Thermocyclops Crassus (Crustacea: Copepoda) Present In North America: A New Record From Lake Champlain

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1 J. Great Lakes Res. 18(3): Internat. Assoc. Great Lakes Res., 1992 Thermocyclops Crassus (Crustacea: Copepoda) Present In North America: A New Record From Lake Champlain Alan Duchovnay 1 School of Natural Resources University of Vermont Burlington, Vermont Janet W. Reid Department of Invertebrate Zoology NHB-163, National Museum of Natural History Smithsonian Institution Washington, D.C Alan McIntosh School of Natural Resources University of Vermont Burlington, Vermont Abstract. The cyclopoid copepod Thermocyclops crassus was collected in Missisquoi Bay, Lake Champlain, Vermont, U.S.A., in May and August Since this is the first confirmed record of the species in North America, the population is considered to be introduced. Thermocyclops crassus is widespread in temperate and tropical Eurasia and Africa, but, in the Americas, has been collected previously only in Costa Rica. It is planktonic and thermophilic, with a preference for eutrophic waters. INDEX WORDS: Cyclopoida, plankton, new record, Lake Champlain, Thermocyclops crassus, eutrophic. Introduction During routine identification of zooplankton from Lake Champlain, Vermont (U.S.A.) in 1991, the cyclopoid copepod Thermocyclops crassus Fischer 1853 was found in abundance in Missisquoi Bay. Thermocyclops crassus is a common plankter of Eurasia and Africa, with a single confirmed American record from Costa Rica. The occurrence in Missisquoi Bay is the first confirmed collection in North America. We describe the environment of Missisquoi Bay and summarize knowledge of the biology of T. crassus, reviewing taxonomic considerations and morphological characters useful in its identification. 1 Corresponding Author

2 Methods Vertical tows from Missisquoi Bay were taken on 10 May and 7 August 1991 with a 0.5 m diameter, 202 µт mesh plankton net. Samples were narcotized with carbonated water and preserved with a 10% formalin-sugar solution. In the laboratory, samples were rinsed to remove formalin and successively split until subsamples contained approximately 200 organisms. Initial plankton identifications were done with an inverted microscope by A. D. Copepods were eventually transferred to a solution of 70% ethanol for long-term storage. Taxonomic confirmations of adults were done by J. W. R. from specimens in glycerine. Missisquoi Bay (Lat '; Long ') lies in the extreme northeastern part of Lake Champlain. It is the shallowest major basin of the lake, with a mean depth of less than 3 m (Myer and Gruendling 1979). Missisquoi Bay has a surface area of 77 km 2, seven percent of the lake's total. There is no reported permanent summer stratification of Missisquoi Bay, and relatively high wind velocities in the area encourage substantial mixing. As a result, the bay's waters are usually turbid (Myer and Gruendling 1979). Missisquoi Bay is eutrophic, with total phosphorus content of its waters ranging from 32 to 41 µg/l in 1990 (Vermont Department of Conservation and New York Department of Environmental Conservation 1991). Substantial nutrient contributions enter the bay from both point and non-point sources along the Pike and Missisquoi rivers (Myer and Gruendling 1979). In contrast to Missisquoi Bay, the rest of the lake is considered mesotrophic, with summer total phosphorus concentrations ranging from 10 to 14 µg/l in 1990 (Vermont Department of Environmental Conservation and New York Department of Environmental Conservation 1991). As a result of the elevated nutrient levels, algal blooms are common in Missisquoi Bay. Chlorophyll a values ranged from 7 to 11 µg/l in 1990, compared to values between 3 and 5 µg/l for the main lake (Vermont Department of Environmental Conservation and New York Department of Environmental Conservation 1991). Our sample program (Shambaugh, unpublished data) indicated that the dominant species of phytoplankton in Missisquoi Bay in the spring of 1991 was the cryptomonad, Chroomonas sp. Earlier observations (Myer and Gruendling 1979) indicated that diatoms such as Melosira italica and Asterionella formosa were most abundant. Results Among the 22 sites sampled throughout Lake Champlain, adults of T. crassus were found only in Missisquoi Bay in Samples taken from the bay on 10 May 1991 contained only immature copepodid stages up to CV, at an abundance of approximately 237 ind/m 3. Nauplii would have passed through the 202 µm mesh net. Samples taken on 7 August 1991 contained both adults and copepodids, approximately 630 ind/m 3. Samples on both dates also contained adults and copepodids of the cyclopoid copepod Mesocyclops edax S. A. Forbes 1891, at abundances of approximately 590 and 630/m 3 in May and August respectively. Voucher specimens of T. crassus from the August 1991 samples were deposited in the collections of the National Museum of Natural History, Smithsonian Institution (USNM ). Adult T. crassus were not present in samples from 20 deep-water sites in Lake Champlain taken in Samples taken in 1977 from Missisquoi Bay inspected by A. D. contained no specimens of T. crassus.

ventral (compressed by cover slip pressure); c, Anal somite and caudal rami,

adjacent medial seta of coxopodite; f, Leg 4 endopodite article 3.

segment, ventral; i, Anal somite and caudal rami, dorsal; j, Antennule article

coxopodite; l, Leg 4 endopodite article 3. Setal plumage omitted in some figures.

3 FIG. 1. Mesocyclops edax, female; a, Habitus, dorsal; b, Pediger 5 and genital segment, ventral (compressed by cover slip pressure); c, Anal somite and caudal rami, dorsal; d, Antennule article 17 and part of article 16; e, Leg 4 coupler and adjacent medial seta of coxopodite; f, Leg 4 endopodite article 3. Thermocyclops crassus, female: g, Habitus, dorsal; h, Pediger 5 and genital segment, ventral; i, Anal somite and caudal rami, dorsal; j, Antennule article 17 and part of article 16; k, Leg 4 coupler and adjacent medial seta of coxopodite; l, Leg 4 endopodite article 3. Setal plumage omitted in some figures. Arrows indicate recognition features described in text. Scales: Figure la, 100 µт; Figures 1b and 1c, 150 µт; Figures 1d-f, 50 µm; corresponding structures of both species to same scale.

4 Discussion Thermocyclops crassus is widespread in Eurasia and Africa, occurring in large and small natural and artificial lakes and reservoirs, and occasionally in rivers [Kiefer 1978, Rylov 1948 (1963)]. The species is primarily pelagic but can also attain high populations among dense littoral immersed macro-phytes [Flossner 1967, Rylov 1948 (1963)]. It is thermophilic and in more temperate regions comprises a significant component of the plankton only during the warmer months. In tropical climates this species is often among the dominant crustacean plankters (Fernando 1980, Hodgkiss 1977, Lewis 1979). It has been collected from waters of ph , but the optimum ph is 7-8 [Rylov 1948 (1963)]. It is tolerant of salinities up to 7.2 (Löffler 1961). It is herbaceous, feeding on diatoms, cryptomonads, and cyanophyceans (Fernando 1980, Lewis 1979), and thrives in mesotrophic and eutrophic waters [Patalas and Patalas 1966, Rylov 1948 (1963)]. Its naupliar stages were described by Manfredi (1925) as Cyclops oithonoides var. hyalina and partially by Kiefer (1973); the copepodid stages were partially described by Andreae (1955) as Cyclops (Mesocyclops) hyalinus. Maturation time can be as short as a few weeks at tropical temperatures, with multiple generations per year (Lewis 1979), although in temperate waters, the species may have as few as two generations annually [Rylov 1948 (1963)]. Thermocyclops crassus may diapause as a CIV or CV copepodid. In several Italian lakes, T. crassus overwinters in the benthos as diapausing copepodid CV stages (Stella et al. 1972; E. Stella, personal communication to J.W.R., 1992), whereas in several German lakes, T. crassus overwinters as a CIV copepodid (Maier 1990). Because of the difficulty of discrimination of T. crassus and similar congeners, information on this species appears in the scientific literature under a confusing variety of names. Kiefer (1978) and Rylov [1948 (1963)] discussed its taxonomic history in detail and provided a list of synonyms, the most common of which is Thermocyclops (or Mesocyclops) hyalinus Rehberg Additional nomenclatural confusion has been caused by the former inclusion of species of Thermocyclops in the genus Mesocyclops, or, in older literature, Cyclops. The inverse of this taxonomic confusion is the multiplicity of erroneous reports of T. crassus. Most published records of T. crassus from the Americas were found by Reid (1989) to refer to the similar pantropical species T. decipiens Kiefer The single exception is the record by Collado et al. (1984) from small ponds in Costa Rica. Kiefer (1978) provided extensive figures of T. crassus and several European congeners. The species was included by Herbst (1986) in his world key to the genus Thermocyclops. Thermocyclops crassus also appears under the name Mesocyclops hyalinus in the key of Yeatman (1959) to North American cyclopoids. Yeatman's decision to include this species, although based on earlier erroneous reports from Central America, appears particularly prescient in the view of the present find. The species was not listed in the key of Pennak (1989) to cyclopoids of the United States. Thermocyclops crassus is the fourth member of the genus now known to inhabit the continental United States. The other species are T. tenuis Marsh 1910, occurring widely in South and Central America and sporadically in the southwestern and central United States as far north as Kentucky; T. inversus Kiefer 1936, a neotropical species recently reported from Louisiana (Marten 1989, Reid 1989); and T. parvus (Reid 1989), from the Florida Everglades. Records of the Eurasian species T. dybowskii Lande 1890 and T. oithonoides G.O. Sars 1863 from the United States are either dubious or proven erroneous (Coker 1943, Reid 1989), although one or both were included in the keys of Pennak (1989) and Yeatman (1959). No member of Thermocyclops is known to inhabit Canada or Alaska. Thermocyclops crassus is superficially similar to the common North American plankter Mesocyclops edax (Fig. 1). Thermocyclops crassus can be distinguished by

5 the lack of hairs on the medial surfaces of the caudal rami; the longest caudal setae which are usually curved anteriorly at the tips in adult individuals; the very narrow and smoothly edged antennular hyaline membrane; the coupler of swimming leg 4 with two large spiny protrusions; and the leg 4 endopodite article 3 with its lateral terminal spine less than half the length of the medial terminal spine. Mesocyclops edax, recently redescribed by Dussart (1985), has haired caudal rami; all caudal setae straight; the antennular hyaline membrane broad and coarsely serrate; the leg 4 coupler with two small unornamented protrusions; and the leg 4 endopodite article 3 medial terminal spine slightly shorter than the lateral terminal spine. The date of introduction of the Lake Champlain population is uncertain. Its localized distribution with the lake indicates that introduction was recent, since other shallow eutrophic areas appear to be as suitable habitat as Missisquoi Bay. The origin and means of introduction are unknown. In spite of its inclusion in the widely used key of Yeatman (1959), T. crassus has not been reported in North America in recent decades. For this reason we do not believe that the species is presently distributed widely on this continent. It is hoped that this note will cause others to re-examine samples identified as M. edax for the presence of T. crassus. The authors would appreciate specimens from other researchers for confirmation. Acknowledgments We thank Dr. C. Herbert Fernando for introducing the first and second authors. We also thank the Melosira boat crew whose collecting assistance made this discovery possible: Captain Richard Furbush, Sally Keefer, Debbie Lester, and Angela Shambaugh. Dr. Emilia Stella provided helpful information on the biology of T. crassus in Italy. Monitoring the plankton of Lake Champlain is being supported by a grant from the Lintilhac Foundation.

Thermocyclops crassus Ecological Risk Screening Summary

U.S. Fish and Wildlife Service Thermocyclops crassus Ecological Risk Screening Summary U.S. Fish and Wildlife Service, October 2016 Photo: Mesocyclops crassus [accepted as Thermocyclops crassus] from Sars,