Pterygosomatidae and Trombiculidae mites infesting Tropidurus hispidus (Spix, 1825) (Tropiduridae) lizards in northeastern Brazil/Acaros Pterygosomatidae e Trombiculidae infestando lagartos Tropidurus hispidus (Spix, 1825) (Tropiduridae) no nordeste do Brasil.
Lizards and parasitic mites demonstrate ancient relationships, so much so that some lizards have developed skin folds (through independent phylogenetic events) that form structures known as "mite-pockets" in different regions of their bodies where mites tend to aggregate (Rodrigues, 1987; Bauer, 1990, 1993). Arnold (1986) argued that the development of these "mite pockets" acts as an adaptation to limit the distribution of trombiculidae ectoparasites on their bodies and thus reduce their damage. However, scansorial mites such as Geckobiella spp. (as well as other pterygosomatids) are not usually found in mite-pockets (Bauer, 1990, 1993; Bertrand and Modry, 2004).
Among the parasitic mites found on lizards, the family Pterygosomatidae comprises nine genera, only one of which has to date been found on lizards (Pimeliaphilus) (Bertrand and Modry, 2004). Geckobiella texana (Banks, 1904) has herpetological importance among the pterygosomatid ectoparasites since it is a vector of the protozoarian Schellackia occidentalis Bonorris and Ball, 1955, found in the intestines and blood tissue of lizards (Bonorris and Ball, 1955). Trombiculidae represents one of the most widely distributed families in the Neotropical Region (Zippel et al., 1996, Daniel and Stekolnikov, 2004; Klukoswski, 2004), presenting interactions mainly of Eutrombicula alfreddugesi (Oudemans, 1910) with a few other lizard species. In Brazil, the larvae of this chigger mite have been reported as ectoparasites on lizards in 'restinga' (sandy coastal) vegetation formations (Cunha-Barros and Rocha, 1995, 2000; Cunha-Barros et al., 2003), on tropidurid lizards from 'cerrado' (savanna) vegetation regions (Carvalho et al., 2006), and in the ecotone between the 'caatinga' (dry thorny shrub/stunted trees) and 'campos rupestres' (higher altitude rocky field) habitats (Rocha et al., 2008). Chiggers (the larvae of the Trombiculidae) are important pests on some groups of reptiles and cause dermatitis, blood loss, and are vectors of infectious diseases (Frye, 1991).
Price (1980) argued that vacant niches still exist for parasites and that niches of coexisting parasites are mostly non-overlapping. For an arthropod ectoparasite, for example, the host surface constitutes its habitat, and its mode of occupation will depend on intrinsic and extrinsic factors acting at that environment scale (Marshall, 1981; Bittencourt and Rocha, 2002). In some cases, different ectoparasite species can share different portions of the surface body of a host, with parasite species presenting different niche width and overlap in microhabitats of host body surface (Bittencourt and Rocha, 2003).
We investigated the infestation patterns (prevalence and intensity; sensu Bush et al., 1997) of the mites Geckobiella sp. and Eutrombicula alfreddugesi on the lizard Tropidurus hispidus in a mountainous region of Chapada do Araripe, Brazil, to evaluate which microhabitats were occupied and to what extent are there spatial niche overlaps between these mite species. Additionally we evaluated the relationship between i) host body size and ii) host sex with infestation rates.
2. Material and Methods
Field work was carried out on the lower slopes of the Chapada do Araripe Mountains (07[degrees]16' S and 39[degrees]26' W) within the Chapada do Araripe Environmental Protection Area, in the municipality of Crato, Ceara State, Brazil. The regional vegetation there is a mosaic of palm trees and montane and secondary forests. The area has experienced anthropogenic alterations resulting from agricultural use, the harvesting of natural products, and land development. The regional climate is warm, semi-arid tropical. Mean annual temperatures range from 24[degrees] to 26[degrees]C. The rainy season extends from January to May, and the mean annual rainfall is 1090 mm (IPECE, 2008).
Lizards were captured by hand using rubber slings or nooses. Immediately after capture, each lizard was transferred to a plastic sack containing cotton soaked in ether that anaesthetized and euthanized them. Their snout-vent lengths (SVL) were measured (to the nearest 0.05 mm) using calipers. The lizards were subsequently fixed in 10% formalin and stored in 70% alcohol.
All of the external surfaces of the lizards' bodies were carefully searched for mites using a stereomicroscope. The number and the position of the mites on the lizard bodies (mite microhabitats on host body) were recorded in order to identify and to map the specific occupied sites. The following sites were designated in this mapping analysis: Forearm (Fa), Doral Face of Head (DFH), Ventral Face of Head (VFH), Thigh (Th), Dorsal (Do), Ventral (Ve), Lateral neck pocket (Lnp), Auxiliary pocket (Pax), Inguinal Mite Pocket (Pin), Arm (Ar), Inside Elbow (IE), Inside knee (IK), Pre-Femoral Region (PFR), Leg (Lg), Dorsal Face of the Tail (DFt), Ventral Face of the Tail (VFt) (Figure 1).
The mites were collected using forceps and fine-bristle brushes and mounted on permanent slides in Hoyer medium for subsequent identification.
Statistical tests were performed utilising: the Z test for proportions (Zar, 1999) to evaluate if there were significant differences in the overall prevalence of mites on male and female lizard hosts. We also used Student t-test (Zar, 1999) to evaluate if there were significant differences in the mean infestation intensity among host sexes, and between E. alfreddugesi and Geckobiella sp.
Principal component analysis (PCA) (Jongman et al., 1995) was performed to evaluate the relationships between the mite species and their infestation sites, using the MVSP 3.1 software program (Kovach, 1999).
We used Pianka's measure of niche overlap (Pianka, 1973) to evaluate the overlap in spatial niches between the two mite species (Equation 1):
[O.sub.12] = [O.sub.21] = [n.summation over (i=1)] P2iP1i/[square root of [n.summation over (i=1)] ([P2i.sup.2])([P1i.sup.2])] (1)
where P2i and P1i are the rate of use of microhabitat type i by mite species 1 and 2 respectively. We compared the observed overlap values against a null model (1000 interactions) generated by the R3 randomization algorithm (Lawlor, 1980) using ECOSIM 7.0 software (Gotelli and Entsminger, 2001).
A total of 56 specimens of T. hispidus were collected, including 26 females (SVL 77.84 [+ or -] 2.33, 55-95 mm), 27 males (SVL 95.29 [+ or -] 2.57, 70-113 mm), and 3 juveniles (SVL 49.66 [+ or -] 0.33, 49-50 mm).
Forty lizards were infested by at least one mite species; overall prevalence was 71.4%.
Two mite species, E. alfreddugesi (Trombiculidadae) and Geckobiella sp. (Pterygosomatidae) were found.
Host females parasitised by E. alfreddugesi had a mean infestation intensity of 8.57 [+ or -] 3.62 (range 1-27). Infested host males had a mean infestation intensity of 11.90 [+ or -] 2.63 (range 1-25). Female lizards infested by Geckobiella sp. had a mean intensity of infestation of 5.91 [+ or -] 2.28, 1-25, whereas males had a mean infestation intensity of 5.43 [+ or -] 1.52, 1-23. The three juvenile specimens were parasitised exclusively by E. alfreddugesi, and their mean infestation intensity was 8.0 [+ or -] 4.72, 1-17. Seven adult lizards were infested by eggs and immature forms of unidentified mites (mean 2.28 [+ or -] 0.89, 1-7).
There was no significant difference between the overall infection rates of adult male (70.4%) and adult female (65.4%) lizards (Z-test: zc = 1.44; p = 0.925).
The overall mean infestation intensity of adult male lizards (12.3 [+ or -] 8.4) was not significantly different from the overall mean infestation intensity of females (7.9 [+ or -] 9.2) (t-test: t = -1.62; g.l. = 35; p > 0.05).
[FIGURE 1 OMITTED]
The mean intensity rate of infestation by E. alfreddugesi (10.2 [+ or -] 8.7) was significantly higher than that by Geckobiella sp. (5.9 [+ or -] 6.8) (t-test: t = -1.94; g.l. = 47; p < 0.05).
The first two axes of the PCA explained 99.9% of the observed variance (Table 1). Axis 1 ordered the mite species principally in regards to their abundance in mite-pockets (Lnp) and in auxiliary-pockets (Pax) in the direction of positive values (Table 2, Figure 2). Axis 2 ordered the mite species principally in relation to their abundance on abdomen (Ab), thigh (Th), and leg (Pr) sites, with positive values (Table 2, Figure 2).
[FIGURE 2 OMITTED]
The spatial niche overlap between E. alfreddugesi and Geckobiella sp. was [O.sub.12] = [O.sub.21] = 0.197. This value did not differ significantly from that generated by null models (RA3; 1000 iterations; [O.sub.12] = [O.sub.21] = 0.248; p = 0.50).
The ectoparasite species E. alfreddugesi has been found in all studies of mite infestations on lizards in Brazil, and their infestation rates have varied from 5.0% (in Ameiva ameiva) to 100% (in Tropidurus cocorobensis, T. erythrocephalus, and T. hispidus) (Cunha-Barros and Rocha, 2000; Rocha et al., 2008) (Table 3). The total infestation prevalence by E. alfreddugesi among the specimens analysed here was 32.14% (n = 18), which was significantly lower than rates reported in earlier studies of tropidurids infected by E. alfreddugesi, as for example T. torquatus (n = 146) from an area of restinga (sandy coastal) vegetation in Marica, Rio de Janeiro State, with 97% prevalence (Cunha-Barros and Rocha, 2000); or T. cocorobensis (n = 16), T. erythrocephalus (n = 13), T. hispidus (n = 20), and T. semitaeniatus (n = 33) from an area of caatinga (dryland) vegetation in Morro do Chapeu, Bahia State, with prevalences ranging from 97-100% (Rocha et al., 2008); or Tropidurus itambere (n = 74) with a prevalence rate of 88.2%, T. oreadicus (n = 85) with 87.6% and T. torquatus (n = 16) with 65.2% in the Brazilian cerrado (savanna) (Carvalho et al., 2006). The present reported prevalence rate is only slightly higher than the lowest rate of 17.3% reported for T. torquatus (n = 13) (Carvalho et al., 2006).
The total mean infestation intensity by E. alfreddugesi (9.27 [+ or -] 1.83, 1-25) was comparatively low when compared to the mean infestation intensity of 164.9 [+ or -] 161.9 reported for T. torquatus (Cunha-Barros and Rocha, 2000), or 36.67 [+ or -] 41.09 reported for T. itambere (Carvalho et al., 2006).
The presence of Geckobiella sp. represents the first report of this parasite using T. hispidus as a host in northeastern Brazil. The infestation rate of this parasite in the present study (prevalence 50%, and mean intensity of infestation of 5.64 [+ or -] 1.28, 1-25) was found to be within the range previously published for the species E. alfreddugesi (Cunha-Barros and Rocha, 1995, 2000; Cunha-Barros et al., 2003; Carvalho et al., 2006; Rocha et al., 2008).
Our data showed that mean intensity rate infestation by E. alfreddugesi by Geckobiella sp. differed consistently. These differences may arise when some species are favoured in the occupation of particular mocrohabitats in the body of a host. In some cases the host body surface may be occupied by a considerable number of parasites but they differ greatly in infestation rates due to the particular specificity to some microhabitats (Bittencourt and Rocha, 2003).
Data indicated that adults of the sexes did not differ regarding the overall infection rates and the mean intensities of infestation. These results probably are due to the low selectivity of their parasites (Carvalho et al., 2006).
The sites most infested by E. alfreddugesi in the present study were the mite pockets, as was also found in T. hispidus in areas in Bahia state (Rocha et al., 2008). These pockets offer protection from mechanical shocks and from dehydration and may act to isolate the mites (Cunha-Barros and Rocha, 2000; Cunha-Barros et al., 2003; Garcia-de-la-Pena et al., 2004). Additionally, once the mites are established in these pockets they cannot be easily removed (Carvalho et al., 2006). However, in addition to the mite pockets, skin wrinkles (especially those found on the neck and inguinal regions) were the most highly infested sites in T. itambere, T. oreadicus and T. torquatus from the Cerrado (Carvalho et al., 2006); skin wrinkles were the preferred micro-habitats for mites among lizards captured in the restinga region at Marica, perhaps because these animals have imbricate scales that also facilitate mite feeding and protection (Cunha-Barros and Rocha, 2000).
Scale patterns appear to influence rates of parasitism (Cunha-Barros and Rocha, 2000), as does the presence and the morphology of the mite pockets (Carvalho et al., 2006). Additionally, tropidurids show large variation in the number of pockets found among different species (Rodrigues, 1987). Considering the fact that Tropidurus hispidus has two pockets on its neck and two more in the axilar region (Rodrigues, 1987), and according to Clopton and Gold (1993) populations of E. alfreddugesi are sensitive to environmental variations and the effects of environmental degradation, the infestation rates of these lizards would be expected to differ from those observed in the present study.
Geckobiella sp. was found to be present on every part of the body in the lizards in the present study, with no specific preferred site, reflecting the fact that these mites are pterygossomatids that live under the imbricate scales of their hosts (Bertrand et al., 1995). Studies of infestations on Tropiduridae lizards undertaken in Brazil have previously identified only a single parasite, the trombicuilid Eutrombicula alfreddugesi (Cunha-Barros and Rocha, 2000; Cunha-Barros et al., 2003; Carvalho et al., 2006; Rocha et al., 2008). We presented here, however, evidence for two mite species infesting the same host. But, as the two mite species occupy distinct micro-habitats on the same host they can potentially avoid mutual competition --as has been seen with some species of nematodes found in specific infection sites in the digestive tracts of the same lizard species (see Bush et al., 2001). We did not find skin lesions on any of the infested specimens or any indication that these animals were debilitated or demonstrated behavioural modifications, but additional studies will be undertaken in the near future to more closely examine these aspects.
Acknowledgements--We are grateful to the Fundacao Cearense de Apoio ao Desenvolvimento Cientifico e Tecnologico--FUNCAP for the research grant awarded to W. O. Almeida (BPI-0112-2.05/08); the Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior--CAPES for the scholarship awarded to S. C. Ribeiro; the Brazilian Institute for the Environment and Natural Resources--IBAMA for the collecting permit (process number 14100-1 and 007/2007--CGFAP/IBAMA 02007.001009/2004). A. Carvalho, M. Valim, and M. Bertrand for their help in identifying the mite species; Geraldo Saraiva and his family for the kind use of their home during the collections; Francisco Pereira-Junior for helping with the collections.
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Delfino, MMS. (a), Ribeiro, SC. (b), Furtado, IP. (a), Anjos, LA. (c) and Almeida, WO. (d) *
(a) Departamento de Ciencias Biologicas, Centro de Ciencias Biologicas e da Saude, Universidade Regional do Cariri--URCA, Campus do Pimenta, CEP 63105-000, Crato, CE, Brazil
(b) Programa de Pos-graduacao em Biologia Animal, Departamento de Zoologia, Universidade Federal do Pernambuco--UFPE, Av. Prof. Moraes Rego, 1235, CEP 50670-420, Recife, PE, Brazil
(c) Laboratorio de Parasitologia de Animais Silvestres--LAPAS, Departamento de Parasitologia, Instituto de Biociencias, Universidade Estadual Paulista--UNESP, Distrito de Rubiao Junior, s/n, CEP 18618-000, Botucatu, SP, Brazil
(d) Departamento de Quimica Biologica, Centro de Ciencias Biologicas e da Saude, Universidade Regional do Cariri--URCA, Campus do Pimenta, CEP 63105-000, Crato, CE, Brazil
* e-mail: email@example.com
Received June 4, 2010--Accepted June 28, 2010--Distributed May 31, 2011 (With 2 figures)
Table 1. Autovalues and the percentage of variance that was explained by the two principal components (axes 1 and 2) of the Principal Component Analysis (PCA) for the abundance of E. alfredugesi, Geckobiella sp., and immature mite forms at diverse infection sites on the host Tropidurus hispidus. Axis 1 Axis 2 Autovalues 13055.3 1584.7 Percentages 89.1 10.8 Accumulated percentages 89.1 99.9 Table 2. Autovectors of the two principal components (axes 1 and 2) of the Principal Component Analysis (PCA) of the abundance of E. alfredugesi, Geckobiella sp., and immature mite forms at diverse infection sites on the host Tropidurus his. The most important variables on axes 1 and 2 are indicated in bold type. LEGEND: ventral side of the head = VFH; forearm = Fa; axially-pocket = Pax; mite-pocket = Lnp; inguinal-pocket = Pin; arm = Ar; Thigh = Th; forearm/ inner elbow = IE; leg fold/thigh = IK; dorsal = Do; Doral side of the head = DFH; dorsal face of the tail = DFt; ventral side of the tail = VFt; leg = Lg; pre-femoral region = PFR; Ventral region = VE. Site Axis 1 Axis 2 VFH 0.00 0.02 Ab 0.00 0.11# Pax 0.41# 0.07 Lnp 0.91# -0.07 Pin 0.00 0.11# Br 0.00 0.16# Th 0.01 0.44# IE 0.00 0.12# IK 0.01 0.25# Do 0.01 0.29# DFH 0.00 0.02 DFt 0.00 0.02 VFt 0.00 0.09 Lg 0.01 0.30# PFR 0.01 0.03 VE 0.03 0.70# Note: Bold character indicated with #. Table 3. Parasite species of different Brazilian lizard species (with their respective host habitat type), and values of prevalence (in %), intensity of infection, as well as the corresponding range of the infection intensity, and source of the data. Pa = Parasite specie; Pr = Prevalence; M = Mean Intensity. Hosts Habitats N Pa Pr Ameiva ameiva Restinga 42 E. alfreddugesi 5.0% Cnemidophorus Restinga 100 E. alfreddugesi 72.0% littoralis Restinga 21 E. alfreddugesi 95.2% Mabuya agilis Restinga 26 E. alfreddugesi 96.1% Restinga 26 E. alfreddugesi 96.1% Restinga 7 E. alfreddugesi 100% Mabuya Restinga 72 E. alfreddugesi 94.4% macrorhyncha Restinga 78 E. alfreddugesi 94.0% Restinga 12 E. alfreddugesi 100% Tropidurus Ecotone(*) 16 E. alfreddugesi 100% cocorobensis Tropidurus Ecotone(*) 13 E. alfreddugesi 100% erythrocephalus Tropidurus Ecotone(*) 20 E. alfreddugesi 100% hispidus Montane 56 E. alfreddugesi 37.5% secondary forest Tropidurus Cerrado 85 E. alfreddugesi 88.2% itambere Tropidurus Cerrado 97 E. alfreddugesi 87.6% oreadicus Tropidurus Ecotone(*) 34 E. alfreddugesi 97.1% semitaeniatus Tropidurus Restinga 146 E. alfreddugesi 97.7% torquatus Restinga 62 E. alfreddugesi 100% Cerrado 75 E. alfreddugesi 65.2% Tropidurus Montane 56 Geckobiella sp. 50% hispidus secondary forest Hosts Habitats M Ameiva ameiva Restinga 1.0 Cnemidophorus Restinga 8.3 [+ or -] 10.2 littoralis Restinga 19.1 [+ or -] 16.8 Mabuya agilis Restinga 105.7 Restinga 110.1 [+ or -] 115.8 Restinga 20.9 [+ or -] 9.3 Mabuya Restinga 42.6 macrorhyncha Restinga 42.4 [+ or -] 50.3 Restinga 11.1 [+ or -] 13.1 Tropidurus Ecotone(*) 70.1 [+ or -] 41.7 cocorobensis Tropidurus Ecotone(*) 165.8 [+ or -] 126.0 erythrocephalus Tropidurus Ecotone(*) 146.2 [+ or -] 114.2 hispidus Montane 10.2 [+ or -] 8.7 secondary forest Tropidurus Cerrado 36.67 [+ or -] 41.09 itambere Tropidurus Cerrado 15.38 [+ or -] 21.08 oreadicus Tropidurus Ecotone(*) 52.3 [+ or -] 42.4 semitaeniatus Tropidurus Restinga 164.9 [+ or -] 161.9 torquatus Restinga 86.4 [+ or -] 94.6 Cerrado 12.13 [+ or -] 21.09 Tropidurus Montane 5.9 [+ or -] 6.8 hispidus secondary forest Hosts Habitats References Ameiva ameiva Restinga Cunha-Barros and Rocha (2000) Cnemidophorus Restinga Cunha-Barros and Rocha (2000) littoralis Restinga Cunha-Barros et al. (2003) Mabuya agilis Restinga Cunha-Barros and Rocha (1995) Restinga Cunha-Barros and Rocha (2000) Restinga Cunha-Barros et al. (2003) Mabuya Restinga Cunha-Barros and Rocha (1995) macrorhyncha Restinga Cunha-Barros and Rocha (2000) Restinga Cunha-Barros et al. (2003) Tropidurus Ecotone(*) Rocha et al. (2008) cocorobensis Tropidurus Ecotone(*) Rocha et al. (2008) erythrocephalus Tropidurus Ecotone(*) Rocha et al. (2008) hispidus Montane Present study secondary forest Tropidurus Cerrado Carvalho et al. (2006) itambere Tropidurus Cerrado Carvalho et al. (2006) oreadicus Tropidurus Ecotone(*) Rocha et al. (2008) semitaeniatus Tropidurus Restinga Cunha-Barros and Rocha (2000) torquatus Restinga Cunha-Barros et al. (2003) Cerrado Carvalho et al. (2006) Tropidurus Montane Present study hispidus secondary forest