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Infestation by chigger mites in two lizard species from a dune habitat of Northern Mexico.

Abstract. -- The occurrence and levels of infestation by larvae of the chigger mite Eutrombicula alfreddugesi on the desert lizards Uma exsul and Uta stejnegeri were studied on the sand dunes of Viesca, Coahuila, Mexico. Chiggers were observed on 68.1% of U. exsul males with an average of 7.81 [+ or -] 2.7 chiggers per lizard; chiggers occurred on 54.5% of the females and averaged 4.18 [+ or -] 1.5 mites per lizard. For U. stejnegeri males, chiggers were observed on 100% of the captured lizards and each lizard averaged 61.12 [+ or -] 6.8 chiggers; 86.8% of the females were parasitized and they averaged 38.05 [+ or -] 6.8 mites per lizard. Regression analyses were used to test the relationship between chigger infestation levels and lizard body size; however, no relationships were detected. All chiggers were found on the neck folds in both lizard species. Morphology (shallow neck folds), microhabitat selection (sandy and sunny), and burrowing behavior could influence the infestation pattern of U. exsul. Home range size (for males), deeper neck folds and selection for cooler and shaded microhabitats with higher relative humidity could account for the greater chigger infestation levels found on U. stejnegeri.

Resumen. -- Se estudio la prevalencia e intensidad de infestacion por larvas de Eutrombicula alfreddugesi en los saurios deserticos Uma exsul y Uta stejnegeri en las dunas de arena de Viesca, Coahuila, Mexico. En U. exsul la prevalencia e infestacion en los machos fue de 68.1% y 7.81 [+ or -] 2.7 acaros respectivamente, y en las hembras fue de 54.5% y 4.18 [+ or -] 1.5 acaros. En U. stejnegeri fue del 100% y 61.12 [+ or -] 6.8 acaros para los machos, y 86.8% y 38.05 [+ or -] 6.8 acaros para las hembras. Utilizando el analisis de regresion se determino que no hubo relacion entre la intensidad de infestacion y el tamano de los saurios. Todos los acaros se encontraron dentro de los pliegues del cuello en ambas especies. La morfologia (pliegues poco profundos en el cuello), la seleccion de microhabitat (arenoso y soleado) y la conducta de entierro son caracteristicas que pueden influenciar el patron de infestacion de U. exsul. El tamano del ambito hogareno (en los machos), los pliegues profundos en el cuello y una seleccion de microhabitats templados y sombreados con una mayor humedad relativa, pueden intervenir en el alto grado de infestacion de U. stejnegeri.

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Chigger mite occurrence and parasitism rates on lizards have been associated with host species' characteristics such as morphology, behavior, and gender. Size of the lizard, scale type, and the presence of folds or pockets, are morphological variables that affect chigger parasitism (Cunha-Barros & Rocha 2000; Salvador et al. 1999). The foraging mode and the activity patterns are examples of behavioral factors (Clopton & Gold 1993; Cunha-Barros et al. 2003), and home range size and male testosterone levels (Salvador et al. 1996; Talleklint-Eisen & Eisen 1999) are examples of gender-specific attributes that influence chigger mite parasitism on lizards.

Eutrombicula alfreddugesi is a chigger mite with a wide distribution. It has been reported throughout the American continent from southern Canada to Argentina and the Caribbean Islands (Loomis & Wrenn 1984; Lareschi et al. 2003; Daniel & Stekol'nikov 2004). Larval chiggers attach themselves to the skin of amphibians, reptiles, birds and mammals (Daniel & Stekol'nikov 2004), and have medical importance because they cause dermatitis in humans (Potts 2001). The parasitic occurrence of this mite on lizards has been studied mainly in the U.S. (Klukowski 2004) and in South America (Cunha-Barros et al. 2003). In Mexico, the few mite/lizard studies that have been conducted were mainly in forest habitats (Garcia-De la Pena et al. 2005a; 2005b); mite/lizard relationships in desert habitats have not been previously studied.

In the sand dunes of Viesca, Coahuila, the Coahuila fringe-toed lizard Uma exsul (currently under a special protection category [SEMARNAT 2001]) and the side blotched lizard Uta stejnegeri are sympatric species. Because sympatric lizards can have species-specific levels of parasitism related to their morphological, behavioral and gender specific characteristics (Cunha-Barros & Rocha 2000), determining the occurrence and infestation levels by E. alfreddugesi on these two phrynosomatid species is important. In this study the proportion of lizards parasitized by at least one mite, the intensity of infestation, its relationship with the size and gender of the lizards, and the distribution of E. alfreddugesi over the body was calculated for both lizard species.

MATERIALS AND METHODS

The study area was located in the middle of Chihuahuan Desert, to the southwest of Coahuila State, Mexico, municipality of Viesca (25[degrees]26'27"N, 102[degrees]55'15"W) (Fig. 1). This region has an elevation of 1100 m. The annual average precipitation is 250 mm, occurring mainly between July to September (INEGI 1988). Annual temperature averages 21[degrees] C, with December and January being the coldest months, and July and August the warmest (Garcia 2004). Perennial dune vegetation consists of creosote bush (Larrea tridentata), black seepweed (Suaeda nigrescens), and honey mesquite (Prosopis glandulosa) (Rzedowski 1978). In November there are high densities of annual plants including desert marigold (Baileya multiradiata) and woolly tidestromia (Tidestromia lanuginosa) (Garcia-De la Pena et al. 2007).

Data collection was limited to November 2004 to factor out possible seasonal effects on chigger infestation patterns. Individuals of U. exsul and U. stejnegeri were captured with a noose or by hand. Data collected for each lizard included: sex (hemipenal eversion used to identify U. exsul males, and dorsal pattern and coloration to identify U. stejnegeri males), snout-vent length (SVL, to the nearest 0.1 mm), weight (W) measured to the nearest 0.1 g with a 30-g Pesola[TM] spring scale, and total number of chigger mites carried ([T.sub.m]). To measure [T.sub.m], each specimen was carefully examined with special attention to neck folds, axillae and posfemoral pleats. The mites were removed in the field using wetted cotton swabs. The red color of the mites facilitated counting them on the surface of the cotton with a magnifying glass and then collecting them. Each lizard was temporally marked on its back using an indelible marker to avoid recaptures. Lizards were released at the place of capture.

[FIGURE 1 OMITTED]

Kolmogorov-Smirnov goodness of fit tests revealed SVL, W, and [T.sub.m] to be normality distributed, so t-tests were used to compare means of SVL, W, and [T.sub.m] between sexes of each species, and between species (combined data for females and males). To identify differences in infestation intensity between sexes for each species and between species, Analyses of Covariance (SVL and weight as covariates) were used. Regression analyses were also conducted between SVL and [T.sub.m], and W and [T.sub.m] for both species. All tests assumed to be significant at [alpha] = 0.05. Measurements are reported as mean [+ or -] SE.

RESULTS

Mite parasitism levels for 44 Uma exsul (22 males and 22 females) and 88 Uta stejnegeri (50 males and 38 females) were measured. Results revealed that 68.1% of males and 54.5% of females of U. exsul showed infestation. For U. stejnegeri, 100% of males and 86.8% of females carried at least one chigger. The difference in SVL of males and females in U. exsul did not reach traditional levels of statisitical significance (t = 1.91, d.f. = 42, P = 0.06); however, males averaged statistically heavier than females (t = 2.28, d.f. = 42, P = 0.02) (Table 1). The mean SVL of male U. stejnegeri was significantly greater (t = 8.48, d.f. = 86, P = 0.0001) and the males were heavier than females (t = 7.87, d.f. = 86, P = 0.0001) (Table 1). As with SVL, differences in mean [T.sub.m] values for U. exsul males and females (Table 1) did not reach traditional levels of statistical significance (ANCOVA: F = 3.04, d.f. = 1.40, P = 0.08). Males of U. stejnegeri did have greater mite infestations than females (ANCOVA: F = 5.92, d.f. = 1.84, P = 0.01) (Table 1).

There was no relationship between SVL and [T.sub.m] in either species (U. exsul: [r.sup.2] = 0.04, F = 2.09, d.f. = 1.42, P = 0.15; U. stejnegeri: [r.sup.2] = 0.04, F = 2.02, d.f. = 1.42, P = 0.16) or between W and [T.sub.m] (U. exsul: [r.sup.2] = 0.006, F = 0.48, d.f. = 1.86, P = 0.48; U. stejnegeri: [r.sup.2] = 0.11, F = 1.07, d.f. = 1.86, P = 0.30). Ignoring gender differences, U. exsul averaged larger than U. stejnegeri [SVL: U. exsul (61.59 [+ or -] 1.8 mm), U. stejnegeri (48.84 [+ or -] 0.4 mm), t = 8.63, d.f. = 130, P = 0.0001; Weight: U. exsul (8.72 [+ or -] 0.9 g), U. stejnegeri (4.78 [+ or -] 0.1 g), t = 5.49, d.f. = 130, P = 0.0001. The overall intensity of mite infestations on U. stejnegeri (51.15 [+ or -] 4.9 chiggers, range = 0-218) was greater than on U. exsul (6 [+ or -] 1.5 chiggers, range = 0-56), ANCOVA: F = 18.93, d.f. = 1.128, P = 0.0001]. Mites were found exclusively in the neck folds of males and females of both species.

DISCUSSION

For both sexes of Uma exsul and Uta stejnegeri chiggers occurred on more than 50% of the individuals, indicating that Eutrombicula alfreddugesi did not appear to discriminate between the two lizard species as hosts. The level of mite infestation in males and females of U. exsul was similar and was not related to the SVL or W of the individuals. In contrast, the number of chiggers found on males of U. stejnegeri was higher than on females. The size of individuals of U. stejnegeri did not influence the level of infestation, however, it may be that the home range of this species is related to the number of chiggers that parasite it. It was observed that during the non-breeding fall season (November), the males of U. stejnegeri occupied home ranges twice the size as those of the females in comparison with the breeding season. When males cover a greater area, they encounter many microhabitats. This increases the probability of contacting more chiggers and becoming parasitized by them (Davis & Ford 1983; Talleklint-Eisen & Eisen 1999).

Individuals of U. exsul had reduced chigger levels compared to U. stejnegeri. The microhabitats which each species occupies may explain this finding. Clopton & Gold (1993) observed that Eutrombicula alfreddugesi prefers areas of low to moderate temperature, high relative humidity, little incidence of sunlight, and dense vegetation. Garcia-De la Pena et al. (2007) observed that U. exsul and U. stejnegeri select different microhabitats on the dunes of Viesca. U. exsul primarily use creosote bushes for thermoregulating and foraging. Creosote has an open canopy that allows considerable sunlight to reach the ground below, and generally grows in very sandy areas where rodent burrow abundance is low. During this study, air and substrate temperatures around 30[degrees] C and 38[degrees] C, respectively, and a relative humidity around 20% were observed in these areas. This may explain the low numbers of chiggers in this microhabitat, which would explain the relatively low mite levels found on U. exsul. In the drier and hotter sand dunes in the northwest portion of the Sonoran Desert, another fringe-toed lizard, Uma inornata, was never observed with mite infestations (Barrows, pers. comm.). Also, the sand burrowing behavior that characterizes members of the genus Uma may offer an additional explanation for the fewer chiggers found on U. exsul. Fringe-toed lizards dive into loose sand and can "swim" beneath the sand surface for short distances to avoid thermal stress and to escape predators (Stebbins 1944). This behavior results in friction of their skin against the sand, which can act like an abrasive that removes the mites that are not well protected by the folds of the neck.

In contrast, U. stejnegeri has been more frequently observed thermoregulating and foraging beneath black seepweed (Garcia-De la Pena et al. 2007). This shrub has a dense canopy and usually grows in compact sand mounds. Its roots and the burrows that rodents construct underneath are likely refuges and nesting sites for this lizard. Air and substrate temperatures around 28[degrees] C and 35[degrees] C, respectively, and a relative humidity around 25% were observed in these areas. Because the microclimates that exist underneath this plant and within the burrows are cooler and more humid than on the more open sand dunes, the abundance of chiggers would be greater and so would explain the higher chigger infestations on U. stejnegeri.

In both lizard species, mites were found exclusively in the neck folds. Chiggers infesting U. stejnegeri were concentrated in folds that form deep cavities (almost a pocket) where mites remained well protected. In contrast, U. exsul has shallow folds on the neck and near the shoulders, which probably do not provide good protection for the chiggers and it make them susceptible to be detached during the lizards' sand burrowing behavior.

In conclusion, mechanisms explaining the disparity in the occurrence and intensity of chigger infestations on two lizard species can be complex. Different neck fold morphology, burrowing behavior and microclimate selection each likely contributes to the differences observed between the species considered in this analysis. Within U. stejnegeri, differences in chigger levels between males and females may be explained by the much larger home ranges traveled by the males. This species' lack of sand burrowing behavior, and deeper neck folds and selection for cooler microhabitats with higher relative humidity could explain the observed higher chigger infestation levels compared to U. exsul. Although this study was restricted to November, infested lizards of both species were observed in April and August. Seasonal changes in infestation intensity of chiggers on U. exsul and U. stejnegeri are likely because of climatic factors (temperature and humidity) influence (Sasa 1961; Klukowski 2004). Further studies are needed to elucidate these host-parasite relationships.

ACKNOWLEDGEMENTS

To Consejo Nacional de Ciencia y Tecnologia (CONACyT) for the economical support during doctoral programs of CGP and GC. To Nixon Wilson (University of Northern Iowa) for the determination of the species of chigger mite, and to A. Rios-Saldana, G. Mata-Flores, and A. Sanchez-Almazan for their valuable help in the field.

LITERATURE CITED

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Cunha-Barros, M. & C. F. D. Rocha. 2000. Ectoparasitism by chigger mites (Eutrombicula alfreddugesi: Trombiculidae) in a restinga lizard community. Ciencia e Cultura, 52:108-114.

Cunha-Barros, M., M. Van Sluys, D. Vrcibradic, C. A. B. Galdino, F. H. Hatano & C. F. D. Rocha. 2003. Patterns of infestation by chigger mites in four diurnal lizard species from a restinga habitat (Jurubatiba) of Southeastern Brazil. Braz. J. Biol., 63(3):393-399.

Daniel, M. & A. A. Stekol'nikov. 2004. Chiggers mites of the genus Eutrombicula Ewing, 1938 (Acari: Trombiculidae) from Cuba, with the description of three new species. Folia Parasit., 51:359-366.

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Loomis, R. B. & W. J. Wrenn. 1984. Systematics of the pest chigger genus Eutrombicula (Acari: Trombiculidae). Pp. 152-159, in Acarology VI, vol. 1. (D. A. Griffiths & C. E. Bowman, eds.), Wiley, New York, 646 pp.

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CG at: cristina.g.delapena@gmail.com

Cristina Garcia-De la Pena, Gamaliel Castaneda and Cameron W. Barrows*

Facultad de Ciencias Biologicas, Universidad Autonoma de Nuevo Leon C.P. 66450, San Nicolas de los Garza, Nuevo Leon, Mexico

*Center for Conservation Biology, University of California 75-080 Frank Sinatra Drive, Palm Desert, California 92211, USA
Table 1. Snouth-vent length (SVL), weight (W), total number of chigger
mites carried ([T.sub.m]) and [T.sub.m] range for males and females of
Uma exsul and Uta stejnegeri.

Species Uma exsul
Sex [male] [female]

SVL 65.09 [+ or -] 3.4 mm 58.09 [+ or -] 1.2 mm
W 10.84 [+ or -] 1.8 g 6.60 [+ or -] 0.4 g
[T.sub.m] 7.81 [+ or -] 2.7 4.18 [+ or -] 1.5
[T.sub.m] range 0-56 0-31

Species Uta stejnegeri
Sex [male] [female]

SVL 51.36 [+ or -] 0.4 mm 45.52 [+ or -] 3.5 mm
W 5.55 [+ or -] 0.1 g 3.76 [+ or -] 0.1 g
[T.sub.m] 61.12 [+ or -] 6.8 38.05 [+ or -] 6.8
[T.sub.m] range 3-218 0-188
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Author:Garcia-De la Pena, Cristina; Castaneda, Gamaliel; Barrows, Cameron W.
Publication:The Texas Journal of Science
Geographic Code:1MEX
Date:Feb 1, 2007
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