Pentastomid, Raillietiella mottae Almeida, Freire and Lopes, 2008,
infecting lizards in an area of caatinga, northeast, Brazil
                          Almeida, WO.a*, Santana, GG.b, Vieira, WLS.b, Wanderley, IC.b,
                                      Freire, EMX.c and Vasconcellos, A.c
                    Departamento de Ciências Físicas e Biológicas, Universidade Regional do Cariri – URCA,
                    a
                               Rua Cel. Antônio Luiz, 1161, CEP 63105-000, Crato, CE, Brazil
           Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Laboratório Coleção de Herpetologia,
           b
                Departamento de Sistemática e Ecologia, Centro de Ciências Exatas e da Natureza – CCEN,
                                  Campus I, Universidade Federal da Paraíba – UFPB,
                             Cidade Universitária, CEP 58059-900, João Pessoa, PB, Brazil
                c
                    Campus Universitário Lagoa Nova, Universidade Federal do Rio Grande do Norte – UFRN,
                                             CEP 59072-970, Natal, RN, Brazil
                                                   *e-mail: walmeida@urca.br
                        Received October 13, 2006 – Accepted February 27, 2007 – Distributed May 31, 2008
                                                         (With 1 figure)
Abstract
Pentastomids can infect the respiratory tract of lizards, causing their death and as a result influencing the population
size of hosts. Despite this, studies on rates of pulmonary infection of Brazilian lizards, including those living in
Caatinga ecosystems of northeastern Brazil are scarce. Active collections of lizards were performed from October to
December 2004 in an area of Caatinga of the Estação Experimental de São João do Cariri − EESJC (07° 25’ S and
36° 30’ W), located in the state of Paraíba, Northeast of Brazil. Forty-five lizards inhabiting granite outcrops in an
area of Caatinga were captured, belonging to the following species: Tropidurus hispidus (Spix, 1825) (18 individuals),
T. semitaeniatus (Spix, 1825) (15 individuals), Phyllopezus periosus Rodrigues, 1986 (6 individuals), and P. pollicaris
(Spix, 1825) (6 individuals). Laboratory examination revealed that all species had some degree of pulmonary infection
caused by Raillietiella mottae. The highest rates of prevalence (66.7%) and mean intensity of infection (5.25 ± 2.01,
range of 2-11) were observed in P. periosus. The results obtained in this study show that lizards of the Brazilian semi-
arid region are infected by a generalist species of pentastomid. The most likely cause for such pattern is the similarity
in lizards’ diets (ants and termites). It is particularly noteworthy that T. semitaeniatus, P. periosus, and P. pollicaris
represent new host records for R. mottae.
Keywords: Raillietiella, Pentastomida, Tropiduridae, Gekkonidae, neotropical region.
       Infecção por Pentastomida, Raillietiella mottae Almeida, Freire and Lopes, 2008,
                  em lagartos de uma área de caatinga, nordeste do Brasil
Resumo
Pentastomídeos podem infectar o trato respiratório e até levar lagartos à morte e, por isso, exercem influência sobre o
tamanho populacional de seus hospedeiros. Apesar disso, existem muito poucos trabalhos sobre as taxas de infecção
pulmonar de lagartos brasileiros, sobretudo na região nordeste. Entre outubro e dezembro de 2004 foram realizadas
coletas ativas em uma área de Caatinga localizada na Estação Experimental de São João do Cariri − EESJC (07° 25’ S e
36° 30’ W), localizada no estado da Paraíba, nordeste do Brasil. Quarenta e cinco lagartos foram capturados habitando
afloramentos de granito (lajeiros): Tropidurus hispidus (18 indivíduos), T. semitaeniatus (15 indivíduos), Phyllopezus
periosus (6 indivíduos) e P. pollicaris (6 indivíduos). Após o exame laboratorial ficou demonstrado que todas as es-
pécies possuíam algum grau de infecção pulmonar causado por Raillietiella mottae. As maiores taxas de prevalência
(66,7%) e intensidade média de infecção (5,25 ± 2,01, range 2-11) foram encontradas em P. periosus. Os resultados
demonstram que a espécie de pentastomídeo que infecta lagartos é generalista e a sobreposição da dieta dos lagartos
(formigas e térmites) aparentemente deve ser a fonte de infecção. Tropidurus semitaeniatus, P. periosus e P. pollicaris
representam são registrados como novos hospedeiros para R. mottae.
Palavras-chave: Raillietiella, Pentastomida, Tropiduridae, Gekkonidae, região neotropical.
Braz. J. Biol., 68(2): 427-431, 2008                                                                                         427
                                                            Almeida, WO. et al.
      1. Introduction                                                   shots and through manual collection, from October to
                                                                        December 2004. The outcrops, locally known as ‘la-
           Brazil still holds one of the most significant bio-
                                                                        jeiros’, are situated in the Estação Experimental de São
      logical diversities in the world, with a herpetofauna
                                                                        João do Cariri − EESJC (07° 25’ S and 36° 30’ W), in the
      represented by a great number of species described
                                                                        state of Paraíba, Northeast Brazil. The area where the an-
      (Rodrigues, 2005). A rich fauna of endoparasites is as-
                                                                        imals were captured is characterized by xerophytic veg-
      sociated to reptiles, but much of the published work on
                                                                        etation, with thorny shrubs, stunted trees with entwined
      these animals is mostly descriptive (Vicente et al., 1993;
                                                                        branches, having high density of cacti and bromeliads
      Rocha et al., 2000). Studies on community variables, like
                                                                        (Mélo and Bandeira, 2004; Andrade et al., 2005). It is
      abundance, prevalence, and mean intensity of infection
                                                                        situated in the semi-arid region of Paraíba, characterized
      have only recently been published (Ribas et al., 1995;
                                                                        temperatures ranging between 28 and 35 °C on average
      1998; Rocha, 1995; Vrcibradic et al., 1999; Vrcibradic
                                                                        and annual mean rainfall of 387 mm. The rainfall concen-
      et  al., 2000; Vrcibradic et al., 2002a; 2002b; Rocha
                                                                        trates from February to April. During drier years the dry
      et  al., 2003; Rocha and Vrcibradic, 2003; Dias et al.,
                                                                        period lasts over eight months (Núcleo de Meteorologia
      2005; Anjos et al., 2005).
                                                                        Aplicada, 1987).
           Pentastomids are essentially parasites of reptiles’
                                                                             Upon collection, the lizards were frozen-euthanized
      respiratory tract (Riley, 1986). In Brazil, except from
                                                                        and their snout-vent length (SVL) measured with a ruler
      one review and a few phylogenetic studies (Rego, 1984;
                                                                        (to the nearest 1 mm). They were then fixed in formalin
      Almeida and Christoffersen, 1999; 2002), research on
                                                                        10% and preserved in ethanol 70%.
      these animals has been restricted to their occurrence
                                                                             The respiratory tracts of the lizards were removed
      and descriptions of new species (Motta, 1963a, b; Motta
                                                                        and the search for pentastomids was carried out under
      and Gomes, 1968; Rego, 1983; 1984; Almeida et al.,
                                                                        a stereomicroscope. The pentastomids collected were
      2006a,b; Almeida et al. 2008b; Rocha and Vrcibradic,
                                                                        cleared in Hoyer’s medium, temporarily slide-mounted
      2003; Dias et al., 2005; Anjos et al., 2005). Also, only          and preserved in ethanol 70%. Identification was per-
      the pentastomid species Raillietiella freitasi (Motta and         formed based on dimensions of the hooks and copu-
      Gomes, 1968) was described as parasitizing the lungs of           latory spiculae of males, with the aid of a microscope
      Mabuya punctata (Spix, 1825), a lizard of the Fernando            with a micrometric eyepiece (see Ali et al., 1984; 1985;
      de Noronha Island (Motta and Gomes, 1968).                        Almeida et al., 2008b).
           Recent publications have included evaluations on in-              Each specimen was compared with vouchers of
      fection rates, prevalence, and mean intensity of infection        Raillietiella freitasi (Motta and Gomes, 1968) numbers
      in studies of snakes, amphisbaenians and lizards of the           20420, 20421, 20429, 20431, 20432, 20434, 20439,
      northeastern region of Brazil (Dias et al., 2005; Almeida         30325a-c, 30326, 30327, 30328, 30329a-c, 30330a-b
      et al., 2006a; Almeida et al. 2006b; Almeida et al. 2007;         provided by the Helminthological Collection of the
      Almeida et al. 2008a; Almeida et al. 2008b; Anjos et al.,         Oswaldo Cruz Institute (CHIOC). After identification
      2008), nevertheless, only four lizard species were inves-        the material was deposited in the Zoological Collection
      tigated. Dias et al. (2005) reported a likely new species of      of the Universidade Regional do Cariri (LZ-URCA) and
      Raillietiella aff. furcocerca (Diesing, 1863) infecting the       labelled as Raillietiella mottae numbers 201-212. The
      lungs of two whiptail lizard species, Cnemidophorus aba-          eco-parasitological terms used in this study followed
      etensis Dias, Rocha and Vrcibradic, 2002 and C. ocellifer        Bush et al. (1997).
      (Spix, 1825) in a restinga habitat in the state of Bahia.
      Almeida et al. (2008b) investigated infection caused by R.
                                                                        3. Results
      mottae in the lungs of Tropidurus hispidus (Spix, 1825) liv-
      ing in the semi-arid region of Cariri, state of Ceará, north-          Forty-five lizards were captured, being 18 individ-
      eastern Brazil. Anjos et al. (2008) reported Hemidactylus         uals of the species T. hispidus, 15 of T. semitaeniatus
      mabouia (Moreau de Jonnès, 1818), a dwelling’s invader            (Spix, 1825), 6  of P. periosus Rodrigues, 1986 , and
      gecko in the Cariri region (municipality of Barbalha, Ceará       6  of P. pollicaris. All species had their lungs infected
      state), as a new host of R. mottae. The authors reported in       by only one species of pentastomid, R. mottae (Table 1;
      their work, the first occurrence in Brazil of R. frenatus Ali,    Figure 1). The highest rates of prevalence and mean in-
      Riley and Self, 1981 parasitizing H. mabouia.                    tensity of infection were found in P. periosus.
           In the present study we evaluate infections caused
      by pentastomids in an assemblage of lizards living in an          4. Discussion
      area of Caatinga. It is specifically addressed here i) the
      composition of pentastomid fauna and ii) rates of infec-              Almeida et al. (2008b), using data from literature
      tion (prevalence and intensity).                                  reports, emphasized the possibility of specificity of
                                                                        R. mottae parasitizing T. hispidus, which had not yet
                                                                        been recorded as a host of any species of pentastomid.
      2. Material and Methods
                                                                        Almeida et al. (2008b) stated that together with morpho-
          Diurnal and nocturnal active lizards living on gran-          logical evidence, such evaluation would reinforce the
      ite outcrops in the Caatinga were captured using sling-           proposition for the existence of a new species. However,
428                                                                                              Braz. J. Biol., 68(2): 427-431, 2008
                                                  Pentastomid infection in lizards
Table 1. Epidemiological data of lizards (sample size in parentheses) and their respective pentastomid infection in an area
of Caatinga, State of Paraíba. For each host species (overall and by species) it is shown the mean snout-vent length (SVL)
(range in mm), prevalence (in absolute values and proportions), and intensity of infection (mean ± one standard deviation,
with range in parentheses).
        Host species (n)                     Mean SVL                   Weight           Prevalence Mean intensity
                                                (mm)                      (g)               (%)          (range)
Phyllopezus periosus (6)               89.30 ± 8.50 (54-114)   20.03 ± 4.64 (3.30-36.13)  4 (66.7)  5.25 ± 2.01 (2-11)
Phyllopezus pollicaris (6)             70.22 ± 2.87 (61-75.80) 8.24 ± 1.06 (4.99-10.87)   1 (16.6)          5.0
Tropidurus hispidus (18)               77.04 ± 4.21 (32-112)   20.68 ± 3.27 (5.51-54.70)  2 (11.1)          1.0
Tropidurus semitaeniatus (15)          60.79 ± 3.12 (38.6-82)   6.28 ± 1.01 (1.25-14.20)  2 (13.3)    4.0 ± 3.0 (1-7)
                                                                    ing, so searchers should be generalists, a similar condi-
                                                                    tion to the one of birds reported by Begon et al. (2006).
                                                                    Lizards would have an overall profitability maximized
                                                                    by a broader diet, constituted by minute insects thriv-
                                                                    ing on outcrops of the Caatinga. Tropidurus hispidus and
                                                                    T. semitaeniatus are diurnal predators while P. periosus
                                                                    and P. pollicaris are nocturnal predators. Both groups
                                                                    (tropidurid and geckonid) feed on ants and termites that
                                                                    are abundant on Caatinga outcrops, as we could ob-
                                                                    serve in situ, and they are likely intermediate hosts of
                                                                    R. mottae.
                                                                         Among the prevalences found in the present study,
                                                                    the one of T. hispidus (11.1%) is identical to prevalence
                                                                    value obtained by Almeida et al. (2008b). All other liz-
                                                                    ards investigated here showed a range of 13.3-16.6%,
                                                                    close to prevalence values of T. hispidus, except the
                                                                    prevalence of P. periosus that showed a value of 66.7%.
                                                                    Other results reported on pulmonary infection by pentas-
                                                                    tomids in lizards showed prevalence values lower than
                                                                    those obtained here, namely: Mabuya agilis Raddi, 1823
                                                                    (3.6-9.0%) (Vrcibradic et  al., 2002b), Cnemidophorus
                                                                    abaetensis (6.0%) (Dias et al., 2005), C. ocellifer (2.5%)
                                                                    (Dias et al., 2005), and H. mabouia (9.1%) (Anjos et al.,
         0.4 mm                                                     2008).
                                                                         Differing values of rates of infection intensity were
Figure 1. Raillietiella mottae: detail of the cephalothorax         also obtained here. The lowest value was observed in
male (LZ-URCA nº 0207) viewed ventrally with sharply tip            T. hispidus (1.0). This value however, is close to the ones
pointed hooks and copulatory spiculae with tips curved or
                                                                    reported for pentastomids in lizards of other Brazilian
“C-shaped” knob-like projection base.
                                                                    ecosystems, namely: M. agilis (1.0), C. ocellifer (1.0)
                                                                    and H. mabouia (1.8 ± 1.4) (Vrcibradic et al., 2002b;
                                                                    Dias et al., 2005; Anjos et al., 2008). However, such
data obtained by Almeida et al. (2006a; 2008a; 2008b) in-
                                                                    values differed from those reported by Almeida et al.
dicates that two species of pentastomids, Cephalobaena
                                                                    (2008b) for infection intensity of R. mottae in T. hispidus
tetrapoda Heymons, 1922 and Raillietiella furcocerca,
                                                                    (6.0 ± 1.4, range 5-7).
should be generalists because of their recorded variety                  Rates of infection intensity obtained here for
of hosts. Anjos et al. (2008) reported only one female of           T. semitaeniatus (4.0 ± 3.0, range 1-7) and P. pollicaris
gecko, H. mabouia, parasitized by R. mottae. This isolat-           (5.0) and also the value of 4.5 obtained for C. abaetensis
ed case reported by these above-mentioned authors could             by Dias et al. (2005) are similar to values obtained by
have resulted from the low sampling they performed.                 Almeida et al. (2008b).
    The results obtained in the present study suggest that               The higher values of mean rates of infection record-
R. mottae is a generalist parasite and does not have any            ed for R. mottae refer to P. periosus, which had mean
reptile specificity, at least with respect to the lizard spe-       rate of infection of 5.25 (± 2.01, range 2-11). According
cies investigated. All lizards studied are insectivores and         to Riley et al. (1991), burdens of 9-20 worms per host
foragers, and therefore, could be deemed as predators               frequently killed geckos.
with short handling times when compared to their search                  Despite all these discrepancies, it is important to
times. Searching is always moderately time consum-                  emphasize that similarity and difference in rates of in-
Braz. J. Biol., 68(2): 427-431, 2008                                                                                              429
                                                                 Almeida, WO. et al.
      fection intensity may result from stochastic events and                Northeastern Brazil. Braz. J. Biol. = Rev. Bras. Biol., vol. 68,
      vary according to sample size and specific environmental               no. 1, p. 193-197.
      characteristics from the studied areas. Therefore, it must             ALMEIDA, WO., FREIRE, EMX. and LOPES, SG., 2008b.
      be emphasized the need for further studies on patterns of              A new species of Pentastomida infecting Tropidurus hispidus
      pulmonary infection by pentastomids in lizards, in the                 (Squamata: Tropiduridae) from caatinga in Northeastern Brazil.
      neotropical region.                                                    Braz. J. Biol. = Rev. Bras. Biol., vol. 68, no. 1, p. 199-203.
      Acknowledgements — Our thanks to D. Noronha, curator of                ANDRADE, LA., PEREIRA, IM., LEITE, UT. and BARBOSA,
      the Helminthological Collection of the Instituto Oswaldo Cruz,         MRV., 2005. Análise da cobertura de duas fitofisionomias de
      for the loan of pentastomid specimens; to FUNCAP – the                 caatinga, com diferentes históricos de uso, no município de
      Fundação Cearense de Apoio ao Desenvolvimento Científico e             São João do Cariri, Estado da Paraíba. Cerne, vol. 11, no. 3,
      Tecnológico (Ref. 943/03 – Edital 003/03) for the research grant       p. 253‑262.
      to W. O. Almeida; to the Conselho Nacional de Desenvolvimento
                                                                             ANJOS, LA., ALMEIDA, WO., VASCONCELLOS, A.,
      Científico e Tecnológico (CNPq) for the research grant received
                                                                             FREIRE, EMX. and ROCHA, CFD., 2008. Pentastomids
      through the Programa Ecológico de Longa Duração (PELD); to
                                                                             infecting an invader lizard, Hemidactylus mabouia (Gekkonidae)
      the Fundação Coordenação de Aperfeiçoamento de Pessoal de
                                                                             in Northeastern Brazil. Braz. J. Biol. = Rev. Bras. Biol., vol. 68,
      Nível Superior (CAPES) for the scholarship to G. G. Santana.
                                                                             no. 4. [in press].
      We also thank the Brazilian Institute for the Environment and
      Natural Resources (IBAMA) for permission to collect samples            ANJOS, L., ROCHA CFD., VRCIBRADIC, D. and VICENTE,
      from protected areas (Documents nr 02021.000075/2006-7 and             JJ., 2005. Helminths of exotic lizard Hemidactylus mabouia
      080/04 – RAN/ IBAMA 02007.001009/04-73); to B. Grisi for               from a rock outcrop area in southeastern Brazil. J. Helmint.,
      the suggestions and the English version of the manuscript; to E.       vol. 79, no. 4, p. 307-313.
      Medeiros (UEPB) for revising the English version of the text;
      and to two anonymous reviewers for their valuable suggestions          BEGON, M., TOWNSEND, CR. and HARPER, JL., 2006.
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Braz. J. Biol., 68(2): 427-431, 2008                                                                                                        431