Comp. Parasitol. 77(2), 2010, pp. 242–246
Research Note
Helminths from Three Species of Anoles: The Humble Anole, Anolis humilis; the Border Anole, Anolis limifrons; and the Lion Anole, Anolis lionotus (Squamata: Polychrotidae), from Nicaragua STEPHEN R. GOLDBERG,1,4 CHARLES R. BURSEY,2
AND
LAURIE J. VITT3
1
Department of Biology, Whittier College, P.O. Box 634, Whittier, California 90608, U.S.A. (e-mail:
[email protected]), 2 Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146, U.S.A. (e-mail:
[email protected]), and 3 Sam Noble Oklahoma Museum of Natural History and Zoology Department, University of Oklahoma, Norman, Oklahoma 73072, U.S.A. (e-mail:
[email protected])
Helminths of 3 species of anoles, Anolis humilis, Anolis limifrons, and Anolis lionotus, from Nicaragua were identified. Twelve new host records and 5 new locality records are reported. It appears that anoles are infected by generalist helminths whose hosts and geographic distributions are structured by ecological fitting rather than any coevolutionary dynamic. KEY WORDS: Polychrotidae, Anolis humilis, Anolis limifrons, Anolis lionotus, Nicaragua, Digenea, Cestoda, Nematoda, Acanthocephala. ABSTRACT:
for helminths. The anoles had been collected by L.J.V. at Isla de Diamante on Rio San Juan, Rio San Juan Province, Nicaragua (11u039N, 85u409W), March–April 1993, and deposited in the herpetology collection at OMNH (A. humilis, OMNH 35921– 35931, 40351–40370; A limifrons, OMNH 35932– 35950, 36372, 40380, 40382–40391; A. lionotus, OMNH 35952–35967, 35969–36003, 36378, 40402– 40411). The body cavity was opened, and the lungs and small and large intestines were examined for helminths. Stomachs had previously been removed and were not available for examination, thereby limiting our results. Nematodes were cleared in glycerol on a microscope slide, coverslipped, and identified from these wet mounts. Digenea, Cestoda, and Acanthocephala were stained in hematoxylin, mounted in Canada balsam, and studied as whole mounts. Parasite terminology is in accordance with Bush et al. (1997); lizard taxonomy is in accordance with Uetz and Hallermann (2009). Found in A. humilis were one species of Cestoda, Mathevotaenia sp.; 2 species of Nematoda, Oswaldocruzia nicaraguensis Bursey, Goldberg, and Vitt, 2006 and Cosmocercoides variabilis (Harwood, 1930); and 1 species of Acanthocephala, Acanthocephalus saurius Bursey and Goldberg, 2003. Found in A. limifrons were 1 species of digenean, Brachycoelium salamandrae (Fro¨lich, 1789); 3 species of Nematoda, O. nicaraguensis, Rhabdias nicaraguensis Bursey, Goldberg, and Vitt, 2007, Skrjabinelazia gaillardi (Chabaud, 1973); and 1 species of Acanthocephala, A. saurius. Found in A. lionotus were 3 species of Digenea, B. salamandrae, Parallopharynx jonesi Ubelaker, 1965, Urotrema shirleyae Zamparo, Brooks, and Tkach, 2005; 2 species of Nematoda, O. nicaraguensis and C. variabilis; and 1 species of
Currently 368 species are assigned to Anolis (Uetz and Hallermann, 2009), of which 14 species are known from Nicaragua (Ko¨hler, 1999). Both the humble anole, Anolis humilis (Peters, 1863), and the border anole, Anolis limifrons (Cope, 1871), are found from eastern Honduras to Panama; the lion anole, Anolis lionotus (Cope, 1861), is known from eastern Honduras to Costa Rica (Ko¨hler, 1999). To our knowledge there are no reports of helminths from A. humilis, 1 report (Bursey and Goldberg, 2003) of helminths in A. limifrons, and 2 reports (Ubelaker, 1965; Zamparo et al., 2004) for A. lionotus. The purpose of this paper is to provide an initial helminth list for A. humilis, to update the helminth lists of A. limifrons and A. lionotus, and to characterize the helminth community infecting Anolis lizards. Thirty-one individuals of A. humilis (mean snoutvent length [SVL] 5 32.4 mm 6 4.7 SD, range 22– 39 mm), 31 individuals of A. limifrons (SVL 5 36.1 mm 6 4.4 SD, range 23–43 mm), and 62 individuals of A. lionotus (SVL 5 52.3 mm 6 13.2 SD, range 24–74 mm) were borrowed from the Sam Noble Oklahoma Museum of Natural History (OMNH), Norman, Oklahoma, U.S.A., and examined 4
Corresponding author 242
RESEARCH NOTES
Acanthocephala, A. saurius. Infection site, number of helminths, prevalence, mean intensity of infections 6 SD, range, and new host records are presented in Table 1. Voucher helminths were deposited in the United States National Parasite Collection (USNPC), Beltsville, Maryland, USA as: A. humilis (Mathevotaenia sp. USNPC 102075, C. variabilis USNPC 102076, O. nicaraguensis USNPC 102077, A. saurius USNPC 102078); for A. limifrons (B. salamandrae USNPC 102079, O. nicaraguensis USNPC 102080, R. nicaraguensis USNPC 102081, S. gaillardi USNPC 102082, A. saurius USNPC 102083); for A. lionotus (P. jonesi USNPC 102086, 102087, U. shirleyae USNPC 102084, 102085, O. nicaraguensis USNPC 102089, C. variabilis USNPC 102088, A. saurius USNPC 102090). Brachycoelium salamandrae is widespread in amphibians and a few reptiles of Europe and North and South America; hosts were summarized in Goldberg et al. (2007). Anolis limifrons and A. lionotus represent new host records and Nicaragua is a new locality record for B. salamandrae. Parallopharynx jonesi was originally described from A. lionotus collected in Nicaragua (Ubelaker, 1965). It is also known from Anolis biporcatus, A. lionotus, and Basiliscus basiliscus from Costa Rica (Zamparo et al., 2004). Urotrema shirleyi was described from A. lionotus and Anolis (as Norops) cupreus collected in Costa Rica (Zamparo et al., 2005). It has been reported from Anolis fuscoauratus from Brazil (Goldberg et al., 2006). Nicaragua is a new locality record for U. shirleyae. Species of Mathevotaenia occur in a variety of birds and mammals (Schmidt, 1986). To our knowledge, A. humilis is the first reptile to harbor a species assigned to this genus. Further work will be necessary to determine whether these specimens represent a previously undescribed species. Anolis humilis represents a new host record for the genus, and Nicaragua is a new locality record. Oswaldocruzia nicaraguensis was described from the teiid lizard, Ameiva festiva, from Nicaragua by Bursey et al. (2006). It has been reported from Anolis (as Norops) capito collected in Nicaragua (Bursey, Goldberg, and Vitt, 2007) and Sphenomophus cherriei collected in Costa Rica (Goldberg and Bursey, 2007). Anolis humilis, A. limifrons, and A. lionotus represent new host records for O. nicaraguensis. Rhabdias nicaraguensis was described from A. capito from Nicaragua (Bursey, Goldberg, and Vitt, 2007). Anolis limifrons is a new host record and the second host known to harbor R. nicaraguensis. Skrjabinelazia
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galliardi was described from Gonatodes humeralis collected in Brazil (Chabaud, 1973). It was reported in Gonatodes albogularis from Panama (Bursey, Goldberg, and Telford, 2007) and Tropidurus torquatus from Brazil (Vrcibradic et al., 2000). Anolis limifrons represents a new host record and Nicaragua is a new locality record for S. galliardi. Cosmocercoides variabilis is well known in salamanders, toads, frogs, lizards, snakes, and turtles of North America; a host list was provided by Bursey, Goldberg, and Telford (2007). It is also known to occur in Mexico, Panama, and Costa Rica (Goldberg et al., 1999; Bursey, Goldberg, and Telford, 2007; Goldberg and Bursey, 2008). Anolis humilis and A. lionotus represent new host records and Nicaragua is a new locality record for C. variabilis. Acanthocephalus saurius was described from A. (as Norops) limifrons from Costa Rica by Bursey and Goldberg (2003). It was previously reported from A. capito collected in Nicaragua and Prionodactylus oshaughnessyi collected in Brazil (Bursey and Goldberg, 2004; Bursey, Goldberg, and Vitt, 2007). Anolis humilis and A. lionotus represent new host records for A. saurius. Currently, helminths of A. humilis include 1 species of cestode, Mathevotaenia sp.; 2 species of nematodes, O. nicaraguensis, C. variabilis; and 1 acanthocephalan species, A. saurius. The helminths of A. limifrons include 2 species of digeneans, B. salamandrae, Mesocoelium monas; 4 species of nematodes, adults of O. nicaraguensis, Piratuba digiticauda, Strongyluris panamanensis, and larvae of a species of Acuariidae; and 1 species of acanthocephalan, A. saurius. Helminths of A. lionotus include 3 species of digeneans, B. salamandrae, P. jonesi, U. shirleyae; 2 species of nematodes, O. nicaraguensis, C. variabilis; and 1 species of acanthocephalan, A. saurius. None of the helminth species collected in this study are restricted to a single host species. Thus, it would appear that Anolis lizards are parasitized by generalist helminths. This was also the case in a helminthological study of 12 species of anoles from the Greater Antilles (Goldberg et al., 1997). Such an interpretation is at odds with the suggestion that virtually all helminths are ecological specialists, especially with respect to transmission patterns and microhabitat preference (Brooks and McLennan, 1993, 2002; Adamson and Caira, 1994). The anole helminth community presented here is composed of monoxenous helminths with direct life cycles (e.g., O. nicaraguensis, R. nicaraguensis, S. gaillardi) as
* 5 new host record.
Acanthocephalus saurius
Acanthocephala
Cosmocercoides variabilis Oswaldocruzia nicaraguensis Rhabdias nicaraguensis Skrjabinelazia gaillardi
Nematoda
Mathevotaenia sp.
Cestoda
Brachycoelium salamandrae Parallopharynx jonesi Urotrema shirleyae
Digenea
Helminth
Small intestine
Large intestine Small intestine Lung Large intestine
Small intestine
Small intestine Small intestine Small intestine
Site
*31
*3 *14 — —
*42
— — —
N
1 3.5 6 1.3 — —
4.7 6 5.0
— — —
x¯ 6 SD
42 (13/31) 2.4 6 1.5
10 (3/31) 13 (4/31) — —
29 (9/31)
— — —
%
Anolis humilis
1–6
— 2–5 — —
1–13
— — —
r
26
— *25 *3 *10
—
*3 — —
N
— 8.3 6 11.6 1.5 6 0.7 5.0 6 4.2
—
1.5 6 0.7 — —
x¯ 6 SD
42 (13/31) 2.0 6 0.8
— 10 (3/31) 6 (2/31) 6 (2/31)
—
6 (2/31) — —
%
Anolis limifrons
1–3
— 1–22 1–2 2–8
—
1–2 — —
r
*4
*2 *3 — —
—
*4 29 285
N
6 (4/62)
3 (2/62) 5 (3/62) — —
—
2 (1/62) 23 (14/62) 66 (41/62)
%
1
1 1 — —
—
4 2.1 6 1.6 7.0 6 7.6
x¯ 6 SD
Anolis lionotus
—
— — — —
—
— 1–6 1–32
r
Table 1. Site of infection, number of helminths (N), prevalence (%), mean intensity (x¯) ± SD and range (r) for Anolis humilis (N = 31), Anolis limifrons (N = 31) and Anolis lionotus (N = 62) from Nicaragua.
244 COMPARATIVE PARASITOLOGY, 77(2), JULY 2010
RESEARCH NOTES
well as heteroxenous life cycles using intermediate hosts (e.g., B. salamandrae, P. jonesi, U. shirleyae, Mathevotaenia sp., and A. saurius). Although we have no information about the species-level phylogenetic relationships among these parasites, the host range precludes any notion that they are products of specialization through cospeciation. The results reported herein parallel the findings of a recent study of the platyhelminth parasites of anurans in the U.S.A., Mexico, and Guanacaste, Costa Rica (Brooks et al., 2006), which suggested that the parasite communities were communities of transmission dynamics and microhabitat preference specialists whose host ranges and geographic distributions were structured by ecological fitting rather than any tight coevolutionary dynamic. We thank Milton Camacho of the Departamento de Fauna Silvestre of Nicaragua for making this research possible, facilitating within-country collecting and obtaining of export permits, and providing excellent logistic aid. Rolando Perez and J. Gabriel Caceres of the Departamento de Fauna Silvestre aided in the field studies and to them we extend our appreciation. Financial aid for this and other Nicaraguan studies stemmed from a research grant from the faculty research council at the University of Oklahoma to L.J.V. and Janalee P. Caldwell. We also thank Sarah Goldsberry and Sean Kark (Whittier College) for assistance with dissections. LITERATURE CITED Adamson, M. L., and J. N. Caira. 1994. Evolutionary factors influencing the nature of parasite specificity. Parasitology 109(Suppl.):S85–S95. Brooks, D. R., and D. A. McLennan. 1993. Parascript: Parasites and the Language of Evolution. Smithsonian Institution Press, Washington, D.C. 429 pp. Brooks, D. R., and D. A. McLennan. 2002. The Nature of Diversity: An Evolutionary Voyage of Discovery. University of Chicago Press, Chicago. 668 pp. Brooks, D. R., D. A. McLennan, V. Leo´n-Re`gagnon, and D. Zelmer. 2006. Ecological fitting as a determinant of parasite community structure. Ecology 87 (Suppl):S76– S85. Bursey, C. R., and S. R. Goldberg. 2003. Acanthocephalus saurius n. sp. (Acanthocephala: Echinorhynchidae) and other helminths from the lizard Norops limifrons (Sauria: Polychrotidae) from Costa Rica. Journal of Parasitology 89:573–576. Bursey, C. R., and S.R. Goldberg. 2004. Cosmocerca vrcibradici n. sp. (Ascaridida: Cosmocercidae), Oswaldocruzia vitti n. sp. (Strongylida: Molineoidae), and other helminths from Prionodactylus eigenmanni and Prionodactylus oshaughnessyi (Sauria: Gymnophthal-
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