Establishment of two invasive crustaceans

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Establishment of two invasive crustaceans (Copepoda: Harpacticoida) in the nearshore sands of Lake Michigan Thomas G. Horvath, Richard L. Whitman, and Laurel L. Last

Abstract: Benthic copepods (Copepoda: Harpacticoida) in the nearshore sediments of southern Lake Michigan appear to be dominated by two new invasive species. We report the first occurrence in North America of Schizopera borutzkyi Montschenko, a native to the Danube River delta, and Heteropsyllus nr. nunni, likely a new species that is morphologically similar to the marine species Heteropsyllus nunni and represents the first occurrence of this genus in freshwater. Schizopera borutzkyi is a euryhaline species occurring in shallow sands in its native habitat and in deeper sands (6–15 m) in southern Lake Michigan. Based on the absence of these species from previous studies, we suggest that they are recent introductions. Heteropsyllus nr. nunni dominated (55–100%) the harpacticoid abundance to depths of 9 m, but S. borutzkyi comprised 75% of the harpacticoid abundance at 15 m. Native harpacticoids were always greatly outnumbered by invasive harpacticoids in our samples, which suggests that the natives are being replaced rapidly or that the invasive species are finding unused resources. The ecological implications of these introductions are not known, but these invasions may represent continued “invasional meltdown” in Lake Michigan. Résumé : Le peuplement des copépodes benthiques (Copepoda: Harpacticoida) des sédiments le long de la rive sud du lac Michigan semble être dominé par deux espèces envahissantes. C’est la première fois que la présence de Schizopera borutzkyi Montschenko, une espèce originaire du delta du Danube, est signalée en Amérique du Nord; il en est de même pour Heteropsyllus près de nunni, probablement une espèce nouvelle morphologiquement semblable à l’espèce marine Heteropsyllus nunni, ce qui représente la première découverte du genre en eau douce. Schizopera borutzkyi est une espèce euryhaline qui vit dans les fonds sablonneux en eau peu profonde dans son milieu d’origine et dans les sables en eau plus profonde (6–15 m) dans le sud du lac Michigan. Absentes des études antérieures, ces espèces nous semblent être des introductions récentes. Heteropsyllus près de nunni est l’espèce dominante d’harpacticoïde (50–100% de la densité) jusqu’à une profondeur de 9 m, alors que S. borutzkyi représente 75% de l’abondance des harpacticoïdes à 15 m. La densité des harpacticoïdes envahissants dépasse toujours de beaucoup celle des harpacticoïdes indigènes dans nos échantillons, ce qui laisse croire que les espèces indigènes sont en train d’être remplacées rapidement ou alors que les espèces envahissantes trouvent des ressources inutilisées. Ces invasions ont des conséquences écologiques inconnues, mais elles s’insèrent peut-être dans un processus d’« effondrement » de la communauté consécutif aux invasions (« invasional meltdown ») en cours au lac Michigan. [Traduit par la Rédaction]

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Introduction Exotic species in the Laurentian Great Lakes are becoming increasingly more common. Most introduced species are coming into the Great Lakes via ballast water, and a majority of the recent invaders have been euryhaline species originating from the Ponto–Caspian region (Ricciardi and

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MacIsaac 2000). Crustaceans appear successful at surviving transport in ballast water, possibly because many have mechanisms (e.g., resting eggs or encystment) to deal with periods of unfavorable environmental conditions or are able to adapt to rapid changes in salinity that occur during ballast water exchange (Lee and Bell 1999). In addition, the water bodies in the Ponto–Caspian region are particularly rich in

Received April 11, 2001. Accepted May 23, 2001. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on June 4, 2001. J16309 T.G. Horvath,1,2 R.L. Whitman, and L.L. Last. U.S. Geological Survey, Lake Michigan Ecological Research Station, 1100 North Mineral Springs Road, Porter, IN 46304, U.S.A. 1 2

Corresponding author (e-mail: [email protected]). Present address: Department of Biology, State University New York College of Oneonta, Oneonta, NY 13820, U.S.A.

Can. J. Fish. Aquat. Sci. 58: 1261–1264 (2001)

J:\cjfas\cjfas58\cjfas-07\F01-089.vp Tuesday, May 29, 2001 11:21:18 AM

DOI: 10.1139/cjfas-58-7-1261

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endemic species, especially crustaceans. Exotic crustaceans recently reported in the Great Lakes include the pelagic cladocerans Cercopagis pengoi (Ostroumov) (MacIsaac et al. 1999) and Daphnia lumholtzi Sars (Muzinic 2000). Changes in the pelagic crustacean community have affected ecosystem function, but the role of benthic crustaceans, especially harpacticoids, is much less known (Hudson et al. 1998), and changes in the benthic zone may have similarly important ecological effects. In marine ecosystems, harpacticoids form an integral link in food webs by coupling nutrients with higher trophic levels, such as salmonid fish (Fujiwara and Highsmith 1997), and also structure benthic and pelagic links (Gregg and Fleeger 1998). In freshwaters, harpacticoids are major consumers of microbial carbon production and may provide an efficient pathway for energy transfer to higher trophic levels (Hudson et al. 1998). Thus, changes in the harpacticoid community may cause drastic shifts in ecosystem processes originating in or involving the benthic zone.

Materials and methods We report changes in the meiobenthic community composition of two areas of southern Lake Michigan, which have been invaded by two harpacticoids. To document the community composition of the nearshore meiobenthos, we collected benthic samples from two sites in the nearshore sands of southern Lake Michigan: Indiana and Chicago. The Indiana site was located directly offshore from Mt. Baldy, Indiana Dunes National Lakeshore (41°42 ¢ N, 86°55 ¢ W) and was sampled on a single date in years 1996–2000 (14 August 1996, 4 December 1998, 22 October 1999, and 28 August 2000). Specific conductance in this area is around 300 mS·cm–1. A single ponar sample (232 cm2) was taken at depths of 1.5, 4, and 6 m along each of four transects (n = 4 for all analyses) in all years except 2000, when samples were collected in triplicate along a single transect but at depths of 1, 1.5, 4, 6, 9, and 15 m. The Chicago site was sampled once on 7 December 1999 by collecting 50 ponar samples from randomly selected spots within an area between Diversey and Belmont harbors (41°56 ¢ N, 87°37 ¢ W). Depth in this area was between 2 and 5 m. Sediments generally were fine- to coarse-grained sands with very little organic matter (>10 m along European coasts, although H. nunni was collected from shallow sands along North American coasts (Williams-Howze and Coull 1992). We collected the highest densities of H. nr. nunni in Lake Michigan at depths around 9 m. These differences, plus subtle morphological differences (B. Coull, University of South Carolina, Columbia, SC 29208, and J. Williams, University of Southern Mississippi–Gulf Coast, Long Beach, MS 39560, personal communications), support the conclusion that H. nr. nunni is a separate species from H. nunni. The typical body size of collected H. nr. nunni was about 510 mm. It is currently impossible to claim a vector of introduction for H. nr. nunni because its origins are not known. However, for a number of reasons, the most likely vector of invasion for S. borutzkyi into Lake Michigan is ballast water exchange. (i) Numerous invasion routes exist directly linking the Great Lakes with the Black Sea (Ricciardi and MacIsaac 2000). (ii) Ballast water has been implicated as the transport vector in most arrivals from Europe since the 1980s (e.g., Dreissena polymorpha, Cercopagis pengoi, Gymnocephalus cernuus; Ricciardi and MacIsaac 2000). (iii) Harpacticoids are known to survive long periods in ballast water (Chu et al. 1997), which would be required of a transoceanic voyage. Current ballast-water exchange programs may not have prevented S. borutzkyi from entering the Great Lakes because © 2001 NRC Canada



Rapid Communication / Communication rapide Fig. 1. Abundance of harpacticoids at both the Chicago and Indiana sites. Bars represent means and error bars are +1 standard error (SE) (n = 50 for Chicago site and n = 4 for Indiana site). The solid line connects the years from the Indiana site only.

its euryhaline nature (Montschenko 1967) would allow it to tolerate the salinity changes that occur during ballast-water exchange, especially if it was transported while encysted. It was clear that the new invasive species were the numerically dominant taxa in our samples (Figs. 1 and 2). At the Chicago site, H. nr. nunni was significantly more abundant than S. borutzkyi, C. robertcokeri, and N. hibernica (Kruskal–Wallace test statistic = 81.462, df = 3, p < 0.001). Although S. borutzkyi was not as numerous as H. nr. nunni, it was more common than the native C. robertcokeri at this site in December (Fig. 1). Schizopera borutzkyi was absent from sediments at the Indiana site in the August 1996 samples but was collected in very low numbers in samples from 1998 and 1999, although samples were collected at different times of the year. Heteropsyllus nr. nunni was the most numerous harpacticoid at this site in 1996–1999 samples (Fig. 1), but differences in abundance among species were significant only in 1996 (Mann–Whitney U test < 0.001, df = 1, p = 0.018). In the October 2000 samples, H. nr. nunni was the most numerous harpacticoid at the shallower depths (about 550 individuals·m–2 between 5 and 9 m), comprising 80–100% of the harpacticoid taxa (Fig. 2). Schizopera borutzkyi was most numerous at the deepest site (about 3700 individuals·m–2 at 15 m), comprising about 75% of the harpacticoids (Fig. 2); however, it was abundant in the shallower sands at the Chicago site (72 ± 12 individuals·m–2). Relative abundance of the native C. robertcokeri at the Indiana site increased from 2% at 9 m deep to 15% at 15 m deep. Recent invaders? We can not put a date of introduction on S. borutzkyi or H. nr. nunni because few data exist about the historical species composition of harpacticoids in the Great Lakes (see Hudson et al. 1998). We believe that S. borutzkyi could be a recent invader because it did not appear in our samples until 1998 and had not been collected in other intensive surveys in the Great Lakes (Evans and Stewart 1977; Nalepa and Quigley 1985; Hudson et al. 1998). The exotic N. hibernica was found by Hudson et al. (1998), but the harpacticoid communities generally were dominated by the commonly

1263 Fig. 2. Relative abundance of harpacticoid species collected on 28 August 2000 from a single transect at the Indiana site. Percentages are based on the means of three samples, and numbers above the bars are the mean number of harpacticoids collected.

occurring genera Canthocamptus spp., Bryocamptus spp., and Moraria spp. (Hudson et al. 1998). However, Hudson et al. (1998) did not sample southern Lake Michigan, whereas Evans and Stewart (1977) and Nalepa and Quigley (1985) sampled only southeastern Lake Michigan. Heteropsyllus nr. nunni may also be a fairly recent invader for the same reason. It also was not recorded in the above-mentioned studies but has been prevalent in all of our samples beginning in 1996. However, given the high abundances of S. borutzkyi and H. nr. nunni relative to other harpacticoid species, we expect that they would have been collected in the other studies had they been present. Both S. borutzkyi and H. nr. nunni are now common in southern Lake Michigan, but we are uncertain of their distribution beyond our sampling sites. It initially seemed that S. borutzkyi was not well established at the Indiana site, with only a few immature specimens collected in 1998. However, we may have missed sampling their preferred habitat in deeper areas in previous years, although they were found commonly in shallow sands at the Chicago site. Heteropsyllus nr. nunni may be more prevalent in the Great Lakes than realized; a few individuals were collected from Lake St. Clair during the summer of 2000 (P. Hudson, Great Lakes Science Center, Ann Arbor, MI 48105, personal communication). Genetic and molecular tools may give better insight into the timing of introductions and the extent to which populations have established. Ecological implications Our data document that S. borutzkyi and H. nr. nunni have become established in the nearshore habitats of southern Lake Michigan. Heteropsyllus nr. nunni is clearly the most abundant harpacticoid at shallow sites, whereas S. borutzkyi is the most abundant at deeper sites. The ecological implications of these invasions are unclear because little is known about the specific role of harpacticoids in the Great Lakes. It is possible that these invaders negatively affect the native © 2001 NRC Canada



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species, if they are in direct competition for similar resources. Alternatively, the invaders may be using habitats or trophic resources not being used by the native species. We can only speculate about further changes that these invasive species may cause in the nearshore food web, but we can say with some confidence that changes are occurring in the harpacticoid community composition. These changes are similar to changes occurring in the pelagic and other benthic communities, which are experiencing increased numbers of introduced species originating from the Ponto–Caspian region. The presence of N. hibernica and now S. borutzkyi, both species originating from the Ponto–Caspian region, could be additional pieces of an “invasional meltdown” occurring in the Great Lakes (Ricciardi and MacIsaac 2000).

Acknowledgements The authors thank Jason Butcher, Maria Goodrich, Meredith Nevers, and Ellen Oberdick for assistance in the field and laboratory and Douglas Wilcox, Martin Berg, William Perry, and an anonymous reviewer for providing critical review of the manuscript. The authors are grateful to Bruce Coull (University of South Carolina), Frank Fiers (Royal Belgium Institute for Natural Sciences), Rony Huys (The Natural History Museum, London), Janet Reid (Smithsonian Museum), and Judith Williams (Southern Mississippi University) for confirming the identifications of harpacticoids. The authors are especially grateful to Patrick Hudson (USGS, Great Lakes Science Center, Ann Arbor) for his constant assistance with harpacticoid taxonomy. This research was partially funded through grants from the U.S. Army Corps of Engineers (W81G6693165796) and through a cooperative agreement with the Chicago Department of Environment. This article is contribution 1149 of the USGS Great Lakes Science Center.

Can. J. Fish. Aquat. Sci. Vol. 58, 2001 cal survey of ballast water in container ships entering Hong Kong. Hydrobiologia, 352: 201–206. Evans, M.S., and Stewart, J.A. 1977. Epibenthic and benthic microcrustaceans (copepods, cladocerans, ostracods) from a nearshore area in southeastern Lake Michigan. Limnol. Oceanogr. 22: 1059–1066. Fujiwara, M., and Highsmith, R.C. 1997. Harpacticoid copepods: potential link between inbound adult salmon and outbound juvenile salmon. Mar. Ecol. Prog. Ser. 158: 205–216. Gregg, C.S., and Fleeger, J.W. 1998. Grass shrimp Palaemonetes pugio predation on sediment- and stem-dwelling meiofauna: field and laboratory experiments. Mar. Ecol. Prog. Ser. 175: 77–86. Hudson, P.L., Reid, J.W., Lesko, L.T., and Selgeby, J.H. 1998. Cyclopoid and harpacticoid copepods of the Laurentian Great Lakes. Ohio Biol. Surv. Bull. New Ser. 12(2). Lee, C.E., and Bell, M.A. 1999. Causes and consequences of recent freshwater invasions by saltwater animals. Trends Ecol. Evol. 14: 284–288. MacIsaac, H.J., Grigorovich, I.A., Hoyle, J.A., Yan, N.D., and Panov, V.E. 1999. Invasion of Lake Ontario by the Ponto–Caspian predatory cladoceran Cercopagis pengoi. Can. J. Fish. Aquat. Sci. 56: 1–5. Montschenko, V. 1967. Beitrag zur Kenntnis der Gattung Schizopera (Crustacea, Harpacticoida) im Schwarzen Meer. Zool. Anzeig. 178: 367–374. Muzinic, C.J. 2000. First record of Daphnia lumholtzi Sars in the Great Lakes. J. Great Lakes Res. 26: 352–35. Nalepa, T.F., and Quigley, M.A. 1985. Distribution of epibenthic microcrustaceans in nearshore Lake Michigan. Freshwater Invert. Biol. 4: 53–63. Ricciardi, A., and MacIsaac, H.J. 2000. Recent mass invasion of the North American Great Lakes by Ponto–Caspian species. Trends Ecol. Evol. 15: 62–65. Williams-Howze, J., and Coull, B.C. 1992. Are temperature and photoperiod necessary cues for encystment in the marine benthic harpacticoid copepod Heteropsyllus nunni Coull? Biol. Bull. 182: 109–116.

References Chu, K.H., Tam, P.F., Fung, C.H., and Chen, Q.C. 1997. A biologi-

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