cladophoroid green alga Basicladia chelonum was common on the shell of both. Blanding's and snapping turtles and also present on the head and tail of the ...
Epizoic Algae from Freshwater Turtles in Nova Scotia D.J. Garbary Department of Biology, St. Francis Xavier University Antigonish, Nova Scotia, Canada, B2G 2W5 and G. Bourquea, T.B. Herman, and JA McNeil Department of Biology, Acadia University Wolfville,
Nova Scotia, Canada, B4P 2R6
ABSTRACT Nineteen Blanding's turtles (Emydoidea blandingii), eight snapping turtles (Chelydra serpentina) and fourteen painted (Chrysemys picta) turtles trapped in Nova Scotia in 2005 were examined for epizoic algae. Algae were macroscopically apparent on 14 Blanding's and seven snapping turtles; microscopic examination of material scraped from various surfaces of these turtles revealed the predominance of two algal taxa. The cladophoroid green alga Basicladia chelonum was common on the shell of both Blanding's and snapping turtles and also present on the head and tail of the latter. B. chelonum is reported for the first time in Canada east of Ontario. A filamentous cyanobacterium, Komvophoron sp., formed extensive colonies solely in the leg bases of Blanding's turtles, where B. chelonum was absent. Although the nature of the interaction is unknown, this is the first potential symbiQsis between a cyanobacterium and a turtle. Examination of a historical (2001-05) photographic database for Blanding's turtle in Nova Scotia revealed a colonization rate of 10% for B. chelonum and 46% for Komvophoron sp. It also revealed population and age-specific differences in frequency of the two algal taxa on Blanding's turtles.
., ,,'
INTRODUCTION In addition to being planktonic, freshwater algae occupy a wide variety of benthic habitats (Round 1981, Burkholder et al. 1996, Graham and Wilcox 2000). Substrata include a diverse mix of biological and non-biological surfaces. Among the most unusual of these substrata is the surface of turtles, from which algae have been described for at least 100 years (Collins 1907). A diversity of algae has been described associated with freshwater turtles (e.g., Yoneda 1952, Edgren et al. 1953, Dixon 1960, Belusz and Reed 1969). To date, only species of the chlorophyte genus Basicladia (Cladophorales) have been recognized as occurring regularly on freshwater turtles; this relationship has been hypothesized as symbiotic and coevolved (see Edgren et al. 1953, Neil and Allen 1954 for discussion). The filamentous, green algal genus Basicladia is primarily epizoic on freshwater turtles. Of the five species assigned to the genus, only one species, B. vivipara has not been recorded on turtles. A further species, Cladophora kosterae (originally assigned to the section Basicladia of Cladophora) was described from benthic substrata, and this species has since been reported on turtles (Belusz and Reed 1969).This species should be formally assigned to Basicladia based on morphology (van den Hoek 1963) and molecular data (Yoshii et al. 2004). Two species, B. chelonum and B. crassa, are widely distributed.whereas the distributions of B. ramulosa,B. sinensis and B. vivipara are poorly known and highly restricted geographically (Smith 1950, Ducker 1958, Normandin and Taft 1959). Basicladia was formally reported from Canada in Ontario; however, the species was not identified (Colt et al. 1995). Later, Krawchuk et al. (1997) also reported aCurrent address: Departement de Sciences biologiques, Universite de Montreal, Montreal, Quebec, Canada, H3C 3J7 677 Journal of Freshwater
Ecology, Volume 22, Number 4 - December 2007
colonization of turtles by green algae in Ontario; this material was likely Basicladia. An initial collection of small fragments of Basicladia sp. from several turtles in June 2005, near Kejimkujik National Park and National Historic Site of Canada (KNP) in southwestern Nova Scotia, suggested that additional sampling later in the season would reveal more definitive material. These later collections showed Basicladia to be common, and also revealed a second alga (Komvophoron sp.) commonly associated with the turtles. This second alga was a cyanobacterium, and although cyanobacteria have been recorded from turtle substrata (e.g., Yoneda 1952, Edgren et al. 1953, Dixon 1960, Senties et al. 1999), none of these represents a regularly occurring symbiosis. We examined the occurrence and location of Basicladia and Komvophoron on three native species of turtle in southwestNova Scotia Blanding's turtle, common snapping turtle and painted turtle. Algae were previously described from these hosts (e.g., Walker et al. 1953, Proctor 1958). Snapping and painted turtles are common and widespread throughout southwest Nova Scotia (Gilhen 1984); Blanding's turtle is 'Endangered' in Nova Scotia (COSEWlC: Committee on the Status of Endangered Wildlife in Canada 2005) and is restricted to three small disjunct populations in the southwest part of the province (Herman et al. 1995, Mockford et al. 2005). Although all three turtle species inhabit humic freshwater systems in the area, they differ in both ecology and behavior. In particular, Blanding's and painted turtles bask and move terrestrially to a greater extent than do snapping turtles, creating differences in light and hydric regimes among the three species.-Such differences may be reflected in the epizoic algal flora. "
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MATERIALS AND METIIODS Blanding's turtles, snapping turtles and painted turtles were live-trapped in hoopnet traps baited with sardines (McMaster and Herman 2000). Sampling occurred in southwest Nova Scotia from July 8 to 13,2005 near the communities ofKempt, Harmony and Lakeview, just east ofKNP (44°24' N 65°04' W). Captured adult and juvenile turtles were closely inspected for presence of algae. When present, samples of algae were gently scraped from the turtle with a scalpel blade; the original location of each sample on the turtle was noted, and samples were stored separately in 70 % ethanol. Portions of the preserved samples were pipetted onto slides and stained with 1% phloxine B for I min. Excess stain was removed from the slide with a tissue, and a solution of 50% clear corn syrup and 5% formalin in distilled water was used as the mounting medium for preparation of permanent slides. Following partial dehydration of the mounting medium, additional liquid was added, and coverslips were ringed with nail polish. Slides are archived in the herbarium of St. Francis Xavier University (STFX). Basicladia chelonum was identified based on the original description of Collins (1907) and later accounts in Hoffinann and Tilden (1930), Smith (1950) and Wehr and Sheath (2003). Our cyanobacterial material was identified as Komvophoron sp. (Komarek", personal communication). This generic name is used based on description by Anagnostidis and Komarek (1988) and Komarek et al. (2003). Without additional study (i.e., culturing and molecular analysis) more precise identification of this cyanobacterium is not possible (Komarek 2006). After gaining familiarity with the macroscopic features of B. chelonum and Komvophoron sp., we examined photographs of 168 additional Blanding's turtles (comprising more than 50% ofthe known populations in Nova Scotia) from the permanent photographic database of the Blanding's Turtle Recovery Team for obvious presence of either algal form. These photographs were taken between 2001 and 2005 in the three known Blanding's turtle populations in southwest Nova Scotia (Mockford et al. "Institute of Botany, Trebon and University of South Bohemia, Czech Republic
678
2005), and although photographs may not be definitive for either species, the thin coating resulting ftom growths of Komvophoron sp. was easily distinguished ftom the much larger, more in relief, clumps of B. chelonum. False negative data (i.e., the non-detection of algae when they are present) are expected. RESULTS Nineteen Blanding's, eight snapping and fourteen painted turtles were inspected for epizoic algae (Table 1). Algae were macroscopically apparent on 14 Blanding's and seven Snapping turtles; all painted turtles appeared to lack epizoic algae. Microscopic examination of material scraped ftom various surfaces of the turtles with apparent algae revealed the predominance of two algal taxa, differing in the host and location on the host colonized. Basicladia chelonum (Fig. 1) occurred on two host species. On the Blanding's turtle, it appeared to be restricted to the carapace; whereas, on the snapping turtle, it occurred on the carapace, head and tail. Komvophoron sp. was apparent only on Blanding's turtles and was most evident on the skin at the base of the fore and hind legs. Basicladia chelonum occurred as an irregular turfto scattered clumps to about I cm high. Erect axes were poorly to commonly branched and varied ftom long unbranched axes to filaments where numerous short lateral branches occurred (Fig. lA). Occasional opposite branching occurred forming trichotomies. Cells varied ftom 18-50 J.lmin diameter and 40 to> I000 J.lmin length, with cell walls 2.5-8.0 J.lmthick. Basal cells in erect axes were the largest, although lengtfi 'quickly declined farther up the branch. The basal system formed a crustose layer (Fig 1B) in which the filamentous organization was somewhat obscured because ofthe tight packing of the cells (Fig. Ie). Sporangia were formed through the differentiation of vegetative cells and even apical cells may form sporangia (Fig. 1D). Erect axes had numerous sporangia, and these formed indistinct rows or were scattered among the vegetative cells. There was no apparent synchrony of reproduction on a given thallus, with fully released sporangia occurring adjacent to early stage sporangia or even apparently undifferentiated vegetative cells. Sporangia typically had a single, well-developed pore, and this developed well before spores were mature, and even prior to cytoplasmic cleavage. We did not observe flagella on the spores, although the non-living state of the thalli and alcohol preservation may have caused shedding of flagella. At the species level, our material is problematic. Cell diameters are the primary diagnostic features distinguishing the two North American species of turtle algae. The Nova Scotia material seems intermediate between B. chelonum and B. crassa as described by Hoffinan and Tilden (1930) with cell sizes slightly larger than the former but never approaching the typical range of the latter. It may be that only a single variable species is represented in the B. chelonum/B. crassum complex. Although B. chelonum was common on both Blanding's and snapping turtles, the
Table 1. Algal incidence, from field assessment of captured turtles and subsequent microscopic examination of algal samples, according to host species and location on host. Sample size for each category given in parentheses. Host species Blanding's
Total algal incidence 0.74 (19)
Snapping
0.88 (8)
Painted
0.00 Qi)
Location on host Leg base (4) Carapace (9) Carapace (8) Head (2) Tail (3) nla 679
Basicladia chelonum 0.00 1.00 0.88 1.00 1.00 nla
Komvophoron sp. 1.00 0.00 0.00 0.00 0.00 nla
most luxuriant growth occurred on snapping turtles, in some cases covering nearly the entire carapace. On this host the B. chelonum thalli were more developed and were accompanied by a more diverse algal flora. In addition, B. chelonum colonized the head and tail of the snapping turtles, whereas this was never observed on the Blanding's turtles where the species was only found on the carapace (Table 1). This algal flora included numerous epiphytic diatoms and entangled fragments ofthe filamentous green algae in the genera Mougeotia, Spirogyra, Oedogonium and Stigeoclonium. Occasional cells of the desmid genera Staurastrum, Euastrum, Pleurotaenium, and Closterium were also present. Although additional algal forms were present, the bleaching in the fixative and
c
E Figure 1. Basicladia chelonum. A- Portion of upper filaments showing several short lateral branches (scale = 200 11m).B- Portion of basal cmst irregular shaped cells and several erect axes (scale = 50 Ilm). C- Portion of basal system showing highly irregular
shaped cells and filamentous
organization
obscured
(scale
= 50
/lm). D- Immature small sporangium from upper portion of filament with cytoplasmic cleavage and well-developed exit pore (scale = 20 Ilm). ETerminal cell of filament differentiated into sporangium with many spores that have not yet been released (scale = 25 11m).
680
subsequent staining with phloxine B precluded identification. Virtually all filaments of B. chelonum had numerous stalked, vorticellid protozoans. Komvophoron sp. (Fig. 2) occurred as colonies up to several cm in diameter at the bases ofthe forelimbs and hind limbs of Blanding's turtles. The colonies were light green and thin. In the resulting scrapings, the filaments were both superficial and apparently embedded on and around host epidermal cells (Fig. 2A and 2B). Filaments were unbranched and mostly 50-150 !lm long and straight to irregularly curved with no regular alignment in the colony mass. Filaments were ftagile and slide preparation produced many short filaments ftee in the mounting medium. Intercalary cells were about 2 !lm in diameter and 2-4 !lm in length (Fig. 2C). Filaments had attenuated terminal cells with slightly rounded to pointed apices (Fig. 2D). Cells showed slight constrictions at the crosswalls. Cell contents were somewhat granular, although there was no alignment of particles along the crosswalls. A colorless sheath, about 0.5 !lm thick, was present. Based on the examination of the Blanding's turtle photo database, the incidence of both algal species varied by host population, and in some populations by host age (Table 2); no sex-related patterns were observed. Two age-related patterns were obvious. B. chelonum occurred more commonly on juveniles than adults, but only in Pleasant River. Conversely, Komvophoron sp. occurred more commonly on adults than juveniles, but only in KNP. Additionally, in all populations, the incidence of Komvophoron sp. was higher than that of B. chelonum. The incidence of both algal species was highest at
B
. c
0
Figure 2. Komvophoron sp. A- Irregularly arranged filaments and host epidermal cell (hc) (scale = 25 !lm). B- Irregularly arranged filaments associated with host cell (hc) (scale = 20 !lm). C- Broken portion of filament without end cells showing welldefined barrel shaped cells and slight constrictions at cross walls (scale = 20 flm). D- Single whole filament with tapered terminal cells (scale = 20 !lm). 681
McGowan Lake and lowest at KNP. In fact, despite a high sample size of hosts, B. chelonum was absent trom the KNP sample. DISCUSSION This is the first report of Basicladia in Canada east of Ontario, where the genus was previously reported (Colt et at. 1995, Krawchuk et al. 1997). Since neither of these papers provided descriptions or illustrations, the species represented in their collections is unknown. The nearest geographic record of Basicladia to Nova Scotia is trom Maine (Chute 1949), where B. chelonum was reported trom the musk turtle (Stenotherus odoratus). Literature records suggest that Basicladia can be expected throughout the eastern and southern portions of the USA and central Canada (if not globally) wherever treshwater turtles are present (e.g., Proctor 1958, Prasad and Jain 1973, Ziglar and Anderson 2005). Given the high trequency of B. chelonum on snapping and Blanding's turtles in southwest Nova Scotia, it is reasonable to assume that Basicladia will be found throughout eastern Canada where the snapping turtle is prevalent. From the characterization of the different species to the naming ofthe appropriate genus, the taxonomy and nomenclature of Basic!adia are problematic. Collins (1907) described the first turtle alga as Chaetomorpha chelonum. Hoffman and Tilden (1930) described B. crassa, and named it the type species of the new genus Basicladia. Van den Hoek (1963) later reduced Basicladia to a section of Cladophora; however, he did not formally transfer any of the species into~Cladophora. In addition, the wrong species (Le., B. chelonum) was indicated as the type of the genus. Consequently, Cladophora section Basicladia has no nomenclatural standing, even though the species fall within van den Hoek's concept of the genus. Thus, while van den Hoek's morphological concept of the genus Cladophora as including Basicladia may be reasonable, Cladophora is a polyphyletic grouping that includes several well-characterized genera (Leliaert et al. 2003). Cladogram topology suggests that Basicladia will be maintained as a generic segregate within a multigeneric Cladophoraceae ,fYoshii et al. 2004).
Table 2. Incidence of Basicladia chelonum on carapace and Komvophoron sp. on leg base of male, female, andjuvenile Blanding's turtles trom three populations in Nova Scotia, from photo database assessment. Sample size for each category is given in parentheses. Abbreviations:KNP = Lejimkujik National Park and National HistoricSite of Canada(44°23'N,65°13'W);MG = McGowanLake (44° 26'N, 65°04'W);PR = PleasantRiver (44°25'N,64°53'W). Population Sex/Age Basicladia chelonum Komvophoron sp. KNP Male 0.00 (16) 0.27 (15) Female 0.00 (17) 0.35(17) 0.00 (18) Juvenile 0.00 (18) Total 0.00 (51) 0.20 (50) MG Male 0.19 (21) 0.70 (20) Female 0.21 (24) 0.63 (24) Juvenile 0.18(11) 0.70(10) Total 0.20 (56) 0.67 (54) PR Male 0.00 (I 8) 0.60 (IS) Female 0.00 (17) 0.44 (I 6) Juvenile 0.26 (19) 0.40 (15) Total 0.09 (54) 0.48 (46) TOTAL 0.10 Q212 0.46 n~°2. 682
Arif (1991) found two cyanobacteria associated with freshwater turtles in Saudi Arabia, which he referred to as Lyngbya epiphytica and L. majuscula. Neither of these species resembles the material we collected from Blanding's turtles in Nova Scotia. Yoneda(1952) referred to Oscillatoria brevis as part of the epizoic biota on turtles from Japan, but this species is also not our entity. Similarly Dixon (1960) described several genera of filamentous cyanobacteria (Trichodesmium, Lyngbya, and Oscillatoria) on the skin of the tail and hind limbs of turtles from Texas and Mexico; however, none of these is the equivalent of Komvophoron sp. described here. There is precedence for Komvophoron being associated with animal substrata. Turon et al. (1991) described a new species,K. bourrellyi, as an epibiote from the Mediterranean Sea where it was associated with two species of ascidians. K. bourrellyi grows on the surface of the animals in small grooves and irregularities. Although cell sizes are similar, K. bourrellyi lacks the tapered end cells characteristic of our material. The presence of Komvophoron on many of the Blanding's turtles and its absence in the two other turtle species suggest that this is more than a random occurrence of the cyanobacterium; additional observations are required to determine the nature of the interaction. The degree of intimacy between algae and freshwater turtles is unclear. The least intimate association would be a commensal relationship in which the turtle only provides a substrate and/or means of dispersal for the algae. Alternatively, the relationship may be more symmetric if the alga provides the tuttle with camouflage from potential prey and predators (Neil and Allen 1954, Dixon 1960, Ziglar and Anderson 2005). Algae may also benefit turtles by serving as a supplemental food source; Krawchuk et al. (1997) reported feeding by painted turtles on algae epizoic on snapping turtles in Ontario. Basicladia could be implicated in any ofthe above relationships. Although it is unlikely that Komvophoron sp. could serve as a food source for turtles, it could form a commensal, mutual or even parasitic relationship, based on the degree of cellular intimacy observed in this study. A parasitic relationship could imply a net nutrient flux toward the algae or a weakening of the turtle epidermis by the algae, favoring growth of opportunistic fungi that could lead in rare cases to death of the host (Neil and Allen 1954). Based on the field collections from three turtle species, painted turtles appear to lack epizoic algae in Nova Scotia, snapping turtles support abundant colonies of B. chelonum, but lack Komvophoron sp., and Blanding's turtles support both species. The lack of algae on painted turtles contrasts with reports from across the species range (Colt et al. 1995, Ziglar and Anderson 2005) but is consistent with differential occurrence of algae on different turtle species (e.g., Dixon 1960). The difference in abundance and location of B. chelonum on the host may reflect habitat and behavior differences; snapping turtles spend less time aerial basking and are less active than the other two species. Restriction of Komvophoron sp. to the leg bases of turtles may reflect an association of the algae with soft tissues, but its restriction to Blanding's turtles remains unexplained. Basicladia chelonum occurred in two of the three populations, but in only three of the 17 locations surveyed. All three ofthese locations were flooded fens similar in character, with extensive areas of flooded sedges (Carex sp.), sweet gale (Myrica gale) and leather-leaf (Chamaedaphne calyculata) near a deep cut slow flowing stream; in this regard they were distinct from all the other locations. In one population (Pleasant River), B. chelonum was restricted to juvenile turtles, possibly reflecting differential microhabitat use by juveniles and adults. Such differential use has also been recorded from trapping and tracking studies in this population. In contrast, in the other population (McGowan Lake), where differential microhabitat use is less apparent, there was no age-related difference in frequency. Komvophoron sp. was more widespread but varied in its incidence amongst the three populations and between age groups in one population 683
(KNP) (Table 2); both patterns lack an obvious explanation. These observations suggest that the study of algal associations with freshwater turtles will provide considerable insight into the natural history of these communities. ACKNOWLEDGEMENTS We thank Jiri Komarek for the identification of Komvophoron, and J.P. Hastey and Mike Lawton for assistance with fieldwork. This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada to DJG. LITERATURE CITED Anagnostidis, K. and 1. Komarek. 1988. Modem approach to the classification system of cyanophytes. 3. Oscillatoriales. Archiv fUrHydrobiologie, Supplement 80: 327-472. Arif, I. A. 1991. Epizoic algal communities of AI-Has sa, Saudi Arabia. Arab Gulf 1. Scientific Research 9: 87-98. Belusz, L. C. and R. J. Reed. 1969. Some epizoophytes on six turtle species collected in Massachusetts and Michigan. American Midland Naturalist 81: 598-601. Burkholder,1.M. 1996. Interactions of benthic algae with their substrata. In: Stevenson, R.J., Bothwell, M.L. and Lowe, R.L. (eds), Algal ecology: fieshwater benthic ecosystems. Academic Press, San Diego. pp. 253-297. Chute, R. M. 1949. Basicladia in Main~..Rhodora 51: 232. Collins, F. S. 1907. Some new green algae. Rhodora 9: 197-202. Colt, L. C., R. A. Saumure, and S. Baskinger. 1995. First record of the algal genus Basicladia (Chlorophyta, Cladophorales) in Canada. Canadian Field-Naturalist 109: 454-455. COSEWIC. 2005. Canadian species at risk. Committee on the Status of Endangered Wildlife in Canada, Ottawa. Davis, D. S. and S. Browne (eds.). 1997. The natural history of Nova Scotia, Vol. 1. Topics and habitats. Nimbus Publishing and Nova Scotia Provincial Museum, Halifax, N.S., Canada. 519 pp. / Dixon, J. R. 1960. Epizoophytic algae on some turtles of Texas and Mexico. Texas J. Science 12: 36-38. Ducker, S. 1958. A new species of Basicladia on Australian freshwater turtles. Hydrobiologia 10: 157-174. Edgren, R. A., M. K. Edgren, and L. H. Tiffany. 1953. Some North American turtles and their epizoophytic algae. Ecology 34: 733-740. Ernst, C. H. and 1. N. Norris. 1978. Observations on the algal genus Basicladia and the Red-Bellied turtle Chrysemys rubiventris. Estuaries I: 54-57. Gibbons, J. W. 1968. Carapacial algae in a population ofthe Painted turtle, Chrysemys picta. American Midland Naturalist 79: 517-519. Gilhen,1. 1984. Amphibians and reptiles of Nova Scotia. Nova Scotia Museum, Halifax. 162 pp. Graham, L. E. and L. W. Wilcox. 2000. Algae. Prentice Hall, Upper Saddle River, New Jersey. 640 pp. + appendices. Herman, T.R., T. D. Power, and B. R. Eaton. 1995. Status of Blanding's turtles, Emydoidea blandingii, in Nova Scotia, Canada. Canadian Field-Naturalist 109: 182191. Hoffinann, W. E. and 1. E. Tilden. 1930. Basicladia, a new genus ofCladophoraceae. Botanical Gazette 89: 374--384. Komarek, J. 2006. Cyanobacterial taxonomy: current problems and prospects for the integration of morphological and molecular approaches. Algae 21: 349-375. Komarek, J., H. Kling, and 1. Komarkova. 2003. Filamentous Cyanobacteria. In: Wehr, J. D. and R. G. Sheath (eds), Freshwater algae of North America. Academic Press, San Diego. pp. 177-196. 684
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685 Received: 8 February 2007
Accepted:
11 May 2007
