. (2 007): Evolutionary Ecology Of Parasites. Princeton, New Jersey, Princeton University Press R Development Core Team (2013): R. A Language And Environment For Statistical Computing. R Foundation For Statistical Computing, Vienna, Austria

Ribas, S.C., Rocha, C.F.D., Teixeira-Filho, P.F., Vicente, J.J. (1995): Helminths (Nematoda) Of The Lizard Cnemidophorus Ocellifer (Sauria: Teiidae): Assessing The Effect Of Rainfall, Body Size And Sex In The Nematode Infection Rates. Cienc. Cult. (São Paulo), 47, 88 - 91

Ribas, S.C., Rocha, C.F.D., Teixeira-Filho, P.F., Vicente, J.J. (1998): Nematode Infection In Two Sympatric Lizards (Tropidurus Torquatus And Ameiva Ameiva) With Different Foraging Tactics. Amphib. Reptil., 19, 323 - 330

Ribeiro, L.B., Ferreira, A.C.S., Silva, D.C.N., Vieira, F.M., Moura, G.J.B. (2018): Helminth Parasites Of The Lizard Nothobachia Ablephara (Gymnophthalmidae) In Caatinga Areas From The Sertão Of Brazil. J. Parasitol., 104, 177 - 182. Doi: 10.1645/17-90.

Rocha, C.F.D. (1995): Nematode Parasites Of The Brazilian Sand Lizard, Liolaemus Lutzae. Amphib. Reptil., 16, 412 - 415

Rocha, C.F.D. , Bergallo, H.G., Van Sluys, M., Alves, M.A.S., Jenkins, C. (2006): Corredores Ecolégicos E Conservação Da Biodiversidade: Um Estudo De Caso Na Mata Atlantica. In: Rocha, C.F.D., Bergallo, H.G., Alves, M.A.S. (Eds) Biologia Da Conservação. Essências. São Carlos, São Paulo, Brasil, Rima.

Rocha, C.F.D., Vrcibradic, D., Vicente, J.J., Cunha-Barros, M. (2003): Helminths Infecting Mabuya Dorsivittata (Lacertilia, Scincidae) From A High-Altitude Habitat In Itatiaia National Park, Rio De Janeiro State, Southeastern Brazil. Braz. J. Biol., 63, 129 - 132. Doi: 10.1590/S1519-69842003000100017

Santos, K.R., Barrella, T.H., Zica, E.O.P., Silva, R.J. (2008): New Reports On Parasitism By Haplometroides Buccicola (Digenea, Plagiorchiidae) In Brazilian Snak. J. Venom. Anim. Toxins. Incl. Trop. Dis., 14 (3), 527 - 532. Doi: 10.1590/S1678-9199200800030001

Silva, R.J., Béda, A.F., Ferreira, V.L. (2008): New Record Of Haplometroides Intercaecalis (Digenea, Plagiorchiidae) Infecting A Brazilian Snake. J. Venom. Anim. Toxins. Incl. Trop. Dis., 14, 161- 165. Doi: 10.1590/S1678-91992008000100013

Silva, R.J., Andrade, P.A., Monteiro E Silva, H.A., Rossellini, M., Barrella, T.H. (2005a): Report On The Occurrence Of Haplometroides Buccicola (Trematoda, Digenea, Plagiorchiidae) Infecting Phalotris Lativittatus (Serpentes, Colubridae) In Brazil. J. Venom. Anim. Toxins. Incl. Trop. Dis., 11, 373 - 379. Doi: 10.1590/S1678-91992005000300013

Silva, R.J., Barrella, T.H. (2002): Micrurus Frontalis As A New Host Recorded For Haplometroides Odhneri (Trematoda, Digenea, Plagiorchiidae). Rev. Bras. Parasitol. Vet., 11, 47 - 48

Silva, R.J., Ferreira, V.L., Strüssmann, C. (2007): New Species Of Haplometroides (Digenea: Plagiorchiidae) From Phalotris Nasutus (Gomes, 1915) (Serpentes, Colubridae). J. Parasitol., 93, 917 -921. Doi: 10.1645/Ge-1123r.1

Silva, R.J., Zica, E.O.P., Cruz, M., O’reilly, J.C., Costa, M.C. (2005b): Occurrence Of Haplometroides Odhneri (Trematoda, Digenea, Plagiorchiidae) Infecting Leptotyphlops Koppesi (Serpentes, Leptotyphlopidae). Arq. Bras. Med. Vet. Zootec., 57, 267- 269. Doi: 10.1590/S0102-09352005000800021

Sousa, J.G.G. , Brito, S.V., Ávila, R.W., Teles, D.A., Araujo-Filho, J.A., Teixeira, A.A.M., Anjos, L.A., Almeida, W.O. (2014): Helminths And Pentastomida Of Two Synanthropic Gecko Lizards, Hemidactylus Mabouia And Phyllopezus Pollicaris, In An Urban Area In Northeastern Brazil. Braz. J. Biol., 74, 943 - 948. Doi: 10.1590/1519-6984.01413

Teixeira, A.A .M., Brito, S.V., Teles, D.A., Ribeiro, S.C., Araujo-Filho, J.A., Lima, V.F., Pereira, A.M.A., Almeida, W.O. (2017): Helminths Of The Lizard Salvator Merianae (Squamata, Teiidae) In The Caatinga, Northeastern Brazil. Braz. J. Biol., 77, 312 - 317. Doi: 10.1590/1519-6984.13515

Teles, D.A., Brito, S.V., Teixeira, A.A.M., Ribeiro, S.C., Araujo Filho, J.A., Lima, V.F., Pereira, A.M.A., Almeida, W.O. (2017): Nematodes Associated With Iguana Iguana (Linnaeus, 1758) (Squamata, Iguanidae) In Semi-Arid Areas Of Northeastern Brazil. Braz. J. Biol., 77, 514 - 518. Doi: 10.1590/1519-6984.17615

Wilson, K., Grenfell, B.T. (1997): Generalized Linear Modelling For Parasitologists. Parasitol. Today., 13, 33 - 38. Doi: 10.1016/S0169-4758(96)40009-6.

Journal Information


IMPACT FACTOR 2017: 0.417
5-year IMPACT FACTOR: 0.619

CiteScore 2016: 0.58

SCImago Journal Rank (SJR) 2015: 0.316
Source Normalized Impact per Paper (SNIP) 2015: 0.678

Target Group researchers in the field of human, veterinary medicine and natural science

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 189 189 15
PDF Downloads 125 125 12