Molecular Identification of Taenia Serialis Coenurosis in a Wild Ethiopian Gelada - DocsLib

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VETPAR-6943; No. of Pages 4 ARTICLE IN PRESS

Veterinary Parasitology xxx (2013) xxx–xxx

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Veterinary Parasitology

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Short communication

Molecular identiﬁcation of Taenia serialis coenurosis in a wild

Ethiopian gelada (Theropithecus gelada)

a,∗,1 a,1

India A. Schneider-Crease , Noah Snyder-Mackler ,

b c,d

Julie C. Jarvey , Thore J. Bergman

a

Department of Evolutionary Anthropology, Duke University, Durham, NC 27708, United States

b

School of Natural Resources and Environment, University of Michigan, Ann Arbor, MI 48109, United States

c

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, United States

d

Department of Psychology, University of Michigan, Ann Arbor, MI 48109, United States

a r t i c l e i n f o a b s t r a c t

Article history:

Since morphological identiﬁcation of a larval Taeniid in geladas (Theropithecus gelada)

Received 24 May 2013

has produced inconsistent results, genetic information is pivotal for species identiﬁca-

Received in revised form 13 August 2013

tion. Nuclear and mitochondrial DNA from a coenurus in a wild gelada were compared

Accepted 21 August 2013

to published sequences from multiple Taeniid species, conﬁrming the identiﬁcation of this

parasite as Taenia serialis. A demographic analysis ﬁnds age to be a strong predictor of

Keywords:

coenuri. Tapeworms rarely employ primates as intermediate hosts, and the presence of

Taenia serialis

Gelada T. serialis in a wild gelada population may indicate a substantial ecological shift in this

parasite’s life cycle. Molecular phylogeny

Multiceps © 2013 Elsevier B.V. All rights reserved.

1. Introduction the intestinal tract, burrow through the intestinal mucosa,

and settle in the connective tissue or intermuscular fas-

Taeniid parasites globally exploit mammalian cia. Each oncosphere develops into a coenurus, a mass of

predator–prey relationships, requiring a carnivorous multiple invaginated scoleces in a ﬂuid-ﬁlled membrane

deﬁnitive host for the adult form and an herbivorous inter- that expands through the branching and invagination of

mediate host for the larval form (Meyer, 1955). Although endogenous daughter cysts. When a carnivore ingests

primates are not known to regularly act as intermediate the infected tissue, each scolex attaches to the intestinal

hosts, the intermediate stage of one Taeniid has been mucosa to sprout the strobila, a series of hermaphroditic

described in the terrestrial and herbivorous Ethiopian and self-fertilizing segments that constitute the tapeworm

gelada (Theropithecus gelada) (Schwartz, 1927; Urbain and body (Meyer, 1955).

Bullier, 1935; Elek and Finkelstein, 1939; Rodhain and Morphological identiﬁcations of this parasite in cap-

Wanson, 1954; Clark, 1969; Oshawa, 1979; Dunbar, 1980). tive geladas have been inconsistent. Thus, the addition of

Geladas become infected when they ingest tapeworm genetic information to species identiﬁcation is critical. A

eggs shed in the feces of the deﬁnitive host. In interme- genetic identiﬁcation of the parasite and an analysis of the

diate hosts, the oncospheres in the eggs are released into patterns of disease in a wild population of geladas in the

Simien Mountains National Park (SMNP), Ethiopia, are per-

formed here.

∗

Corresponding author at: India Schneider-Crease, Department of

Evolutionary Anthropology, Duke University, 104 Biological Sciences

2. Materials and methods

Building, Box 90383, Durham, NC 27708, United States.

Tel.: +1 919 684 4124; fax: +1 919 660 7348.

E-mail address: [email protected] (I.A. Schneider-Crease). A multiloculated cyst from a dead 13-year-old male

1

Co-ﬁrst authors. gelada in the SMNP was procured in November 2011. One

0304-4017/$ – see front matter © 2013 Elsevier B.V. All rights reserved.

http://dx.doi.org/10.1016/j.vetpar.2013.08.015

Please cite this article in press as: Schneider-Crease, I.A., et al., Molecular identiﬁcation of Taenia serialis coenurosis in a

wild Ethiopian gelada (Theropithecus gelada). Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.08.015

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VETPAR-6943; No. of Pages 4 ARTICLE IN PRESS

2 I.A. Schneider-Crease et al. / Veterinary Parasitology xxx (2013) xxx–xxx

Fig. 2. Phylogenetic relationships between four species of Taenia (T. seri-

alis, T. multiceps, T. crassiceps, T. pisiformis) and the sample obtained for

this study (“sample from gelada”). The tree is based on maximum par-

simony using published partial 12S and ITS-2 sequences obtained from

GenBank (T. pisiformis: ITS-2 JX317674, 12S DQ104230; T. crassiceps: ITS-

2 DQ099564, 12S EU219547; T. multiceps: ITS-2 FJ886762, 12S JQ710642;

T. serialis: ITS-2 DQ099575, 12S DQ104236). Numbers above branches

Fig. 1. Microscope view (10×) of a scolex with a branching endogenous

represent the posterior support (max of 1) for each branch.

daughter cyst from a wild Ethiopian gelada. Photograph by Dr. James Flowers.

3. Results

of the authors (J.C.J.), extracted tissue from a protuberant The BLAST search revealed a strong match between

coenurus on the left ventral forelimb (Fig. 1), and stored the sample sequences (ITS-2: GenBank ID KF414738; 12S:

it in RNAlater (Applied Biosystems/Ambion, Austin, TX, GenBank ID KF414739) and published sequences for Tae-

U.S.A.). nia serialis ITS-2 (99% nucleotide identity; GenBank ID

DNA was extracted from the cestodes using the Qia- DQ099575) and 12S (99% nucleotide identity; GenBank ID

gen DNeasy Blood and Tissue Kit (Qiagen). 347 bp of the DQ104236) regions (Jia et al., 2010). The next most closely

mitochondrial rDNA (12S) region and 434 bp of the second related species was Taenia multiceps, with which the sam-

internal transcribed spacer of nuclear rDNA (ITS-2) were ple had 95% and 90% nucleotide identity at 12S and ITS-2,

ampliﬁed and sequenced using the primers and PCR pro- respectively (GenBank IDs: GQ228818, FJ886762) (Padgett

tocol described in Padgett et al. (2005). Sequences were et al., 2005).

aligned using Sequencher v5.0 (Gene Codes Corporation, Phylogenetic reconstruction with published Taeniid

Ann Arbor, MI) and blasted against the NCBI nucleotide data ITS-2 and 12S sequences conﬁrms that this sample is more

bank. closely related to T. serialis than to any other Taeniid species

For the phylogenetic analysis, two nucleotide sub- (Fig. 2). AIC and BIC supported two different models, K81 + I

stitution models were selected using AIC and BIC as and K80 + G; however, both models supported the same

implemented in jmodeltest (Darriba et al., 2012). Both phylogeny as implemented in BEAST v1.7.5 (Drummond

models were run using the Bayesian program BEAST v1.7.5 et al., 2012).

(Drummond et al., 2012). The MCMC chain length was set The prevalence rate of disease for the population was

8 3

to 10 and the state was recorded every 10 , resulting 4.8% (Table 1). The prevalence rate was 9.9% (13/131)

5

∼

in 10 trees. The effective sample size for all parame- among adults (over 3 years old), and 0.9% among juve-

2

ters was greater than 130. After discarding the ﬁrst 10 niles (approx. 1.5–3 years old) (1/110). Coenuri were not

trees as burn-in, the remaining trees were summarized observed in infants (0–1.5 years old) (n = 50). Adults were

into one consensus tree using TreeAnnotater v1.7.5, which signiﬁcantly more likely to display coenuri than juveniles

2

was imported into FigTree v1.4 (http://tree.bio.ed.ac.uk/) and infants (Pearson’s = 13.661, P = 0.001, d.f. = 2). The

for visualization (Fig. 3). prevalence rate for adult females was 10.8% (10/93), and for

To measure the disease prevalence in the SMNP, males was 7.9% (3/38). There was no signiﬁcant difference

researchers surveyed 291 geladas for coenuri. The Uni- in the disease rate between males and females (Pearson’s

2

versity of Michigan Gelada Research Project has collected = .247, P = 0.620, d.f.=1).

behavioral data on this population for seven years, and

researchers are trained to recognize individuals with

4. Discussion

100% accuracy based on morphological traits. Researchers

recorded the presence/absence, size, and location of

The contribution of a genetic component to the iden-

coenuri for each known individual. Recorded cysts were

tiﬁcation of T. serialis in geladas is imperative because

conﬁrmed by two independent observers.

morphological approaches have produced inconsistent

The prevalence rates given are of obvious signs of dis-

results. The ﬁrst studies on this parasite classiﬁed it under

ease, not infection, since infected individuals may not

the genus Multiceps; now Multiceps and Taenia are under-

exhibit coenuri. To ascertain patterns of coenuri across ages

stood to be synonymous, and Taenia is the preferred

and sexes, Pearson’s chi-squared tests were run using JMP

nomenclature (Meyer, 1955; Benger et al., 1981). While ﬁve

statistical software (JMP, Version 7. SAS Institute Inc., Cary,

studies used scolex arrangement and the size and number

NC, 1989–2007).

of rostellar hooks for identiﬁcation (Schwartz, 1927; Urbain

Please cite this article in press as: Schneider-Crease, I.A., et al., Molecular identiﬁcation of Taenia serialis coenurosis in a

wild Ethiopian gelada (Theropithecus gelada). Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.08.015

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I.A. Schneider-Crease et al. / Veterinary Parasitology xxx (2013) xxx–xxx 3

Table 1

a

Prevalence of T. serialis coenuri in geladas across age-sex classes .

Sex Age

Infant Juvenile Adult All

Female 0% (0/17) 1.8% (1/55) 10.8% (10/93) 6.7% (11/164)

Male 0% (0/33) 0% (0/55) 7.9%(3/38) 2.4% (3/126)

Both 0% (0/50) 0.9% (1/110) 9.9% (13/131) 4.8% (14/291)

a

Number of individuals with coenuri/total individuals in that age-sex class.

and Bullier, 1935; Elek and Finkelstein, 1939; Rodhain and The demographic analysis shows that T. serialis coenuri

Wanson, 1954; Clark, 1969), others used the morphology of are signiﬁcantly more likely to be found in adult than

the hook guards (Schwartz, 1927) or hook blades (Meyer, in subadult or infant geladas, corroborating two previous

1955). Other parasitologists assert that no morphological studies of this population (Oshawa, 1979; Dunbar, 1980).

criterion reliably diagnoses Taenia species (Beveridge and The chronic physiological and social stresses of adulthood

Rickard, 1976). may have immunosuppressive effects that increase adult

susceptibility (Muehlenbein and Bribiescas, 2005). Alter-

natively, the time necessary for development of noticeable

cysts may exceed the geladas’ juvenile period.

T. serialis coenuri can displace viscera and exert mechan-

ical pressure on nerves and arteries, causing spastic limb

paralysis, muscle atrophy, increased vulnerability to pre-

dation, and death (Scott, 1926; Elek and Finkelstein, 1939).

Coenuri may also impact ﬁtness by stimulating an ener-

getically costly immune response, requiring an individual

to prioritize feeding and resting over reproductive behav-

iors (Oshawa, 1979). The presence and consequences of T.

serialis in this population will continue to be monitored.

Other diseases may present similarly to T. serialis

coenuri, and, if so, were erroneously included in this anal-

ysis. However, given the history of cysts whose gross

morphology in geladas is similar to those observed at this

site (Fig. 3) and which have been identiﬁed morphologi-

cally as Taenia or Multiceps serialis, we are conﬁdent that

the cysts reported are indicative of T. serialis infection. This

interpretation is strengthened by the genetic conﬁrmation

of T. serialis from a characteristic cyst in this population.

5. Conclusion

A genetic analysis conﬁrms the presence of T. seri-

alis in geladas, and a demographic analysis shows that

adults are more likely to exhibit coenuri than non-adults.

However, the biology of this T. serialis life cycle is not

yet entirely understood. We speculate that the deﬁni-

tive host is the predatory spotted hyena (Crocuta crocuta)

or the scavenging black-backed jackal (Canis mesomelas)

based on previous reports of T. serialis in these species

(Hürni and Stiefal, 2003). Future work should identify the

deﬁnitive host and elucidate the risks for T. serialis infec-

tion in other primates. Anthropogenic habitat change may

increase geladas’ vulnerability to parasites, and changes

in host-parasite dynamics may put humans at risk for

emerging infectious diseases. The ecology of parasite-host

interactions in this region must be understood in order to

predict and control the spread of disease.

Conﬂict of interest

Fig. 3. A Female gelada with facial coenurus. Photograph by Dr. Jacinta

No personal or ﬁnancial relationships inﬂuenced this

Beehner. B Female gelada with mammary coenurus. Photograph by Dr.

Jacinta Beehner. research.

Please cite this article in press as: Schneider-Crease, I.A., et al., Molecular identiﬁcation of Taenia serialis coenurosis in a

wild Ethiopian gelada (Theropithecus gelada). Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.08.015

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Acknowledgements Dunbar, R.I.M., 1980. Demographic and life history variables of a pop-

ulation of gelada baboons (Theropithecus gelada). J. Anim. Ecol. 49,

485–506.

We thank the Ethiopian Wildlife Conservation Author-

Elek, S.R., Finkelstein, L.E., 1939. Multiceps serialis infestation in a baboon.

ity, the Simien Mountains National Park, and the University Report of a case exhibiting connective tissue cystic masses. Zoologica

24, 323–328.

of Michigan Gelada Research Project. We thank Alison Von

Hürni, H., Stiefel, S.L., 2003. Report on a Mission to the Simien Moun-

Striver, Caitlin Barale, Charles Nunn, Jacinta Beehner, James

tains National Park World Heritage Site, Ethiopia. University of Berne,

Flowers, Jenny Tung, Leslie Digby, and Paul Durst for their Switzerland, Report for NCCR North-South and the East & Southern

Africa Partnership Programme of the Centre for Development and

help in the ﬁeld, the laboratory, and during manuscript

Environment.

preparation, and the three anonymous reviewers for their

Jia, W.Z., Yan, H.B., Guo, A.J., Zhu, X.Q., Wang, Y.C., Shi, W.G., Chen, H.T.,

helpful comments. Research was approved by the Univer- Zhan, F., Zhang, S.H., Fu, B.Q., Littlewood, D.T., Cai, X.P., 2010. Complete

sity Committee on Use and Care of Animals (UCUCA no. mitochondrial genomes of Taenia multiceps, T. hydatigena and T. pisi-

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09554) at the University of Michigan, the University of

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Please cite this article in press as: Schneider-Crease, I.A., et al., Molecular identiﬁcation of Taenia serialis coenurosis in a

wild Ethiopian gelada (Theropithecus gelada). Vet. Parasitol. (2013), http://dx.doi.org/10.1016/j.vetpar.2013.08.015

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