BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofitpublishers, academic institutions, research libraries, and research funders in the common goal of maximizing access tocritical research.

Helminths from Three Species of Anoles: The Humble Anole,Anolis humilis; the Border Anole, Anolis limifrons; and theLion Anole, Anolis lionotus (Squamata: Polychrotidae), fromNicaraguaAuthor(s): Stephen R. Goldberg, Charles R. Bursey, and Laurie J. VittSource: Comparative Parasitology, 77(2):242-246. 2010.Published By: The Helminthological Society of WashingtonDOI: http://dx.doi.org/10.1654/4424.1URL: http://www.bioone.org/doi/full/10.1654/4424.1

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in thebiological, ecological, and environmental sciences. BioOne provides a sustainable onlineplatform for over 170 journals and books published by nonprofit societies, associations,museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated contentindicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercialuse. Commercial inquiries or rights and permissions requests should be directed to theindividual publisher as copyright holder.

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: sgoldberg@whittier.edu),2 Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146, U.S.A.

(e-mail: exb13@psu.edu), and3 Sam Noble Oklahoma Museum of Natural History and Zoology Department, University of Oklahoma, Norman, Oklahoma

73072, U.S.A. (e-mail: vitt@ou.edu)

ABSTRACT: 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 limi-

frons, Anolis lionotus, Nicaragua, Digenea, Cestoda,

Nematoda, Acanthocephala.

Currently 368 species are assigned to Anolis (Uetz

and Hallermann, 2009), of which 14 species are

known from Nicaragua (Kohler, 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 (Kohler, 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 snout-

vent 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

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, Oswal-docruzia nicaraguensis Bursey, Goldberg, and Vitt,

2006 and Cosmocercoides variabilis (Harwood,

1930); and 1 species of Acanthocephala, Acantho-cephalus saurius Bursey and Goldberg, 2003. Found

in A. limifrons were 1 species of digenean, Brachy-coelium salamandrae (Frolich, 1789); 3 species of

Nematoda, O. nicaraguensis, Rhabdias nicaraguen-sis Bursey, Goldberg, and Vitt, 2007, Skrjabinelaziagaillardi (Chabaud, 1973); and 1 species of Acan-

thocephala, A. saurius. Found in A. lionotus were 3

species of Digenea, B. salamandrae, Parallopharynxjonesi Ubelaker, 1965, Urotrema shirleyae Zamparo,

Brooks, and Tkach, 2005; 2 species of Nematoda, O.nicaraguensis and C. variabilis; and 1 species of4 Corresponding author

Comp. Parasitol.77(2), 2010, pp. 242–246

242

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 (Mathevo-taenia sp. USNPC 102075, C. variabilis USNPC

102076, O. nicaraguensis USNPC 102077, A.saurius USNPC 102078); for A. limifrons (B.salamandrae USNPC 102079, O. nicaraguensisUSNPC 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. Parallo-pharynx 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. Anolishumilis 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 cherrieicollected in Costa Rica (Goldberg and Bursey, 2007).

Anolis humilis, A. limifrons, and A. lionotus represent

new host records for O. nicaraguensis. Rhabdiasnicaraguensis was described from A. capito from

Nicaragua (Bursey, Goldberg, and Vitt, 2007). Anolislimifrons is a new host record and the second host

known to harbor R. nicaraguensis. Skrjabinelazia

galliardi was described from Gonatodes humeraliscollected in Brazil (Chabaud, 1973). It was reported in

Gonatodes albogularis from Panama (Bursey, Gold-

berg, and Telford, 2007) and Tropidurus torquatusfrom Brazil (Vrcibradic et al., 2000). Anolis limifronsrepresents a new host record and Nicaragua is a new

locality record for S. galliardi. Cosmocercoidesvariabilis 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 Prionodactylusoshaughnessyi collected in Brazil (Bursey and Gold-

berg, 2004; Bursey, Goldberg, and Vitt, 2007). Anolishumilis 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, Piratubadigiticauda, Strongyluris panamanensis, and larvae

of a species of Acuariidae; and 1 species of

acanthocephalan, A. saurius. Helminths of A. lionotusinclude 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

RESEARCH NOTES 243

Ta

ble

1.

Sit

eo

fin

fect

ion

,n

um

ber

of

hel

min

ths

(N),

pre

vale

nce

(%),

mea

nin

ten

sity

(x)

±S

Da

nd

ran

ge

(r)

for

An

oli

sh

um

ilis

(N=

31

),A

no

lis

lim

ifro

ns

(N=

31

)a

nd

An

oli

sli

on

otu

s(N

=6

2)

fro

mN

ica

rag

ua

.

Hel

min

thS

ite

Ano

lis

hum

ilis

Ano

lis

lim

ifro

nsA

noli

sli

onot

us

N%

x6

SD

rN

%x

6S

Dr

N%

x6

SD

r

Dig

enea

Bra

chyc

oeli

umsa

lam

andr

ae

Sm

all

inte

stin

e—

——

—*3

6(2

/31)

1.5

60.7

1–2

*4

2(1

/62)

4—

Par

all

opha

rynx

jones

iS

mal

lin

test

ine

——

——

——

——

29

23

(14/6

2)

2.1

61.6

1–6

Uro

trem

ash

irle

yae

Sm

all

inte

stin

e—

——

——

——

—285

66

(41/6

2)

7.0

67.6

1–32

Ces

toda

Mat

hevo

taen

iasp

.S

mal

lin

test

ine

*42

29

(9/3

1)

4.7

65.0

1–13

——

——

——

——

Nem

atoda

Cos

moc

erco

ides

vari

abil

isL

arge

inte

stin

e*3

10

(3/3

1)

1—

——

——

*2

3(2

/62)

1—

Osw

aldo

cruz

iani

cara

guen

sis

Sm

all

inte

stin

e*14

13

(4/3

1)

3.5

61.3

2–5

*25

10

(3/3

1)

8.3

611.6

1–22

*3

5(3

/62)

1—

Rhab

dias

nica

rague

nsi

sL

ung

——

——

*3

6(2

/31)

1.5

60.7

1–2

——

——

Skrj

abin

elazi

aga

illa

rdi

Lar

ge

inte

stin

e—

——

—*10

6(2

/31)

5.0

64.2

2–8

——

——

Aca

nth

oce

phal

a

Aca

ntho

ceph

alus

saur

ius

Sm

all

inte

stin

e*31

42

(13/3

1)

2.4

61.5

1–6

26

42

(13/3

1)

2.0

60.8

1–3

*4

6(4

/62)

1—

*5

new

host

reco

rd.

244 COMPARATIVE PARASITOLOGY, 77(2), JULY 2010

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 phylo-

genetic 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 col-

lecting 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. Evolutionaryfactors 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. SmithsonianInstitution Press, Washington, D.C. 429 pp.

Brooks, D. R., and D. A. McLennan. 2002. The Nature ofDiversity: An Evolutionary Voyage of Discovery.University of Chicago Press, Chicago. 668 pp.

Brooks, D. R., D. A. McLennan, V. Leon-Regagnon, andD. Zelmer. 2006. Ecological fitting as a determinant ofparasite community structure. Ecology 87 (Suppl):S76–S85.

Bursey, C. R., and S. R. Goldberg. 2003. Acanthocephalussaurius n. sp. (Acanthocephala: Echinorhynchidae) andother helminths from the lizard Norops limifrons(Sauria: Polychrotidae) from Costa Rica. Journal ofParasitology 89:573–576.

Bursey, C. R., and S.R. Goldberg. 2004. Cosmocercavrcibradici n. sp. (Ascaridida: Cosmocercidae), Os-waldocruzia vitti n. sp. (Strongylida: Molineoidae), andother helminths from Prionodactylus eigenmanni andPrionodactylus oshaughnessyi (Sauria: Gymnophthal-

midae) from Brazil and Ecuador. Journal of Parasitol-ogy 90:140–145.

Bursey, C. R., S. R. Goldberg, and S. R. Telford, Jr.2007. Gastrointestinal helminths of 14 species oflizards from Panama with descriptions of five newspecies. Comparative Parasitology 74:108–140.

Bursey, C. R., S. R. Goldberg, and L. J. Vitt. 2006. Newspecies of Oswaldocruzia (Nematoda: Molineidae) inAmeiva festiva (Squamata: Teiidae) from Nicaragua.Journal of Parasitology 92:350–352.

Bursey, C. R., S. R. Goldberg, and L. J. Vitt. 2007. Newspecies of Rhabdias (Nematoda: Rhabdiasidae) and otherhelminths from Norops capito (Sauria: Polychrotidae)from Nicaragua. Journal of Parasitology 93:129–131.

Bush, A. O., K. D. Lafferty, J. M. Lotz, and A. W.Shostak. 1997. Parasitology meets ecology on its ownterms: Margolis et al. revisited. Journal of Parasitology83:575–583.

Chabaud, A. G. 1973. Skrjabinelazia Sypliaxov 1930 (5Salobrella Freitas 1940), genre de transition entrecosmocercoides et spirurides. Annales de ParasitologieHumaine et Comparee 48:329–344.

Goldberg, S. R., and C. R. Bursey. 2007. Sphenomorphuscherriei (Striped Litter Skink Chirbala Lisa). Endopar-asites. Herpetological Review 38:83–84.

Goldberg, S. R., and C. R. Bursey. 2008. Helminths from10 species of brachycephalid frogs (Anura: Brachyce-phalidae) from Costa Rica. Comparative Parasitology75:255–262.

Goldberg, S. R., C. R. Bursey, J. P. Caldwell, L. J. Vitt,and G. C. Costa. 2007. Gastrointestinal helminthsfrom six species of frogs and three species of lizards,sympatric in Para state, Brazil. Comparative Parasitol-ogy 74:327–342.

Goldberg, S. R., C. R. Bursey, and J. L. Camarillo-Rangel. 1999. Helminths of two lizards, Barisiaimbricata and Gerrhonotus ophiurus (Sauria: Angui-dae), from Mexico. Journal of the HelminthologicalSociety of Washington 66:205–208.

Goldberg, S. R., C. R. Bursey, and H. Cheam. 1997.Helminths of 12 species of Anolis lizards (Polychroti-dae) from the Lesser Antilles, West Indies. Journal of theHelminthological Society of Washington 64:248–257.

Goldberg, S. R., C. R. Bursey, and L. J. Vitt. 2006.Helminths of the brown-eared anole, Norops fuscoaur-atus (Squamata, Polychrotidae), from Brazil andEcuador, South America. Phyllomedusa 5:83–86.

Kohler, G. 1999. The Amphibians and Reptiles of Nicaragua.A Distributional Checklist with Keys. Courier For-schungsinstitut Senckenberg, vol. 213, SenckenbergResearch Institute, Frankfort, Germany. 120 pp.

Schmidt, G. D. 1986. CRC Handbook of TapewormIdentification. CRC Press, Inc., Boca Raton, Florida.675 pp.

Ubelaker, J. E. 1965. Parallopharynx jonesi, a newplagiorchiid trematode from the lizard, Anolis lionotus,in Nicaragua. Journal of Parasitology 51:773–774.

Uetz, P., and J. Hallermann. 2009. The reptile database[Internet]. http://www.reptile-database.org. Accessed2009 June 15.

Vrcibradic, D., M. Cunha-Barros, J. J. Vicente, C. A. C.Galdino, F. H. Hatano, M. Van Sluys, and C. F. D.Rocha. 2000. Nematode infection patterns in foursympatric lizards from a restinga habitat (Jurubatiba) in

RESEARCH NOTES 245

Rio de Janeiro state, southeastern Brazil. Amphibia-Reptilia 21:307–316.

Zamparo, D., D. R. Brooks, and V. Tkach. 2005.Urotrema shirleyae n. sp. (Trematoda: Digenea:Urotrematidae) in Norops oxylophus and N. cupreus(Squamata: Iguania: Polychrotidae) from the Area deConservacion Guanacaste, Costa Rica. Journal ofParasitology 91:648–652.

Zamparo, D., D. R. Brooks, V. Tkach, and B.Rodriguez. 2004. Parallopharynx spp. (Trematoda:Digenea: Plagiorchioidea) in iguanian lizards fromthe Area de Conservacion Guanacaste, Guanacaste,Costa Rica, including Parallopharynx matternaen. sp. in Basiliscus basiliscus (Squamata: Iguania:Corytophanidae). Journal of Parasitology 90:359–363.

246 COMPARATIVE PARASITOLOGY, 77(2), JULY 2010