549 DISCUSSION / DISCUSSION Comment on “Rate of species introductions in the Great Lakes via ships’ ballast water and sediments”1 Janet W. Reid and Patrick L. Hudson Abstract: The four species of freshwater copepod crustaceans found in ballast water or sediments in ships and characterized as “nonindigenous” to the Laurentian Great Lakes region by Drake and Lodge (Can. J. Fish. Aquat. Sci. 64: 530–538 (2007)) are all widespread, North American natives. Drake and Lodge’s use of these native species to estimate the size of the “source pool” of the richness of potential invasive species resulted in an overestimation of its size. We list the fresh- and brackish-water species of copepods found in or on ships in the Great Lakes and discuss taxonomic and other questions pertaining to some of them. We suggest that Skistodiaptomus pallidus, Cyclops strenuus, Salmincola lotae, Nitokra incerta, and Onychocamptus mohammed be removed from the current list of nonindigenous copepod and branchiuran species established in the Great Lakes system, leaving seven species: Eurytemora affinis, Megacyclops viridis, Neoergasilus japonicus, Heteropsyllus nunni, Nitokra hibernica, Schizopera borutzkyi, and Argulus japonicus. Résumé : Les quatre espèces de crustacés copépodes d’eau douce trouvées dans les eaux de ballastage ou les sédiments dans les navires et caractérisées de « non indigènes » à la région des Grands Lacs laurentiens par Drake et Lodge (J. Can. Sci. Halieut. Aquat. 64: 530–538 (2007)) sont toutes des espèces natives de l’Amérique du Nord à large répartition géographique. L’utilisation de ces espèces indigènes par Drake et Lodge dans leur estimation de la taille du « bassin d’origine » de la richesse des espèces envahissantes potentielles mène à une surestimation. Nous dressons une liste des espèces de copépodes d’eaux douce et saumâtre trouvées dans ou sur les navires dans les Grands Lacs et nous discutons de questions taxonomiques ou autres qui concernent certaines d’entre elles. Nous suggérons de retirer Skistodiaptomus pallidus, Cyclops strenuus, Salmincola lotae, Nitokra incerta et Onychocamptus mohammed de la liste actuelle de copépodes et de branchioures non indigènes établis dans le système des Grands Lacs, ce qui laisse sept espèces, soit Eurytemora affinis, Megacyclops viridis, Neoergasilus japonicus, Heteropsyllus nunni, Nitokra hibernica, Schizopera borutzkyi et Argulus japonicus. [Traduit par la Rédaction] Reid and Hudson 553 Drake and Lodge (2007a) presented a list of 17 species of small invertebrates found in ballast water in ships entering the Laurentian Great Lakes and characterized all of the species as “nonindigenous” to the Great Lakes. They then used these data to estimate the size of the “source pool” of the richness of potential invasive species. The seven freshwater species that the authors characterized as nonindigenous include one rotifer, one mysid, one ostracode, and four copepods: Microcyclops rubellus, Microcyclops varicans, Paracyclops chiltoni, and Maraenobiotus insignipes. We question the criteria for terming these copepods nonindigenous. The first three occur widely in North America, including the Great Lakes (Hudson and Lesko 2003). Maraenobiotus insignipes, although not reported from the Great Lakes proper, is widespread in northern North America (Wilson and Yeatman 1959); a juvenile Maraenobiotus sp. was collected in the early 1970s in Lake St. Clair (Hudson and Lesko 2003). Members of this genus are usually found in streams, seeps, and damp moss, so would be unlikely to establish in the Great Lakes proper. Received 31 May 2007. Accepted 30 December 2007. Published on the NRC Research Press Web site at cjfas.nrc.ca on 19 February 2008. J20024 J.W. Reid.2,3 Research Associate, Virginia Museum of Natural History, Martinsville, VA 24112, USA. P.L. Hudson. Emeritus, USGS Great Lakes Science Center, 1451 Green Road, Ann Arbor, MI 48105, USA. 1 Appears in Can. J. Fish. Aquat. Sci. 64: 530–538 (2007). Corresponding author (e-mail: jwrassociates@sitestar.net). 3 Present address: JWR Associates, 1100 Cherokee Court, Martinsville, VA 24112, USA. 2 Can. J. Fish. Aquat. Sci. 65: 549–553 (2008) doi:10.1139/F08-018 © 2008 NRC Canada 550 Can. J. Fish. Aquat. Sci. Vol. 65, 2008 Table 1. Nonindigenous species of copepod and branchiuran crustaceans established in the Laurentian Great Lakes system. Year discovered Lake(s) recorded from North America, Europe (estuaries); brackish to freshwater 1958 All Megacyclops viridis Europe; freshwater 1989 Superior Neoergasilus japonicus East Asia; introduced into Cuba and Europe; ectoparasite of freshwater fishes East coast of North America (estuaries); brackish to freshwater 1994 Huron 1996 2000 Michigan St. Clair Nitokra hibernica Eurasia; brackish to freshwater 1973 Huron, Michigan, Erie, Ontario Schizopera borutzkyi Ponto-Caspian; brackish to freshwater 1998 2003 Michigan Erie Argulus japonicus Asia; now found on most continents; ectoparasite of freshwater fishes 1989 Huron, Michigan, Erie Species Native distribution Eurytemora affinis Heteropsyllus nunni The analysis of these collection data to estimate the rate of species introduction into the Great Lakes appears to us to suffer from mischaracterization of a high proportion of the freshwater species as nonindigenous. The result is a serious overestimation of the pool of potential invaders. We encourage Drake and Lodge to recalculate their estimates after consulting with taxonomic experts for all of the groups listed in their article. Some other publications listing copepods found in ships in the Laurentian system include instances of, in our view, similar mischaracterizations of the native distributions and (or) taxonomy of certain species. We list the species of copepods found in the Great Lakes system that we consider to be nonindigenous (Table 1). For consistency, we adopted the definition of a nonindigenous species as “The condition of a species being moved beyond its natural range or natural zone of potential dispersal …” from the Nonindigenous Aquatic Nuisance Prevention and Control Act of 1990 (Public Law 101-646, 16 USC 4701-4741, approved 29 November 1990). Our purpose here is to discuss only species considered to have been moved by human activities, rather than those that may have expanded their ranges naturally. Below, we discuss some species that have been mentioned in other publications and that present taxonomic or distributional problems. We have placed each of the species into categories for ease of classifying taxa in future studies of invasion biology (Table 2). A cryptogenic species is a spe- Recent references Hudson and Lesko 2003; Great Lakes Environmental Research Laboratory (GLERL) 2006 Hudson and Lesko 2003; Great Lakes Environmental Research Laboratory (GLERL) 2006 Grigorovich et al. 2003; Great Lakes Environmental Research Laboratory (GLERL) 2006 Grigorovich et al. 2003; Hudson and Lesko 2003; Holeck et al. 2004; Great Lakes Environmental Research Laboratory (GLERL) 2006 Grigorovich et al. 2003; Hudson and Lesko 2003; Holeck et al. 2004; Great Lakes Environmental Research Laboratory (GLERL) 2006 Grigorovich et al. 2003; Hudson and Lesko 2003; Holeck et al. 2004; Great Lakes Environmental Research Laboratory (GLERL) 2006 Mills et al. 1993; Grigorovich et al. 2003; Hudson and Lesko 2003; Great Lakes Environmental Research Laboratory (GLERL) 2006 cies that is not demonstrably native or introduced (Carlton 1996). Skistodiaptomus pallidus: occurs throughout the central and northeastern United States in ponds, lakes, and rivers. It has been recorded from Lakes Huron, Erie, St. Clair, and Ontario (Hudson and Lesko 2003), where it is considered as introduced by some (e.g., Mills et al. 1993). Individuals may occasionally be flushed from nearby stream–wetland complexes into the lakes proper, where they will likely not persist. Therefore, S. pallidus should be removed from the list of accidentally introduced species. Acanthocyclops americanus: reported from ballast water by Locke et al. (1993), who termed it a potential invader. This taxon is not currently recognized as valid. It is a member of the controversial vernalis–robustus species complex, discussed below. Acanthocyclops exilis: reported from ship hulls by Drake and Lodge (2007b) and is widespread in eastern North America, mainly in springs and small streams. Like S. pallidus, we consider it unlikely to become established in the Great Lakes proper. Acanthocyclops robustus: the robustus–vernalis group remains incompletely understood (e.g., Dodson et al. 2003; Grishanin et al. 2006) and is so problematical from a morphological standpoint that it is difficult or impossible to ascertain whether old records or new collections represent a new introduction, without genetic analyses. © 2008 NRC Canada Reid and Hudson 551 Table 2. Reasons for excluding copepod species from analyses of introductions. Reason for exclusion Copepod species Cryptogenic species Acanthocyclops robustus, Eucyclops agilis, Eucyclops serrulatus, Onychocamptus mohammed Bryocamptus pygmaeus, Canthocamptus staphylinus, Nitokra incerta, Thermocyclops crassus Cyclops strenuus, Skistodiaptomus pallidus Potential invader Nonindigenous to Great Lakes proper, but with natural dispersal mechanisms Cannot become established (marine or estuarine species) Unlikely to become established (different habitat requirements) Invalid taxon Cyclops strenuus: supposedly a circumboreal species found in Alaska and northern Canada and has been collected rarely in Lake Superior. Holeck et al. (2004) included range extension and (or) natural dispersal among the possible modes of entry into the lake. Furthermore, North American records of C. strenuus may refer to the similar Cyclops canadensis (Ho»y½ska and Dahms 2004). We recommend removal of C. strenuus from the list of nonindigenous species. Eucyclops agilis and Eucyclops serrulatus: in view of continuing revision of the serrulatus group (e.g., Alekseev et al. 2006), it is difficult to reliably assign morphs found outside Europe to one or another named species. Megacyclops viridis: a Palaearctic species that was reported from Duluth Harbor in Lake Superior by Hudson et al. (1998). It is likely to have been introduced into that harbor, but the extent of its spread, if any, should be assessed. Oithona similis: characterized as a “freshwater” species by Drake and Lodge (2007b); it is actually euryhaline– marine pelagic, unlikely to establish in the Great Lakes. Thermocyclops crassus: reported from Lake Champlain by Duchovnay et al. (1992). Although this Palaearctic species has not yet been found in the Great Lakes proper, investigators should remain alert to its possible appearance. Bryocamptus pygmaeus and Canthocamptus staphylinus: European harpacticoids that were reported from ballast water by Duggan et al. (2005). In spite of early records and inclusion in North American keys (e.g., Wilson and Yeatman 1959), we consider that both species are potential invaders. Heteropsyllus nunni: native to estuaries of eastern North America (Hudson and Lesko 2003), not a Eurasian species as characterized by Grigorovich et al. (2003). Nitokra incerta: reported from the Detroit River by Grigorovich et al. (2001). We are unaware of any reports since that time. Pending further field studies, we suggest that N. incerta be removed from the list of established nonindigenous species. Onychocamptus mohammed: occurs on most continents, in estuaries or near-coastal fresh waters; it was collected in Lake Huron in 1974–1975 and since found in Lakes Erie, Huron, Ontario, and St. Clair (Hudson and Lesko 2003). Although it has been recorded from ballast water (Duggan et al. 2005; Johengen et al. 2005), its presence in the Great Lakes may well be the result of a natural range extension. Taking a conservative point of view, O. mohammed should be excluded from studies of human-mediated invasion, in agreement with Ricciardi (2006). Oithona similis and other coastal or marine planktonic species Acanthocyclops exilis, Maraenobiotus insignipes Acanthocyclops americanus Salmincola lotae: a parasite of Palaearctic fishes, also recorded from burbot (Lota lota) in the Northwest Territories (Stewart and Bernier 1983, 1999) and in Lake Superior (Lasee et al. 1988). Although Hudson and Bowen (2002) suggested that the Lake Superior population might have been introduced, based on the above records we now consider that S. lotae occurs naturally in the Nearctic. To date, more than 70 fresh- or brackish-water taxa of copepods have been recorded from ballast water, tank sediments, or hulls of ships in the Laurentian Great Lakes. Most of these were listed by Duggan et al. (2005), Johengen et al. (2005), or Drake and Lodge (2007a, 2007b). Species that are clearly not indigenous to the lakes include the following freshwater Palaearctic natives: Acanthocyclops venustus, Cyclops abyssorum, Mesocyclops leuckarti, Paracyclops fimbriatus, Thermocyclops crassus, Thermocyclops oithonoides, Bryocamptus pygmaeus, and Canthocamptus staphylinus; and the normally coastal brackish-water or euryhaline Eurytemora affinis, Cyclopina littoralis, Ameira parvula, Halectinosoma curticorne, Mesochra pygmaea, Microarthridion littorale, Microsetella norwegica, Nitokra affinis, Nitokra hibernica, Schizopera baltica, Schizopera borutzkyi, Schizopera knabeni, Tachidius littoralis, Tisbe furcata, and Tisbe gracilis. Native species found in the general region include Epischura lacustris, Leptodiaptomus minutus, Leptodiaptomus siciloides, Senecella calanoides, Acanthocyclops brevispinosus, Diacyclops nanus, Diacyclops navus, Diacyclops nearcticus, Diacyclops thomasi, Eucyclops prionophorus, Macrocyclops albidus, Mesocyclops americanus, Mesocyclops edax, Microcyclops rubellus, Microcyclops varicans, Orthocyclops modestus, Paracyclops chiltoni, Tropocyclops prasinus, Bryocamptus zschokkei, Canthocamptus robertcokeri, Canthocamptus staphylinoides, Maraenobiotus insignipes, Mesochra alaskana, Nitokra lacustris, Nitokra spinipes, Onychocamptus mohammed, and Salmincola lotae. Undetermined species that may or may not have been natives, some of which were reported by Harvey et al. (1999), include Diaptomus sp., Eurytemora sp., Acanthocyclops spp., Cyclops sp., Diacyclops sp., Halicyclops sp., Mesocyclops sp., Paracyclops sp., Ameira sp., Maraenobiotus sp., Mesochra sp., Nitokra spp., and Schizopera sp. Records of Acanthocyclops americanus, Acanthocyclops exilis, Acanthocyclops robustus, Acanthocyclops vernalis, Cyclops strenuus, Eucyclops agilis, Eucyclops serrulatus, Megacyclops viridis, Oithona similis, and Salmincola lotae present taxonomic or other problems, as discussed above. In the study by Drake and Lodge (2007a) and some reports by others, the lack of familiarity of the authors or their © 2008 NRC Canada 552 taxonomic consultants with the current literature on North American copepods is apparent. These flaws raise suspicion that taxonomic treatment of other groups may suffer from similar inadequacies. Although a single individual cannot be expected to be competent in all freshwater taxa, up-to-date regional keys now exist for copepods and some other zooplankton groups (e.g., Hudson and Lesko 2003; Aliberti et al. 2003). In view of the current unstable taxonomy of copepods and many other groups of freshwater invertebrates, certain minimum criteria should be met in assessing whether a new record represents an introduction. First, the specimens must be examined by an experienced specialist. The likelihood of introduction should be evaluated based on the historical taxonomy and the species’ known distribution and life-history characteristics, as exemplified by Mills et al. (1993) and Duggan et al. (2005), using the criteria for introduction proposed by Chapman and Carlton (1991). Second, voucher specimens should be deposited in a public institution. We have not located any reports on organisms found in ballast water that stated that voucher specimens were archived in permanent collections. Vouchers are the only means of verifying taxonomic determinations and also can provide a resource for further explorations of genetic differences that could assist in identifying the actual geographical origin of specimens. Third, to be considered as established, the species should be collected at least twice, from different localities or different time periods, with multiple life stages. Fourth, information on the species should be entered into an appropriate website, with illustrations and information on identification, distribution, life history, ecology, and taxonomic synonyms. No one disputes that many nonindigenous aquatic vertebrates, invertebrates, and plants have invaded the Laurentian system, but because of low densities, they are not detected, recognized, or do not persist. Our concern is that organisms should be examined by experienced taxonomists. 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