Metamorphosis of freshwater mussel Glochidia (Bivalvia: Unionidae) on amphibians and exotic fishes.
Identification of hosts for freshwater mussels has become an important consideration in their conservation and management. While experiments with artificial media to bypass the parasitic stage on hosts have been promising (Isom and Hudson, 1982; Keller and Zam, 1990), this approach is not successful with every species. Thus, a host is required for laboratory glochidial metamorphosis from parasitic glochidium to juvenile mussel. Unfortunately, natural hosts have not been identified for most species. Even if known, the hosts may be as endangered as their mussel parasite, or they may be difficult to maintain in captivity.
Several exotic fish species already are identified as hosts for North American mussels. The common carp, Cyprinus carpio, is reported as host for five mussel species (Lefevre and Curtis, 1910, 1912; Parker et al., 1984). The goldfish, Carassius auratus, is the only known host for the rare Cyprogenia aberti (Chamberlain, 1934), although native hosts obviously must exist. The green swordtail, Xiphophorus helleri, and the guppy, Poecilia reticulata, also are reported as hosts for Anodonta oregonensis and Lasmigona compressa, respectively (Chamberlain and Jones, 1929; Tompa, 1979). Dechtiar (1972) found glochidia of an unidentified unionid on wild common carp in Lake Erie. Conversely, introduced mussels may use native fishes as hosts (Watters, 1997b). Despite these accounts, no experimental study of exotic piscine hosts has been undertaken.
Although reports of glochidial metamorphosis on amphibians have been published, workers have rarely included amphibians in studies of host identification for mussels. Faussek (1901) reported that Anodonta glochidia metamorphosed on larval tiger salamanders (Ambystoma tigrinum ssp.), tadpoles of Rana and Peltobates, and the Austrian cave salamander (Proteus sp.). Watters (1997a) partially confirmed Faussek's results by metamorphosing the pocketbook Lampsilis cardium on Ambystoma tigrinum ssp. Seshaiya (1941, 1969) and Walker (1981) demonstrated that other unionaceans metamorphosed on tadpoles. Howard (1951) reported metamorphosis of the salamander mussel Simpsonaias ambigua on mud-puppies (Necturus maculosus), and found nonmetamorphosed glochidia of the washboard Megalonaias nervosa on them as well.
Glochidial metamorphosis on crustaceans is virtually unknown, although Walker (1981) reported metamorphosis of a hyriid mussel on freshwater decapod crustaceans in Australia. Panha (1990) found unidentified glochidia on a palaemonid decapod in Thailand. No occurrences of metamorphosis on crustaceans were reported for North American mussels. Again, no experimental study of the role of these nonpiscine potential hosts has been undertaken.
The purpose of this study was to determine whether inexpensive and easily maintained exotic fishes, amphibians and crustaceans could serve as hosts for native North American mussels. These could serve as surrogate hosts, and bypass the need to identify native hosts when the objective is to culture captive mussels. Two species of mussels were used: the pocketbook Lampsilis cardium, and the paper pondshell Utterbackia imbecillis. Both are long-term brooders, producing glochidia in the autumn and carrying them in the marsupial portions of the gills over winter. Utterbackia imbecillis, and probably most anodontines, are believed to be host generalists (Trdan and Hoeh, 1982). Although originally reported as not needing a host for metamorphosis (Howard, 1914), no study in the past 50 yr has substantiated that claim. On the contrary, subsequent studies have identified 14 fish hosts (see review of Watters, 1994). There is no evidence that Utterbackia imbecillis develops without a host (Heard, 1975). Lampsiline glochidia generally attach to gills, whereas anodontine glochidia attach to fins. These two species were chosen as representatives of two unionid subfamilies (Lampsilinae and Anodontinae) that differ in reproductive adaptations and host specificity (Trdan and Hoeh, 1982; Waller et al., 1985; Rashleigh, 1995; Watters, 1997c). They represent extremes in the unionid reproduction spectrum for these characteristics.
MATERIALS AND METHODS
Two gravid females of Lampsilis cardium were collected in early summer from Conneaut Creek in northeastern Ohio. Seven gravid females of Utterbackia imbecillis were collected in summer from Lake Erie and Raccoon Creek, Ohio, and Lake Monticello, South Carolina. Both species were held in flow-through 38-liter aquaria at 20-21 C. Mussels were fed a suspended mixture of the algae Chlorella vulgaris, Ankistrodesmus falcatus and Chlamydomonas reinhardtii.
Tiger salamander larvae, African clawed frog (Xenopus laevis), freshwater shrimp (Palaemonetes sp.) and exotic fish species were obtained commercially. These potential hosts included 16 fish families, three amphibian families, and two decapod crustacean families. One to three individuals of each species were used per mussel species. Because of project constraints, we chose to test as many exotics as possible rather than more replicates of a fewer number of subjects, accepting that meaningful statistical comparisons would be sacrificed. Potential hosts were held in 38-liter aquaria at 20-21 C, with no substrate, and were fed every 2 days with aquatic oligochaetes or flake fish food. Largemouth bass (Micropterus salmoides) were known to be hosts for these mussels (Trdan and Hoeh, 1982; Waller et al., 1985). Young-of-year hatchery-raised largemouth bass were used as controls, to ensure that glochidia were infective, and to give a comparable level of metamorphosis on a native piscine host. Animals were maintained according to the Ohio State University Animal Care and Use protocols.
Glochidia were removed from gravid mussels by inserting a water-filled insulin syringe into the distal portion of the marsupium and flushing glochidia from the gills. A sample of glochidia was tested for viability with table salt; viable glochidia react by rapidly closing their valves. Glochidia were suspended in a container of 20-21 C water by gentle agitation with an airstone. Potential hosts were placed in the container and simultaneously exposed for 1 h (Table 1). After exposure, test subjects were segregated by species and returned to the aquaria.
Beginning the day after exposure and continuing every other day for up to 45 days, 1 liter of water was siphoned from the bottom of the aquarium and passed through a 145-[[micro]meter] sieve. Glochidia of both species are 250-[[micro]meter] in length or greater. The debris was examined for glochidia with a stereomicroscope using the polarized light method devised for detecting zebra mussel veligers (Johnson, 1995). Metamorphosed juveniles were identified by the presence of two adductor muscles, a foot and movement. Percent metamorphosis was calculated from the number of metamorphosed juveniles divided by the sum of the number of nonmetamorphosed glochidia and juveniles recovered (total attached). Total attached and percent metamorphosis were each averaged for multiple individuals in the same species.
Lampsilis cardium successfully metamorphosed on six species of exotic fishes from the families Fundulidae, Poecilidae and Belontiidae (= Anabantidae), as well as on larval tiger salamanders (Table 1). These suitable hosts represented 13.5% of all exotic and nonpiscine species tested. Percent metamorphosis on these exotics was below that of the control, largemouth bass. An average of 62% of glochidia metamorphosed on control fishes, whereas successful metamorphosis on test species ranged from only 3 to 22% (mean = 8.9%).
Utterbackia imbecillis successfully metamorphosed on 30 species (57%) of exotic fishes or nonpiscine hosts (Table 1). Nine of these hosts produced metamorphosed juveniles at a level comparable to or above that of largemouth bass. Percent metamorphosis on controls averaged 43%, whereas successful metamorphosis on test species ranged from 7 to 83% (mean = 36%). Three exotic host fishes previously reported in the literature, guppy (Poecilia reticulata), goldfish (Carassius auratus), and green swordtail (Xiphophorus helleri), also served as hosts. However, none resulted in a percentage of metamorphosis comparable to largemouth bass or belontiids.
No metamorphosis occurred in the limited number of crustaceans tested. Most crustaceans molted at least once during the tests, undoubtedly removing any glochidia attached to the gills or other parts of the exoskeleton. No encysted glochidia were found on any exuviae.
Host use. - Of the three fish families serving as hosts for Lampsilis cardium, the poecilids and fundulids have members native to North America. Several species in these families have been identified as hosts of North American mussels. In the Fundulidae, western banded killifish, Fundulus diaphanus diaphanus, was identified as a host for the fatmucket, Lampsilis radiata luteola (Watters, 1996), and six other species of freshwater mussels (Young, 1911; Wiles, 1975a, b; Trdan and Hoeh, 1982). Golden topminnow, Fundulus chrysotus, was a host for the giant floater, Pygandon grandis (Penn, 1939). Plains killifish, Fundulus zebrinus, was a host for the squawfoot, Strophitus undulatus (Ellis and Keim, 1918). In the Poecilidae, mosquitofish, Gambusia affinis, was reported as a host for three North American mussels (D'Eliscu, 1972; Stern and Felder, 1978; Neves et al., 1985). Thus, it was not surprising that [TABULAR DATA FOR TABLE 1 OMITTED] other species of these fish families, from outside North America, could serve as hosts for L. cardium.
Explanations for the suitability of belontiids as hosts to Lampsilis cardium are more complicated. Belontiids are found in India, southeast Asia and Indonesia. No native representatives occur in North America. However, Asian unionids occur within the ranges of belontiids. We surmise that belontiids are suitable hosts for the two species tested, and perhaps other North American unionids, by virtue of their co-occurrence and co-evolution with Asian unionids, where they probably act as hosts. However, worldwide, unionids do not greatly overlap the ranges of the other fish families tested (Cichlidae, Callichthyidae, etc.), which predominantly come from Africa, South America and Australia, where few or no unionids occur. The atherinids are reported as hosts for hyriid mussels (Humphrey and Simpson, 1985), cichlids are hosts for hyriid, mutelid and mycetopodid mussels (Bonetto and Ezcurra, 1962, 1963; Mansur and Veitenheimer-Mendes, 1979; Kondo, 1984), characids as hosts for hyriids and mycetopodids (Bonetto and Ezcurra, 1962, 1963), and callichthyids are hosts for mycetopodids (Bonetto and Ezcurra, 1962). Although these fishes co-occur with and act as hosts for species of these freshwater mussel families, they apparently are not suitable hosts for the Unionidae.
The gyrinochelids and silurids also are native to Indonesia where unionids occur, but were not suitable hosts for Lampsilis cardium in this study. It is possible that these bottom feeders ingested metamorphosed juveniles before they were retrieved from the aquaria. Of the remaining families tested for L. cardium, most either have no native species in North America (e.g., Cichlidae), or are represented by very few species (e.g., Characidae, Atherinidae). Only the Cyprinidae is well-represented in North America. However, only one native cyprinid is reported as a host for a Lampsilis: the common shiner, Luxilus cornutus (Fuller, 1978).
We suggest that if a fish family in North America has suitable hosts for Lampsilis cardium (e.g., Poecilidae, Fundulidae), then exotic species of that family may be hosts as well. Fish families not serving as hosts in North America (e.g., Cyprinidae) do not serve as hosts when exotic members are used. Further support of this idea is the finding that mussels will metamorphose on extralimital congeners of natural hosts within North America (Neves et al., 1985). This study demonstrates that Utterbackia imbecillis can successfully parasitize a wide range of piscine or amphibian hosts, including members of families not native to North America. Many of these may be parasitized to the same or greater degree than a native host. The broad distributions of many anodontine species likely are the result of this generalist use of hosts.
Lampsilis cardium glochidia averaged nearly twice as long to complete metamorphosis (mean = 14 days, range 9 to 19 days) as did Utterbackia imbecillis glochidia (mean = 7.5 days, range 3 to 13 days) when maintained at the same temperature. The metamorphosis of U. imbecillis in 3 days on silver tip tetra (Hemigrammus nanus) is one of the shortest glochidial parasitic durations recorded. Seshaiya (1969) reported the same duration for an Indian unionid on native host fishes.
Numbers of attached glochidia per host species varied greatly. For example, although exposed simultaneously to the same concentration of Utterbackia imbecillis glochidia, a Betta splendens harbored only five glochidia, whereas a Gasteropelecus levis bore 900. The probability of encountering glochidia as the result of differences in swimming behavior obviously will lead to differences in parasite burden, although no differences were noted between these two species. This extreme variation suggests differences in susceptibility, but the mechanisms underlying this phenomenon are not known. Most glochidia attached to fins, but there was no obvious relationship between fin area and levels of infestation.
An individual belontiid, Sphaerichthys osphromenoides, shed eight of 13 attached glochidia as nonmetamorphosed larvae 11 to 17 days postexposure. This was the period when metamorphosed glochidia typically were shed by other hosts. This phenomenon was reported in Mid-caught fishes and may represent a secondary immune reaction of a suitable host (Watters and O'Dee, 1996).
Phylogenetic and zoogeographic implications. - based on host specificity, lampsilines are regarded as specialists, and anodontines as generalists (Trdan and Hoeh, 1982; Neves et al., 1985; Watters, 1977c). Lampsilines have evolved morphological adaptations to more efficiently contact their hosts, including mantle displays and conglutinates (packages of glochidia bound within a mucous matrix). This has resulted in their specialization for certain types of hosts. Anodontines have few or no such luring behaviors or morphological adaptations, but are able to parasitize successfully a wider range of host species, including exotics. These represent two different coevolutionary paths for these host/parasite relationships. Amblemine unionids were not included in this study, and it has not been shown that they can use exotic hosts. Many amblemines produce conglutinates, which often mimic specific fish food items, suggesting host specificity (Chamberlain, 1934; Haag et al. 1995, Hartfield and Hartfield, 1996).
Metamorphosis of a North American unionid on tiger salamander larvae was first reported by Watters (1997). Additional amphibians were shown to be suitable hosts for the mussels in this study. If this is a widespread phenomenon, then an important aspect of freshwater mussel zoogeography has been overlooked. Clearly, efforts to identify other amphibian and mussel associations are needed.
Management implications. - In contrast to many native hosts, the exotic hosts identified here are commercially available from most tropical fish suppliers. Many are routinely bred in captivity and may be obtained in large numbers. They are easily maintained with well-known diets and breeding requirements. Many commercially obtained surrogates are relatively parasite-free, and the probability of previous glochidial infection is very small, whereas wild-caught natural hosts are usually infested with numerous parasites, including glochidia that may interfere with subsequent infestations.
All surrogate hosts for Lampsilis cardium produced fewer juveniles when compared to the native host, whereas many surrogates for Utterbackia imbecillis performed as well as or better than native hosts. Of all groups tested, the belontiids were most suitable to both mussel species. Using inexpensive, easily available, parasite-free surrogate hosts may be a valuable alternative to natural hosts in some situations. Obviously, we do not advocate the release of exotic hosts to bolster native mussel populations. But in hatchery conditions, or to obtain metamorphosed juveniles for introduction, surrogate hosts may be more cost-effective and practical.
Acknowledgments. - This study was funded by the Ohio Chapter of The Nature Conservancy (TNC). Some labor and materials were donated by the Aquatic Ecology Laboratory and the Ohio Biological Survey of Ohio State University, and the Ohio Division of Wildlife through the Do Something Wild state income tax checkoff. Mr. Scott O'Dee's (Ohio State University) assistance in taking samples is greatly appreciated. Ms. Margaret Barfield (Arkansas State University) generously supplied live mussels from South Carolina. I particularly thank Dr. Steve Sutherland (TNC) for his interest in and support of this project.
BONETO, A. A. AND I. D. EZCURRA. 1962. El desarrollo del lasidium de Anodontities trapesialis forbesianus (Lea) (Moll. Lamell.). Physis, 23:195-203.
----- AND -----. 1963. Notas Malacologicas. I. (1) El desarrollo del glochidium de Diplodon delodontus delodontus (Lam.); (2) El glochidium de Prisodon (Triplodon) corrugatus Lam.; (3) El lasidium de Monocondylea paraguayana d'Orb. Physis, 24:17-22x.
CHAMBERLAIN, T. K. 1934. The glochidial conglutinates of the Arkansas fanshell, Cyprogenia aberti (Conrad). Biol. Bull., 66:55-61.
----- AND D. T. JONES. 1929. A descriptive catalog of the Mollusca of Utah. Bull. Univ. Utah, 19:1-203.
DECHTIAR, A. O. 1972. New parasite records for Lake Erie fish. Great Lakes Fish. Comm. Tech. Rep., 17:1-20.
D'ELISCU, P. N. 1972. Observation of the glochidium, metamorphosis, and juvenile of Anodonta californiensis Lea, 1857. Veliger, 15:57-58.
ELLIS, M. AND M. KEIM. 1918. Notes on the glochidia of Strophitus edentulus pavonius (Lea) from Colorado. Nautilus, 32:17-18.
FAUSSEK, V. 1901. Ueber den Parasitismus der Anodonta Larven. Verb. 5th Int. Zool-Congr Berlin, 12-16 August 1901:761-766.
FULLER, S. L. H. 1978. Fresh-water mussels (Mollusca: Bivalvia: Unionidae) of the upper Mississippi River: Observations at selected sites within the 9-foot channel navigation project on behalf of the U.S. Army Corps of Engineers. Final Rep. Army Corps Engineers, (78-33). 401 p.
HAAG, W. R., R. S. BUTLER AND P. D. HARTFIELD. 1995. An extraordinary reproductive strategy in freshwater bivalves: prey mimicry to facilitate larval dispersal. Freshw. Biol., 34:471-476.
HARTFIELD, P. AND E. HARTFIELD. 1996. Observations on the conglutinates of Ptychobranchus greeni (Conrad, 1834) (Mollusca: Bivalvia: Unionoidea). Am. Midi. Nat., 135:370-375.
HEARD, W. H. 1975. Sexuality and other aspects of reproduction in Anodonta (Pelecypoda: Unionidae). Malacologia, 15:81-103.
HOWARD, A.D. 1914. A second case of metamorphosis without parasitism in the Unionidae. Science, 40:353-355.
-----. 1951. A river mussel parasitic on a salamander. Nat. Hist. Misc., 77:1-6.
HUMPHREY, C. L. AND R. D. SIMPSON. 1985. The biology and ecology of Velesunio angasi (Bivalvia: Hyriidae) in the Malaga Creek, Northern Territory. Rep. Office Supervising Sci. Alligator Rivers Region, Open File Rec., 38:476 p., 2 appen.
ISOM, B. G. AND R. G. HUDSON. 1982. In vitro culture of parasitic mussel glochidia. Nautilus, 96:147-151.
JOHNSON, L. E. 1995. Enhanced early detection and enumeration of zebra mussel (Dreissena ssp.) veligers using cross-polarized light microscopy. Hydrobiologia, 312:139-143.
KELLER, A. E. AND S. G. ZAM. 1990. Simplification of in vitro culture techniques for freshwater mussels. Environ. Toxicol. Chem., 9:1291-1296.
KONDO, T. 1984. Hosts of the larvae of Moncetia lavigeriana (Bivalvia: Mutelidae) in Lake Tanganyika. Venus, 43:347-352.
LEFEVRE, G. AND W. C. CURTIS. 1910. Reproduction and parasitism in the Unionidae. J. Exp. Zool., 9: 79-115.
----- AND -----. 1912. Studies on the reproduction and artificial propagation of fresh-water mussels. Bull. U.S. Bur. Fish., 30:105-201.
MANSUR, M. C. AND I. L. VEITENHEIMER-MENDES. 1979. Redescicao de Mycetopoda legumen (Martens, 1888) (Bivalvia: Mycetopodidae). Rev. Bras. Biol., 39:695-702.
NEVES, R. J., L. R. WEAVER AND A. V. ZALE. 1985. An evaluation of host suitability for glochidia of Villosa vanuxemi and V. nebulosa (Pelecypoda: Unionidae). Am. Midl. Nat., 113:13-19.
PANHA, S. 1990. The site survey and the study on reproductive cycles of freshwater pearl mussels in the central part of Thailand. Venus, 49:240-257.
PARKER, R. S., C. T. HACKNEY AND M. F. VIDRINE. 1984. Ecology and reproductive strategy of a south Louisiana freshwater mussel, Glebula rotundata (Lamarck) (Unionidae: Lampsilini). Freshwater Invertebr. Biol., 3:53-58.
PENN, G. H. 1939. A study of the life cycle of the fresh-water mussel, Anodonta grandis, in New Orleans. Nautilus, 52:99-101.
RASHLEIGH, B. 1995. Simulation modeling of competition between freshwater mussels for fish hosts. Assoc. Southeast. Biol. Bull., 42:114.
SESHAIYA, R. V. 1941. Tadpoles as hosts for the glochidia of the fresh-water mussel. Curr Sci. (Bangalore), 10:535-536.
-----. 1969. Some observations on the life-histories of south Indian freshwater mussels. Malacologia, 9:286-287.
STERN, E. M. AND D. L. FEEDER. 1978. Identification of host fishes for four species of freshwater mussels (Bivalvia: Unionidae). Am. Midl. Nat., 100:233-236.
TOMPA, A. S. 1979 Life-cycle completion of the freshwater clam Lasmigona compressa (Bivalvia: Unionidae) in an experimental host, Lebistes reticulatus. Veliger, 22:188-190.
TRDAN, R.J. AND W. R. HOEH. 1982. Eurytopic host use by two congeneric species of freshwater mussel (Pelecypoda: Unionidae: Anodonta). Am. Midl. Nat., 108:381-388.
WALKER, K. F. 1981. The ecology of freshwater mussels in the River Murray. Austr. Water Res. Tech. Pap., 63:1-110.
WALLER, D. L., L. E. HOLLAND, L. G. MITCHELL AND T. W. KAMMER. 1985. Artificial infestation of largemouth bass and walleye with glochidia of Lampsilis ventricosa (Pelecypoda: Unionidae). Freshwater Invertebr. Biol., 4:152-153.
WATTERS, G. T. 1994. An annotated bibliography of the reproduction and propagation of the Unionoidea (Primarily of North America). Ohio Biol. Surv. Misc. Contrib. 1, 1-158.
-----. 1996. New hosts for Lampsilis cardium. Trian. Unionid Rep., 9:8.
-----. 1997a. Glochidial metamorphosis of the freshwater mussel Lampsilis cardium (Bivalvia: Unionidae) on larval tiger salamanders, Ambystoma tigrinum ssp. (Amphibia: Amystomidae). Can. J. Zool., 75:505-508.
-----. 1997b. A synthesis and review of the expanding range of the Asian freshwater mussel Anodonta woodiana (Lea, 1834) [Bivalvia: Unionidae]. Veliger; 40:152-156.
-----. 1997c. Individual-based models of mussel-fish interactions: a cautionary study p. 45-62. In: K. S. Cummins, A. C. Buchanan, C. A. Mayer and T. J. Naimo (eds.). Conservation and management of freshwater mussels. II. Proceedings of a UMRCC symposium, 16-18 October 1995, St. Louis, Mo. Upper Mississippi River Conservation Committee, Rock Island, IL.
----- AND S. O'DEE. 1996 Shedding of untransformed glochidia by fishes parasitized by Lampsilis fasciola Rafinesque, 1820: evidence of acquired immunity in the field? J. Aquat. Ecol., 11:383-389
WILES, M. 1975a. The glochidia of certain Unionidae (Mollusca) in Nova Scotia and their fish hosts. Can. J. Zool., 53:33-41.
-----. 1975b. Parasites of Fundulus diaphanus (LeSueur) (Pisces: Cyprinodontidae) in certain Nova Scotian freshwaters Can. J. Zool., 53:1578-1580.
YOUNG, D. 1911. The implantation of the glochidium on the fish Univ. Mo. Bull. Sci. Ser., 2:1-16.
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|Author:||Watters, G. Thomas; O'Dee, Scott H.|
|Publication:||The American Midland Naturalist|
|Date:||Jan 1, 1998|
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