Epizoochory, algae and the Australian eastern long-necked turtle Chelodina longicollis (Shaw).
The role of reptiles in seed dispersal has long been recognised (e.g., Beccaeri, 1890; Borzi, 1911), although Ridley (1930) was the first to acknowledge the role of turtles. All existing records of seed dispersal in turtles have been restricted to endozoochory (i.e., dispersal of seeds after passage through the vertebrate gut, cf, van der Piji, 1982). This has been documented in a range of species from various parts of the world including Europe (spurthighed tortoise Testudo graeca, Cobo and Andreu, 1988), Americas (gopher tortoise Gopherus polyphemus, Hayes and Corff, 1989, box turtle Terrapene carolina, Bruan and Brooks, 1987, Florida box turtle T. carolina bauri, Liu et al, 2004), Africa (leopard tortoise Geochelone pardalis, Milton, 1992), Galapagos Islands (giant tortoise T. elephantopus porteri, Rick and Bowman, 1961), Costa Pica (black river turtle Rhinoclemmysfunerea and brown wood turtle R. annulata, Moll and Jansen, 1995), Seychelles Islands (Aldabran giant tortoise Geochelone gigantea, Hnatiuk, 1978) and Australia (northern snapping turtle Elseya dentata, Legler, 1976; Kennett and Russell-Smith, 1993).
In comparison to endozoochoxy, the external dispersal of seeds by animals via attachment to the body, epizoochory (cf., van der Piji, 1982), has the potential to be transported greater distances, particularly when the individual host is unaware that the seeds' presence (Bullock and Primack, 1977). While seed could potentially be dispersed via epizoochory by both terrestrial and aquatic turtle species, there are limited reports of such seed dispersal (Smiths et al., 1989) and no records of freshwater turtles acting as vectors. Although not previously documented, the algae which grows on the carapace of some species of turtle may act as an anchor for the carriage of seeds.
Algae have been observed to grow on the carapace of many species of freshwater turtle (Hoffman and Tilden, 1930; Edgren et al., 1953; Walker et al., 1953; Ducker, 1957; Proctor, 1958; Chessman, 1978; Dalem, 1998) and may also occur on the head, tail and plastron (Edgren et al., 1953; Dalem, 1998). The most commonly recorded algae on turtles are the Basicladia species (Edgren et al., 1953; Ducker, 1957). The distribution and abundance of this alga is influenced by turtle behavioural patterns, for example basking, burrowing and hibernation, influence the distribution and abundance of resident algae, together with moulting, desiccation and available light (Proctor, 1958).
Of the three Australian species of freshwater turtles (Chelodina expansa, C. longicollis, Emydura macquarii) that Chessman (1978) studied, C longicollis supported the thickest algal coverage. This species has a geographic range that covers much of eastern and south-eastern mainland Australia, from Cape York Peninsula to eastern Victoria, including inland areas throughout the Murray-Darling Basin (Cann, 1998). Within its range, C. longicollis occupies a wide range of lotic and lentic water bodies (Cann, 1998), including deep flowing, permanent waterways (Chessman, 1984a, 1988; Kennett and Georges, 1990), but is also widespread in shallow, or ephemeral water bodies (Chessman, 1988), including farm dams (Wong and Burgin, 1997; Burgin et al., 1999). These common turtles have been estimated to reach densities of >1329 turtles/ha in farm dams (Ryan and Burgin, 2007), they have the greatest propensity for overland movement of any Australian freshwater turtle species (Parmenter, 1976; Chessman, 1984; Stott, 1987; Dalem, 1998) and have a predilection for ephemeral water bodies. For example, they have been observed to inhabit a newly filled ephemeral wetland within 4 d of its filling (Kennett and Georges, 1990). With these behavioural attributes, together with algal growth to trap and hold seeds, we hypothesised that C longicollis were a vector for seed dispersal.
The study was undertaken in 1995 within farm dams of the Eastern Creek Catchment, approximately 40 km north-west of Sydney (33[degrees]39'S-33[degrees]51'S; 150[degrees]45'E-150[degrees]53'E). Four dams (A-D, Table 1) were sampled from Apr. (early winter) to Sep. (early spring). Eleven additional dams (E-O, Table 1) were sampled in Sep. only. Each month, two unbaited fyke nets were set at randomly determined positions at the edge ([less than or equal to]5 m depth) of dams and left overnight. Netted turtles were collected the following morning and sexed (cf, Chessman, 1978), the carapace length measured and turtles were uniquely marked (cf, Cagle, 1939).
The density of algae on the carapace was recorded using a visual four-point scale. To initially develop the scale, turtles were placed in an aquarium with clear water to determine coverage and length of algae. Index 1 was designated as turtles with limited coverage, determined by the algae being insufficiently long to float above the carapace when the turtle was placed in water. Turtles were assigned to Index 2 if the algae were such that they floated above the carapace and coverage of the carapace was <80%. Turtles assigned to Index 3 had algae that were at least 2.5 cm long and the carapace had effectively 100% algal coverage. Turtles were assigned to Index 4 when they had a dense growth of algae over the carapace, with growth elsewhere on the body, such that the turtle was effectively camouflaged due to the algae length, density and coverage.
When captured, each turtle was carefully scanned for seeds caught in the algal. This occurred in the field before the turtles were released at their point of capture. Seeds were removed using forceps and those from each turtle were placed in a separate container. They were later air dried on the laboratory bench and identified to species under a dissecting microscope (x40 magnification). Identification was determined using the botanical resources of the laboratory. Representative seeds of each species were retained and photographed and identification checked by at least one of the resident botanists.
Chi-square test of association analysis was used to investigate the association between the independent variables turtle sex, turtle size, dam of capture and month of capture and the response variables carapacial algal mass index and seed species diversity. In addition, in dams that had been sampled over 6 too, the association between the independent response variables and the response variables presence/absence of seeds and seed species diversity were investigated. A Mann-Whitney U test was used to test seed species presence against size of turtle when the data did not fit the assumptions for the alternative analysis (Dytham, 2003).
Of the 158 Chelodina longicollis sampled, 90.5% supported epizoic carapacial growth of Basicladia rumulosa. Most of these had an intermediate algal mass index (34.2% Index 2, 38.6% Index 3), only 17.7% supported dense mass consistent with Index 4. Four turtles caught in Apr. or May and then recaptured four to five months later, showed an increase in algal presence of 1 to 2 indices, indicating that algal growth continued through winter. The only other recapture, a turtle caught in two successive months, showed no visual change in algal mass index. There was a lack of association between the algal mass index and sex ([chi square] 3 = 6.88), although there was an association between the algal mass index and turtle size ([chi square] 3, 0.001 = 15.49): larger turtles were more likely to carry greater coverage and density of algae than smaller turtles. There was also an association between the algal mass index and the dam of origin ([chi square] 9, 0.001 = 25.24).
Of the 101 turtles that were sampled between Apr. and Sep. (Dams A-D), 40.6% carried seeds trapped in the carapacial algae, whereas 11.8% (n = 41) of those from dams sampled only in early Sep. (Dams E-O) had seeds trapped in the algae (Table 2). Seeds of 10 species were collected from Chelodina longicollis: all plant species were closely associated with wetlands of the area, or were wetland obligates (Table 3).
The diversity of seed species was associated with month of sampling ([chi square] 3, 0.001 = 23.09): there was a decrease in species number between Apr. and Sep. There was also an association between dam of turtle capture and diversity of seed species ([chi square] 3, 0.001 = 36.61). The mean rank of turtle size and the seed species diversity were significantly different (Us = 2221, [n.sub.1] = 107, [n.sub.2] = 45, P < 0.001). For example, in one dam 84% (n = 31) of the turtles were observed to have seeds imbedded in their carapacial algae (Table 2), although smaller sized turtles tended to have a lower number of seed species. There was, however, a lack of association between seed species diversity and algal mass index ([chi square] 3 = 4.34) and between algal mass index and sex ([chi square] 1 = 0.068).
Approximately 90% of turtles carried sufficient algae (i.e., Indices 2-4) on their carapace to capture seeds. The number (10) of seed species captured in the algae of 158 Chelodina longicollis was broadly similar to that found in the turtle faeces of other studies. For example, seeds from 13 species were found in the faeces of 145 Terrapene carolina bauri from the lower Florida Keys that were sampled over a full year (Liu et al., 2004), 15 seed species from T. carolina (Braun and Brooks, 1987) and 11 species from Rhinoclemmys funerea (Moll and Jansen, 1995). Although there are reports that seed germination may be enhanced by the passage through the gut (e.g., Moolna, 2007), Moll and Jansen (1995) did not find evidence of enhanced germination among seeds defecated by R. annulata or R. funerea. Epizoochory in C. longicollis may, therefore, provide similar opportunities for seed dispersal as that of some herbivorous species of turtles that disperse seeds by endozoochory.
Seeds of all plant species except an introduced grass Paspalum dilatatum carried in the algae on Chelodina longicoUis occur in habitats associated with shallow, often ephemeral wetlands. Although this turtle species inhabits a wide range of water bodies, preferred habitats include shallow, often ephemeral wetlands of the flood plain (Chessman, 1988) and farm dams (Wong and Burgin, 1997; Burgin et al., 1999). It is also the most terrestrially mobile of the Australian turtles (Chessman, 1984). With these attributes, C. longicollis is likely to play a role in seed dispersal within and between water bodies.
Agnew and Flux (1970) suggested that epizoochory may be influenced by behaviour. Seeds are most likely trapped in the algal mat of turtles as they move in and out of water bodies. Chelodina longicollis are most active in spring and summer (Dalem, 1998). In this study, despite growth of algae during winter, seed species number diminished as winter progressed during the period of the year with lowest turtle activity (Chessman, 1978; Dalem, 1988). The results are, therefore, likely to be an underestimate of the level of seed capture. In the more active summer months, when animals migrate between water bodies, they are more likely to encounter the seeds of the water body's fringing vegetation and thus have a greater level of seed capture.
The number of animals carrying seeds at the time of the study may also reflect prevailing climatic conditions. During drought Chelodina longicollis congregate in permanent waters (Kennett and Georges, 1990; Ryan and Burgin, 2007) and disperse after rain (e.g., Kennett and Georges, 1990), potentially dispersing seeds to newly created/newly filled wetlands. Dalem (1988) found that there were low levels of movement (13%, n = 679) between dams during the period of the study. Subsequently, there has been an extensive drought in the area and towards the end of this drought period Ryan and Burgin (2007a, b) captured only 11.9% (n = 572) of the turtles first captured in the Dalem (1998) study. This indicated that a substantial proportion of the population had moved outside of the 2 km radius of the study area to more distant water bodies. Turtle movement and associated seed dispersal may, therefore, vary over time.
Agnew and Flux (1970) observed differences between male and female hares Lepus capensis in the level of epizoochory, however, such a difference was not associated with an individual's size. Conversely, male and female Chelodina longicollis were equally likely to carry seeds, although smaller individuals carried fewer species of seeds than adults. However, there has been no evidence that there is a difference in migration rate between the sexes, or between smaller animals (juveniles and sub-adults) and adult C. longicollis in the area (Dalem, 1998). It was concluded that the differences in epizoochory between male and female hares was due to sex-specific habitat difference (Agnew and Flux, 1970). The size structure of the population and sex ratio of (7,. longicollis may differ among water bodies (Dalem, 1998; Ryan and Burgin, 2007a, b), while the number of seed species captured in the algae growing on the carapace of turtles and the density of the algae, also differed among dams. Differences in epizoochory among turtles are, therefore, also likely to be linked to differences in the physical and biological characteristics of dams (e.g., nutrient status, turbidity, depth, available light).
No assessment of the viability of seed collected from Chelodina longicollis was undertaken in our study. However, all seeds carried by the turtles were associated with wetlands with water levels that fluctuated widely, dependant upon local climatic conditions. For example, species such as Gahnia sp., Scirpus sp. and Juncus sp. (Table 2) are fringing vegetation of wetlands, widely associated with ephemeral water bodies and/or those with widely fluctuating water levels. Seeds may therefore be fully immersed for long periods, whereas at other times the wetlands remain dry over an extended timeframe, sometimes for years. Based on the observation of Leck and Brock (2000) that many of the Australian plant species of temporary wetlands were amphibious (tolerant of flooding and drying), sometimes wet or dry for long periods, the time turtles spend out of water ([less than or equal to] 55 d, Dalem, 1998), is unlikely to impact on the germination potential of these fringing wetland species.
It has previously been acknowledged that freshwater turtles, including Chelodina longicollis, play an important role in the water quality of aquatic systems (Thompson, 1993), although their role in ecosystem functioning more broadly has had limited attention. Since they are common (e.g., full census of one farm dam revealed 370 [ha.sup.-1]--Burgin et al, 1999; maximum estimated population size >1329 turtles/ha in farm dams--Ryan and Burgin, 2007a) and move among effectively the full range of freshwater habitats across much of eastern Australia, (e.g., river habitat--Thompson, 1993; dune lakes--Kennett and Georges, 1990; farm dams--Burgin et al., 1999), we assume that they play an important role in the dispersal of seed across aquatic habitats by epizoochory.
Freshwater turtles are known to be endozoochronic seed dispersers (e.g., Cobo and Andreu, 1988; Hayes and Corff, 1989; Milton, 1992; Liu et al., 2004). It is, therefore, likely that freshwater turtles are an important component of ecosystem functioning, whether they disperse the seeds in the algal growth on their carapace or by passing the seeds through the gut, as they move among or within water bodies they clearly have adaptations to also disperse seed.
Acknowledgments.--The contribution of Ms. Judith Betts and Mr. Steve Emerton in the fieldwork is acknowledged. We are also grateful to Debbie Rae and two anonymous reviewers who provided editorial comments.
SUBMITTED 15 AUGUST 2007 ACCEPTED 19 DECEMBER 2007
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SHELLEY BURGIN (1) AND ADRIAN RENSHAW
College of Health and Science, University of Western Sydney, Locked Bag 1797, South Penrith Distribution Centre,
New South Wales 1797
(1) Corresponding author: Telephone: +61 (245)701-209; FAX: +61 (245)701-403; e-mail: s.burgin@ uws.edu.au
TABLE 1.--Brief description of dams sampled for investigation of epizoochrony in Chelodina longicollis in north-western Sydney, Australia between Apr. and Sep. 1995 Dam identification Brief description A Emergent vegetation surrounding perimenter. Riparian zone overgrazed by horses. B Partially blanketed in Lemna minor. No emergent vegetation. Riparian zone predominantly Paspalum dilatatum. Irrigation source for local market gardens. C Emergent vegetation. Riparian zone overgrazed by horses/cattle. D No emergent vegetation. Surface blanketed in L. minor. Adjacent land use market gardens and grazing. E Encircled by high earthen levee ('turkey nest dam'). Limited emergent aquatic vegetation. Riparian zone market gardens and grazing. F No emergent vegetation. Overgrazed riparian zone. G No emergent vegetation. Overgrazed riparian zone. H Turkey nest dam with some trees, shrubs and grasses on the bank. No emergent vegetation. Riparian zone grazed. I Received effluent from chicken processing plant. No emergent vegetation. Riparian zone grazed by cattle. J Steep sided, turkey nest dam. Extremely hard clay walls. No emergent vegetation. K Limited emergent vegetation. Grove of trees with sparse ground cover in riparian zone of dam. Area used for cattle grazing and fire wood storage. L Turkey nest dam. No emergent plants, some submerged plants. Riparian zone overgrazed by horses. M Turkey nest dam with banks covered with grass, shrubs, trees. Submerged/emergent plants. Market gardens in riparian zone. N No emergent vegetation. Sheep grazing and market gardens in riparian zone. O Turkey nest dam with high walls. Trees, shrubs and grasses on banks and adjacent. Undergrowth remnant natural vegetation and open area. TABLE 2.--Number of Chelodina longicollis with seeds in their capracial algae, together with seed species number, in farm dams. Dams A-D sampled Apr. to Sep. 1995, E-O sampled in Sep. only Number of Number of Number of turtles seeds Dam ID turtles with seeds species/dam A 33 9 6 B 14 3 3 C 31 26 10 D 24 3 3 E 2 0 0 F 2 1 1 G 13 0 0 H 2 2 1 1 4 1 2 5 0 1 K 9 0 0 L 1 0 0 M 4 2 2 N 14 0 4 O 0 0 -- Total 158 55 TABLE 3.--Seeds retrieved from the carapacial algae of Chelodina longicollis captured from farm dams in South Creek catchment, north-western Sydney (notes from Sainty and Jacobs, 1981 except where otherwise indicated) Taxon Description Baumea sp. 'Twig rush', native perennial, coastal lagoons, swamps, standing water <1 m deep. Gahnia sp. 'Sawsedge', native, creek banks or beds of ephemeral swamps. Potamogeton sp. 'Pondweed', floating annual or perennial, tolerant of brackish water. Eleocharis sp. 'Spikerush', native, perennial, in or alongside waterways. Elocharis acula As other Eleocharis species. Scirpuis sp. 'Clubbush', native, submerged or terrestrial perennial, emergent, favours fast flowing clear streams, water <1 m deep. Sagittaria graminea 'Arrowhead' introduced from North America, emergent, aquatic, perennial herb. Juncus sp. 'Rush' rhizomatous, annual or perennial, most occur in periodically damp areas. Polygonum sp. 'Knotweed', erect or floating annual or perennial herb, margins of lagoons, swamps and channels. Paspalum dilatatum Grass, leaves arising from culms, 40-175 cm tall. Rhizomatous, perennial, introduced, important summer grass for stock (Wheeler et al., 1982). Common locally terrestrially and encroaching on water bodies (pers. obs.).
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|Author:||Burgin, Shelley; Renshaw, Adrian|
|Publication:||The American Midland Naturalist|
|Date:||Jul 1, 2008|
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