INDEX WORDS: Round goby, zebra mussels, sphaeriid clams, Great Lakes.
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1 J. Great Lakes Res. 21(4): Internat. Assoc. Great Lakes Res., 1995 Note Zebra Mussel Predation by Round Gobies in the Laboratory Michael J. Ghedotti, 1 Joseph С. Smihula, and Gerald R. Smith 2 Museum of Zoology, University of Michigan, Ann Arbor, Michigan A B S T R A C T. The round goby (Neogobius melanostomus), a native of the Black and Caspian seas, has spread from the original point of discovery in the St. Clair River to Lakes St. Clair, Erie, Huron, Michigan, and Superior. Round gobies utilize a broad range of foods, but prefer zebra mussels (Dreissena polymorpha). Gobies 6 10 cm in standard length consume mussels up to 7 x 13 mm. Zebra mussels 4 13 mm long are eaten at rates averaging between 36 and 47 per day, depending on predator/prey size; zebra mussels smaller than 4 mm were eaten at rates exceeding 100 per day. Feeding rates averaged 5.4/hr in 140-minute trials. Individual and clumped zebra mussels were preferred over sphaeriid clams on both sand and gravel substrates. INDEX WORDS: Round goby, zebra mussels, sphaeriid clams, Great Lakes. I N T R O D U C T I O N Two Pontocaspian goby species, like zebra mussels (Griffiths et al. 1991, Mills et al. 1993), entered the Great Lakes probably in the ballast tanks of Soviet ships, prior to 1989 (Jude et al. 1991, Carlton and Geller 1993). The tubenose goby (Proterorhinus marmoratus) feeds on small crustaceans and aquatic insect larvae. The round goby feeds primarily on bivalve mollusks; the zebra mussel makes up a substantial part of the diet (Berg 1949, Banarescu 1964, Svedovidov 1964, Miller 1986). The round goby may reach lengths of up to 25 cm in its native range and 18 cm in the Great Lakes (Jude et al. in press), with high fecundity, and a life span of 4 to 5 years (Berg 1949, Miller 1986). In their native habitats, zebra mussels and round gobies occupy littoral and lower tributary habitats in the Black and Caspian seas. The round goby possesses robust molariform teeth (Fig. 1) of the type observed in other mollusk-eating fishes (French 1993). Round gobies, especially large individuals, consume large quantities of zebra mussels in the Great Lakes (D. Jude, University of Michigan, Center for Great Lakes and Aquatic Sciences, pers. comm.). 1 Present address: Museum of Natural History, University of Kansas, Lawrence, Kansas Correspondent
2 We investigated whether round gobies would consume zebra mussels in preference to the less abundant small native mollusks and whether substrate type affects selectivity and feeding rates. M E T H O D S Round gobies were collected by trawling and angling in the St. Clair River, Michigan. They were kept in 40- to 400-L aquaria and fed flake food or tubificid worms. Eighteen experimental gobies, 6-10 cm in standard length, ate zebra mussels in the laboratory (a few gobies refused all food, possibly because of hook wounds). Zebra mussels were collected from the mouth of the Maumee River on Lake Erie and native fingernail clams (Sphaerium sp.) were collected from Fleming Creek north of Ann Arbor, Michigan. In different trials, round gobies were offered zebra mussels (individually or in clumps), clams, or snails (Planorbis) over different substrates. Tests of feeding rates and selectivity were conducted in neutral, conditioned water in 20- to 60-L aquaria with rock, tile, or tube shelters. Each fish was placed in an aquarium at 21 C, given 1-2 days to acclimate, then presented with clumps or counted samples of individually measured mussels. After a predetermined time, broken shells and uneaten zebra mussels were removed, counted, and measured. Thirty-eight 24-hour tests examined different sizes of zebra mussels consumed, the size sequence, and the behavior of ingestion. To test the response to clumped zebra mussels, three round gobies were separately provided with un-anchored clumps of mussels on a glass substrate in 20-L aquaria. Each clump was made up of more than 50 zebra mussels which were about 1-24 mm in length, firmly attached to each other with their byssal threads. Two investigators weighed the clumps and counted the number of mussels in the edible size range before and after each 24-hour feeding bout.
3 To test the effect of substrate on selectivity, aquaria were provided with substrates of sand or coarse gravel (3-35 mm). Two previously untested round gobies were given 25 individual zebra mussels and 25 native clams, representing equivalent size distributions from 4.5 to 12.5 mm. After 140 minutes, mollusks and shell fragments were counted and recorded. Fish were later tested over alternate substrates; four trials using two gobies were analyzed by mixed model multi-way ANOVA. Selectivity of clumped mussels versus native clams was tested by placing one fish, one clump of zebra mussels, and 25 native clams in each of two tanks. Zebra mussels in clumps were measured and those smaller than 4.5 mm and those between 12.5 mm and 13.5 mm were removed. Larger mussels provided attachment substrate for the 25 mussels mm left remaining in each clump. After 140 minutes of feeding opportunity, uneaten mollusks were measured and recorded. Fish were tested with alternate substrates the following day. Data were analyzed by Model I twoway ANOVA. Effect of adjacent sand and coarse gravel substrates on selectivity were ascertained using 60-L aquaria with two adjacent substrates. One round goby was placed in each aquarium and 25 individual zebra mussels mm long were scattered on each substrate. After 140 minutes, mussels and shell fragments were counted and measured. The experiments were repeated with reversed substrate orientation and later repeated again using zebra mussels in clumps. Data were analyzed using a Multi-way ANOVA with individual versus clumped zebra mussels, substrate type, and two individual gobies as variables. R E S U L T S In h trials, round gobies 8-10 cm in standard length consumed an average of 36 zebra mussels per day, depending on prey size (total range, 0 to over 100/day). In two of these trials, gobies ate over 100 juvenile mussels (1-4- mm) in 24 h. Gobies 6-8 cm in length consumed an average of 47 (8-78) zebra mussels mm long in 10 trials. Presented with a size range, round gobies consumed smaller zebra mussels first (Fig. 2). Mussels larger than 6 x 12 mm could not be eaten by a goby 9 cm long (72 mm standard length) with a gape of about 6x8 mm. Mussels larger than 7x13 mm were too large for consumption by 10-cm gobies. Gobies demonstrated the ability to remove almost all ediblesize mussels from clumps of mussels in 24 h (Fig. 3). Estimates of consumption of mussels from clumps averaged 5.5 g (total weight) per day (est ) individuals 4-12 mm long. The analysis of selectivity of individual mussels showed that there was a significant preference for zebra mussels over native clams (Table 1; P <.001). Gobies ate more than twice as many zebra mussels when presented with equal numbers and sizes of separated zebra mussels and sphaeriid clams. There was also significantly greater consumption of clumped zebra mussels than (non-clumped) native clams (Table 1;P =.048). Round gobies ate 5.4 zebra mussels/hr in 140-m trials under varied conditions (Table 1, mean 12.6/140 m). Prey vulnerability was not significantly different over different substrates; gobies effectively preyed on zebra mussels on both sand and gravel. Gobies crushed but did not immediately ingest planorbid snails that were presented to them with zebra mussels, which were consumed first.
4 DISCUSSION Round gobies readily consumed zebra mussels in the laboratory. In all situations presented to the gobies, zebra mussels were preferred over the native clams or snails. The byssal attachments of clumped zebra mussels did not reverse goby preference for zebra mussels over native clams (which are nonclumped). Different substrates caused little variation in feeding preference or rate, however, clams and snails that managed to attach to an aquarium wall more than 20 cm off the bottom seemed safe from goby attack.
5 Gobies 6-10 cm in length will eat 4.5 mm to 12.5 mm zebra mussels. The average-sized round goby in the Great Lakes, 8-11 cm standard length, consumed zebra mussels mm long (Jude et al. in press). The maximum size of round gobies in the Great Lakes may reach 18 cm, nearly twice as large as the modal size in our experiments. Round gobies were frequently observed to take one or more 4-8 mm zebra mussels into the mouth and pharynx and masticate them. Mussels were retained in the mouth for periods ranging from less than 1 h to more than 12 h, before the empty shells were ejested. These shells show tooth marks at the distal edges of the shell. Gobies usually split the shells and removed the bodies of mussels before ingestion in the laboratory, but they crush mussels as well; stomachs of wild-caught gobies frequently contain crushed mussel shell and bodies (D. Jude, pers. comm.). Native molluscivores in the Great Lakes, especially freshwater drum (Aplodinotus grunniens), white sucker (Catostomus commersoni), and river redhorse (Moxostoma carinatum), crush the mussels and pass both the tissues and the shell fragments through their digestive tracts (French, 1993). Gobies will apparently prey on zebra mussels whenever they encounter them in the Great Lakes benthos, but because gobies are negatively buoyant (lack swim bladders), they are not effective predators on mussels inhabiting vertical surfaces away from the bottom (John Janssen, Loyola Univ., Chicago, Illinois, pers. comm.). Although they may be viewed as a benefit because they eat zebra mussels, gobies may also be a nuisance in the Great Lakes. They were nonselective in taking varieties of bait and they prey on small fishes and invertebrates in captivity (Jay Hemdal, Toledo Aquarium, Eric Esper, Belleville, Michigan, and David Jude, pers. comms.). In its native range "the round goby feeds primarily on bivalve mollusks... but it can be expected to feed on nearly everything lying on the bottom" (Svetlana Rudnika, Varna, Bulgaria, personal communication). Because of their aggressiveness and dietary breadth gobies pose potential problems as predators on native benthos. They will compete with sculpins, darters, and sunfishes and provide forage for walleyes and smallmouth bass in the littoral habitats of the Great Lakes.
6 The high fecundity and aggressiveness of round gobies (Berg 1949, Miller 1983) are contributing to rapid population increase and range expansion. The round goby's arrival and explosive population increase at Harsen's Island in the St. Clair River delta was notable: None were caught in the fall of 1989 but by the next spring they made up most of the angling catch there (Eric Esper, pers. comm.). They were reported from Cleveland, Sandusky, and Chicago in 1994 (Roger Thoma, Ohio DNR, D. Jude, and J. Janssen, pers. comms.), and Lake Superior in 1995 (J. Selgeby, U.S. Biol. Serv., D. Jude, pers. comms.). They currently dominate daytime angling at Port Huron (J. Smihula, pers. obs.) and parts of Lake Michigan near Chicago (John Husar, Chicago Tribune, 20 November 1994). It appears that the number and diversity of native fishes at these sites has been substantially reduced. A C K N O W L E D G M E N T S We thank the following individuals for collecting gobies: David Jude, Center for Great Lakes and Aquatic Sciences, University of Michigan; Robert Haas, Michigan Department of Natural Resources; Gary Crawford, University of Michigan; Robert Reider, Detroit Edison Company; William Maier, University of Michigan; and Eric Esper, Belleville, Michigan. Jerrine Nichols of the U.S. Biological survey helped with zebra mussels. Russ Moll, Michigan Sea Grant Program, provided undergraduate research funds. David Jude and John Janssen shared abundant information, assisted by EPA Cooperative Agreement CR R E F E R E N C E S Banarescu, P Fauna Republicii Populare Romine, Vol. XIII. Editura Acadamiei Republicii Populare Romine, Bucharesti. Berg, L.S The Freshwater Fishes of the U.S.S.R. and Adjacent Countries, Vol. 2. Moscow: Academy of Sciences. Carlton, J.T., and Geller, J.B Ecological roulette: The global transport of nonindigenous marine organisms. Science 261: French, J.R.P., III How well can fishes prey on zebra mussels in eastern North America? Fisheries 18(6): Griffiths, R.W., Schloesser, D.W., Leach, J.H., and Kovalak, W.P Distribution and dispersal of the zebra mussel (Dreissena polymorpha) in the Great Lakes region. Can. J. Fish. Aquat. Sci. 48: Jude, D.J., Reider, R.H., and Smith, G.R Establishment of Gobiidae in the Great Lakes basin. Can. J. Fish. Aquat. Sci. 49: , Janssen, J., and Crawford, G. In press. Ecology, distribution, and impact of the newly introduced round and tubenose gobies on the biota of the St. Clair and Detroit Rivers. In The Lake Huron Ecosystem: Ecology, Fisheries, and Management, ed. M. Munawar, T. Edsall, and J. Leach. Ecovision World Monograph Series, S. P. B. Academic Publishing, The Netherlands. Miller, P.J Gobiidae. In Fishes of the North-east Atlantic and Mediterranean, Vol. III, ed. P. White-head, M. Bauchot, J. Hureau, J. Nielsen, and E. Toronese, pp Paris: UNESCO.
7 Mills, E.L., Leach, J.H., Carlton, J.T., and Secor, C.L Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. /. Great Lakes Res. 19:1-54 Svedovidov, A.N Fishes of the Black Sea. Moscow: Soviet Academy of Sciences. Submitted: 22 December 1993 Accepted: 25 September 1995
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