Elsey, 2005

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Comp. Parasitol. 72(2), 2005, pp. 241–244

Research Note

Euhirudinea from Australian Turtles (Chelodina burrungandjii and Emydura australis) of the Kimberley Plateau, Western Australia, Australia ANTON D. TUCKER,1,2,4 NANCY N. FITZSIMMONS,2

AND

FREDERIC R. GOVEDICH3

1

Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, Florida 34236, U.S.A. (e-mail: tucker@mote.org), 2 Applied Ecology Research Group, University of Canberra, Belconnen, ACT 2601, Australia (e-mail: fitzsimm@mote.org), and 3 School of Biological Sciences, Monash University, Clayton, VIC 3800, Australia (e-mail: fredric.govedich@sci.monash.edu.au)

of leech burden for turtle hosts from a comprehensive demographic sample of turtles in the survey area. Annual collecting trips coincided with the dry season in mid- to late-austral winter (June through August) from 1999 to 2004. Turtles were collected from 9 major rivers of the Kimberley Plateau by snorkeling or with baited traps (Table 1). As turtles were marked and measured, leeches were removed from the turtle carapace, inguinal region, or neck, and all turtles were released alive at the original point of capture. Leeches were relaxed in water for 12–24 hr, preserved in 70% ethanol, and identified with reference to a comprehensive collection of Euhirudinea specimens from Australia. Voucher specimens were deposited in the Western Australian Museum, Perth, Western Australia, Australia. Two sites (Drysdale and Isdell Rivers, in the East and West Kimberley Plateau, respectively) were sampled intensively during an ongoing annual mark–recapture study of turtles. From these large samples of turtles, a more detailed analysis of host– parasite dynamics was possible. For these sites, we quantified the presence or absence of Placobdelloides octostriata (Grube 1866) by host taxon, and in 2004, we collected parasite abundance data from individual turtles. A classification and regression tree analysis (De’ath and Fabricus, 2000) was conducted to represent a simplified model of parasitism, derived from leech prevalence by host species, river, host sex (immature, male, female), and host size (in cm straight carapace length). Leeches were detected on turtle hosts from 7 of 9 rivers (Table 1). Placobdelloides is a common leech parasitizing a variety of aquatic vertebrates including turtles and crocodilians (Forrester and Sawyer, 1974; Brooks et al., 1990; Dodd, 1992; McKenna et al., 2005), and P. octostriata was collected from both C. burrungandjii and E. australis. Bogobdella diversa (Richardson 1969) was recorded from a single female

ABSTRACT: Leeches were sampled from 2 turtle species, Chelodina burrungandjii and Emydura australis, from 9 rivers spanning the Kimberley Plateau of Western Australia, Australia. Placobdelloides octostriata was collected from both turtle taxa across the Kimberley Plateau, and Bogobdella diversa was collected from a single specimen of E. australis in the Fitzroy River, the westernmost catchment of the sample area. Relative prevalence of P. octostriata was influenced by host behavior, with a 10-fold difference in prevalence on the sit-wait predator C. burrungandjii (37.4–42.2%) in comparison with the more actively swimming E. australis (1.3–3.7%). The prevalence of parasitism was not substantially different between sites for each species. These are new host and locality records for Euhirudinea in Australia. KEY WORDS: Leech, Euhirudinea, turtle, Chelodina, Emydura, Placobdelloides, Bogobdella, Kimberley Plateau, Western Australia, Australia.

The parasitic fauna of the aquatic vertebrates of Australia is poorly known, particularly in more remote regions of the continent. Where surveys exist, few report the size, age, or sex of hosts examined, although these data are ecologically informative. The study reported in this article is the first survey of parasitic leeches on the sandstone snake-necked turtle, Chelodina burrungandjii, and the north-west red-faced turtle, Emydura australis, from the Kimberley Plateau of northern Western Australia, Australia. The distributions of E. australis and C. burrungandjii are strongly delineated for the Kimberley region (Georges and Adams, 1996; Thomson et al., 2000; Georges et al., 2002), bounded by eastward drainages into the Joseph Bonaparte Gulf and by the Fitzroy River catchment flowing into King Sound to the west. This study examines the correlates

4

Corresponding author. 241


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COMPARATIVE PARASITOLOGY, 72(2), JULY 2005

Table 1. Sample sizes for each of 2 freshwater turtle species, Chelodina burrungandjii and Emydura australis, collected from 9 rivers of the Kimberley Plateau, Western Australia, Australia. Sample size Locality

E. australis

C. burrungandjii

Coordinates

Ord River Pentecost River* Durack River Drysdale River* Carson River* Mitchell River* King Edward River* Isdell River* Fitzroy River*

31 35 36 1,028 36 34 113 678 46

1 3 4 116 6 22 9 125 16

158479170S; 128844950E 158589300S; 127857950E 158509120S; 1278249350E 158409550S; 1268249120E 14827990S; 1268399380E 148499470S; 1258419150E 148549220S; 126812920E 1781930S; 1258139390E 188149250S; 1258329590E

Total

2,037

302

* Leeches parasitized sampled turtles in these sites.

E. australis in the Fitzroy River, the westernmost catchment sampled. Bogabdella diversa is 1 of the few freshwater leeches with gill branchiae and the only species in Australia with this distinctive feature. As an understudied species, genus, and family, it may have a wider distribution than currently reported in Australia (Govedich, 2001). Distributional data are fragmentary for the Australian leech genera, particularly across the northern rivers. The closest reported distribution is based on leech specimens found on pignose turtles, Carettochelys insculpta, and saltwater crocodiles, Crocodylus porosus, in the Daly River, Northern Territory (Saumure and Doody, 2000), Queensland (McKenna et al., 2005), and Malaysia (Govedich et al., 2002). There was a 10-fold difference in prevalence between the sit-wait predator C. burrungandjii (37.4–42.2%) and the more actively swimming E. australis (1.3–3.7%), even though the incidence of parasitism was not substantially different between sites for each species (Table 2). Individual E. australis hosted from 1 to 8 leeches, whereas individual C. burrungandjii hosted up to 130 leeches. A full classification and regression tree extracted most of the useful information after the first 3 nodes,

so a pruning method by cross-complexity penalization function (Breiman et al., 1984) was used to produce a simplified tree for interpretation (Fig. 1). The first branch separates leech burden by host species with an overall low parasite burden for E. australis (0.1) at the first terminal node regardless of river or sex. For C. burrungandjii, the second branch separates leech burden among rivers. Within the Isdell River, modest differences in parasite burden were apparent between females (7.0) and the immatures (3.2), with males intermediate in parasite burdens (5.4). Leech burden was separated by host maturity status within the Drysdale River. There was no difference in parasite burden among adult males and females (14.2 and 17.5, respectively), but adults averaged twice the burden of immature turtles (8.0). Seasonal differences in temperature and water flow may influence turtle activity and thus the opportunity for leech colonization (Koffler et al., 1978; Graham et al., 1997). In this study, leech prevalence on C. burrungandjii was correspondingly lower during warmer water temperatures in 2003 than during cooler water temperatures in 2002 and 2004 (Table 2). A similar thermal relationship might be inferred

Table 2. Prevalence* of Placobdelloides octostriata on 2 turtle hosts, Emydura australis and Chelodina burrungandjii, surveyed from the Isdell River, West Kimberley Plateau, and Drysdale River, East Kimberley Plateau, Western Australia, Australia in 2002–2004. Isdell River Year 2002 2003 2004 Overall

E. australis 6.1% 0.5% 5.5% 3.7%

(9/148) (1/218) (11/199) (21/565)

Drysdale River C. burrungandjii 44.7% 28.9% 57.6% 42.2%

(17/38) (13/45) (19/33) (49/116)

E. australis 0.0% 0.4% 5.5% 1.3%

(0/191) (2/565) (10/182) (12/938)

* Percent prevalence followed parenthetically by the ratio of infected/sampled individuals. Emydura australis is an active predator; C. burrungandjii is a sit-and-wait predator.

C. burrungandjii 83.3% 12.3% 66.6% 37.4%

(10/12) (7/57) (20/30) (37/99)


RESEARCH NOTES

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Figure 1. Classification and regression tree showing the effects of host species, carapace length, sex, maturity, and sampling locality on the intensity of parasitism by Placobdelloides octostriata on Emydura australis and Chelodina burrungandjii from the Kimberley Plateau, Western Australia, Australia. (Partitioned prevalence values are shown parenthetically.)

across years for E. australis for the Isdell River but was not evident in the Drysdale River. Furthermore, host–parasite relationships may shift ontogenetically as chelonians grow and visit different microhabitats (Cann, 1998): larger females of C. burrungandjii were more heavily parasitized than the smaller males or immature animals (Table 3). In contrast, there was

no outstanding evidence of increasing parasite burden with increasing size for E. australis. Fieldwork was conducted with permits from the Western Australia Department of Conservation and Land Management, animal ethics permits from the University of Canberra, and through research agreements with traditional owners among the

Table 3. Prevalence* of Placobdelloides octostriata among 3 age–size classes of 2 turtle species, Emydura australis and Chelodina burrungandjii, from the Isdell and Drysdale Rivers of the Kimberley Plateau, Western Australia, Australia in 2002–2004. Isdell River

Drysdale River

Age–size

E. australis

C. burrungandjii

E. australis

C. burrungandjii

Female Male Immature

2.3% (5/216) 5.3% (9/171) 3.9% (7/178)

51.1% (22/43) 45.1% (23/51) 18.2% (4/22)

2.0% (8/400) 1.0% (3/297) 0.4% (1/241)

42.9% (18/42) 35.3% (12/34) 30.4% (7/23)

* Percent prevalence followed parenthetically by the ratio of infected/sampled individuals.


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COMPARATIVE PARASITOLOGY, 72(2), JULY 2005

Wunambal-Gamberra people. Field support came from the University of Canberra Applied Ecology Research Group, Mote Marine Laboratory, Earthwatch Institute, a Rio Tinto Global Partnership Grant, and a Joyce Vickery Grant from the Linnean Society of New South Wales. We thank Bonnie Bain and Dennis Richardson for their comments on early drafts of the manuscript. LITERATURE CITED Breiman, L., J. H. Freieman, R. A. Olshen, and C. G. Stone. 1984. Classification and Regression Trees. Wadsworth International Group, Belmont, California. 358 pp. Brooks, R. J., D. A. Galbraith, and J. A. Layfield. 1990. Occurrence of Placobdella parasitica (Hirudinea) on snapping turtles, Chelydra serpentina, in southeastern Ontario. Journal of Parasitology 76:190–195. Cann, J. 1998. Australian Freshwater Turtles. Beaumont Publishing, Singapore. 292 pp. De’ath, G., and K. E. Fabricus. 2000. Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81:3178–3192. Dodd, C. K., Jr. 1992. Patterns of distribution and seasonal use of the turtle Sternotherus depressus by the leech Placobdella parasitica. Journal of Herpetology 22: 74–81. Forrester, D. J., and R. T. Sawyer. 1974. Placobdella multilineata (Hirudinea) from the American alligator in Florida. Journal of Parasitology 60:673. Georges, A., and M. Adams. 1996. Electrophoretic delineation of species boundaries within the shortnecked freshwater turtles of Australia (Testudines:Chelidae). Zoological Journal of the Linnean Society 118: 241–260. Georges, A., M. Adams, and W. McCord. 2002.

Electrophoretic delineation of species boundaries within the genus Chelodina (Testudines:Chelidae) of Australia, New Guinea and Indonesia. Zoological Journal of the Linnean Society 134:401–421. Govedich, F. R. 2001. A reference guide to the ecology and taxonomy of freshwater and terrestrial leeches (Euhirudinea) of Australasia and Oceania. Identification Guide No. 35, CRC for Freshwater Ecology, Albury, New South Wales, Australia. 67 pp. Govedich, F. R., B. A. Bain, and R. W. Davies. 2002. Placobdelloides stellapapillium sp. nov (Glossiphoniidae) found feeding on crocodiles and turtles. Hydrobiologia 474:253–256. Graham, T. E., R. A. Saumure, and B. Ericson. 1997. Map turtle winter leech loads. Journal of Parasitology 83:1185–1186. Koffler, B. R., R. A. Seigel, and M. T. Mendonca. 1978. The seasonal occurrence of leeches on the wood turtle, Clemmys insculpta (Reptilia, Testudines, Emydidae). Journal of Herpetology 12:571–572. McKenna, S. A., D. A. Betts, W. W. Pong, F. R. Govedich, and D. P. Barton. 2005. A redescription of the Australian leech Placobdelloides bancrofti with new records of its distribution. Journal of Parasitology. 91:117–121. Richardson, L. R. 1969. The family Ozobranchidae redefined, and a novel ozobranchiform leech from Murray River turtles (class Hirudinoidea; order Rhynchobdelliformes). Proceedings of the Linnean Society of New South Wales 94:61–80. Saumure, R. A., and J. S. Doody. 2000. Carettochelys insculpta: ectoparasites. Herpetological Review 31: 237–238. Thomson, S., R. Kennett, and A. Georges. 2000. A new species of long-necked turtle (Testudines: Chelidae) from the Arnhem Land Plateau, Northern Territory, Australia. Chelonian Conservation and Biology 3: 675–685.


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