Journal of the Oceanographical Society of Japan Vol.42, pp.124 to 133, 1986

Redescription of the Planktonic Calanoid hudsonica from Atlantic and Pacific Waters: A New Record from Japanese Waters*

Hiroshi Ueda•õ

Abstract: The neritic planktonic copepod is redescribed from the Atlantic and Pacific coasts of and newly from Japanese waters. This species formerly has been identified as A. clausi in the Northwest Pacific. The Atlantic and Pacific populations cannot be morphologically separated even in fine ornamentation; the variations found in the two populations overlap each other. Prosome length/width ratio of the female is negatively correlated with the body size and the ratio is not significantly different between Atlantic and Pacific females of the same size. The length/width ratio of the genital segment of Pacific females is positively correlated with their body size, and the mean value of the ratio for Atlantic females is smaller than that expected for Pacific females of the same size. The size-temperature relationship differs among localities but it is uncertain whether there is a genetic difference in copepod size between the Atlantic and Pacific populations.

1. Introduction specimens from the Atlantic coast of North Acartia (Acartiura) clausi Giesbrecht has been America, and with specimens from San Juan known as an abundant and widespread plank- Island, Puget Sound, on the Pacific coast of the tonic calanoid copepod in Japanese inlet waters United States, which Bradford (1976) described and as a good indicator species of these waters as an uncertain species apparently identical with (Yamazi, 1956). Bradford (1976), however, A. hudsonica except for their body size and some making a revision of Acartiura species, dis- fine ornamentation. In this paper A.hudsonica tinguished the Japanese A. clausi from Gies- is redescribed from several Atlantic and Pacific brecht's A. clausi s. str. and described the new localities; particular attention is given to fine species A. omorii from Tokyo Bay. During the ornamentation and female body proportions. course of an ecological study on plankton cope- Relationships between copepod size and temper- pods in Maizuru Bay, an inlet of Wakasa Bay ature in Maizuru Bay and Akkeshi Bay are also on the Japan Sea coast of middle Japan, I found described. two types of which could be previously attributed to A. clausi. According to Bradford's 2. Materials and methods revision, one of them was identified as A. omorii The following Atlantic specimens were ex- and the other A. hudsonica Pinhey; the latter amined: about 60 females from Chesapeake Bay species is widespread in coastal waters between (38•‹20'N, 76•‹15'W), 17 March 1939; about 40 Hudson Bay and Chesapeake Bay, North America, females and 20 males from Montauk Bay, Long but has not been recorded from the Northwest Island Sound (41•‹02'N, 71•‹57'W), 20 June 1972. Pacific. Specimens identified as A. hudsonica Pacific specimens examined in detail were: about also were collected from Akkeshi Bay, east 60 females and 20 males from Maizuru Bay

Hokkaido. Because copepods previously attribu- (35•‹29'N, 135•‹22'E), 19 March 1984; 40 females ted to A. clausi are very similar, the Japanese and 10 males from Akkeshi Bay (43•‹00'N, specimens were compared with A. hudsonica 144•‹50'E), 27 May and 23 August 1982; 21 * Received 29 November 1985; in revised form 4 females and 12 males from Jakle's Lagoon on April 1986; accepted 14 April 1986. San Juan Island, Puget Sound, Washington, 30 † Department of Marine Sciences, College of May 1985. More than 800 females collected Science, University of the Ryukyus, Nishihara- generally at 2-4 days intervals from 6 January to cho, Okinawa 903-01, Japan 29 May 1978 from Maizuru Bay, and 45 females Redescription of Acartia hudsonica 125

collected on 9 September and 5 October 1982 and Acartia hudsonica, Bradford, 1976: P. 176, figs. 6 August 1985 from Akkeshi Bay were measured 14-16. to obtain size-temperature relationships. Acartia sp. from San Juan Island, Bradford, Examination and measurements were made of 1976: p.179, fig. 17. specimens in 70 % lactic acid or 50 % glycerin ? Acartia (Acartiura) clausi, Brodsky, 1950: with a compound microscope with ocular micro- p.420, fig. 296. meter. Specimens examined for fine hairs or Body length: Chesapeake Bay females, 1.00- spinules and for illustration were stained with 1.32 mm. Long Island Sound females, 1.05-1.13 chlorazol black E then examined with a differ- mm, males, 0.97-1.07 mm. Maizuru Bay, 19' ential interference microscope with drawing-tube March 1984, females, 0.92-1.10 mm, males, attachment. In addition, fine ornamentation on 0.86-0.93 mm; 13 June 1978, females, 0.81-0.92 the metasome and urosome was examined with mm. Akkeshi Bay, 27 May 1982, females, 1.09- a scanning electron microscope (SEM). For this 1.17 mm, males, 0.94-1.00 mm; 23 August 1982, purpose, copepods were prepared by standard females, 0.78-0.95mm. San Juan Island fe- critical point drying techniques prior to gold males, 0.74-0.85mm, males 0.71-0.84 mm. coating. Water temperatures in Maizuru Bay Ornamentation: The following details are used in the size-temperature correlation were redescribed or added to Bradford's (1976) de- measured at the surface at each sampling time scription of A. hudsonica. with a salinity-temperature indicator. Temper- a) Atlantic specimens (Figs. 1A-D, I; 2A, B,D) ature in Akkeshi Bay is based on daily records Female: Posterolateral corner of metasome taken by the Akkeshi Marine Biological Station, usually with a few fine hairs. First urosomal Hokkaido University. segment (genital segment) usually with a few irregular rows of very minute spinules on ventro- 3. Description lateral surfaces; posterodorsal margin without Acartia (Acartiura) hudsonica Pinhey, 1926 spines or spinules. Second segment usually with hudsonica Pinhey, 1926: p. 184, very minute hair-like spinules on posterodorsal figs.3,4. margin (Fig. 2A). Third segment (anal segment)

A I B C D

J

K F H E G

Fig. 1. Acartia hudsonica, female and male. A-H, urosome of female, dorsal and lateral views: A, B, Long Island Sound; C, D, Chesapeake Bay; E, F, Maizuru Bay (19 March 1984); G, H, San Juan Island. I-K, P5 of male, anterior views: I, Long Island Sound; J, Maizuru Bay (19 March 1984); K, San Juan Island. 126 Ueda naked or sometimes with some fine hairs on Male: Posterolateral corner of metasome dorsal and lateral surfaces. Caudal rami'usually with several hairs (Fig. 2D) usually in two rows with a few small spines on outer posterodorsal and more conspicuous than those of female. margin, numerous fine hairs on lateral margin First urosomal segment with lateral hairs; 2nd- and a few minute hair-like spinules at distal 5th segments with very minute hair-like spinules end of lateral margin. on dorsal and/or lateral surfaces (Fig. 2B); 5th

Table 1. Prosome length and body proportions of Acartia hudsonica females from various Atlantic and Pacific localities. PL and PW, prosome length and width; GL and GW, genital segment length and width; RL and RW, right caudal ramus length and width (see Fig. 1). Redescription of Acartia hudsonica

PLATE I

A D

B E

C F

Fig. 2. SEM photographs showing fine ornamentation of Acartia hudsonica . A-C, hair-like spinules on urosome, dorsal views: A, Long Island Sound female, 2nd segment (left); B, Long Island Sound male, 2nd (right) to 5th (left) segments; C , San Juan Island male, 2nd (left) to 5th (right) segments. D-F, posterior hairs on metasome of males: D , Long Island Sound; E, Maizuru Bay (19 March 1984); F , San Juan Island. Redescription of Acartia hudsonica 129 segment sometimes with several fine hairs on lation between the prosome length/width ratio ventral surface. Caudal rami usually with a and body size (Fig. 3), and the mean ratio does few, small spines on outer posterodorsal margin, not significantly differ between Atlantic and with very minute hair-like spinules on dorsal Pacific females of the same size (e.g., between. surface, and with several fine hairs on lateral the specimens from Long Island Sound and and medial margins. Second segment of left 5th Akkeshi Bay, 27 May 1982). The length/width leg (P5) usually with one or two small spines ratio of the genital segment is positively corre- on anterior surface. lated with body size in Pacific females (Fig. 4). b) Pacific specimens (Figs. 1E-H, J, K; 2C, This ratio differs between the Atlantic and Pacific E, F) populations, although the variations found in the Female: Posterolateral corner of metasome two populations considerably overlap; the mean without hairs. Second and 3rd urosomal seg- values of the ratio for the Chesapeake Bay and ments without spinules or hairs. Other orna- Long Island Sound specimens were significantly mentation similar to Atlantic females. (P<0.05) smaller than those expected for Pacific Male : Posterolateral corner of metasome with females of the same size. The caudal ramus several hairs (Figs. 2E, F) which are usually in length/width ratio varies greatly and there is two rows as in the Atlantic male. Spinules no notable difference in this ratio between the and hairs on 2nd to 5th urosomal segments and Atlantic and Pacific populations. caudal rami vary depending on the localities; Size-temperature relationship: It is well these fine structures usually absent in the speci- known that in waters with a wide annual mens from Maizuru Bay, but usually present in temperature range there is a negative relation the specimens from Akkeshi Bay (27 May 1982) ship between copepod size and temperature. and San Juan Island (Fig. 2C). Other orna- The relationship is well described by Belehradek's mentation similar to Atlantic males. function (McLaren, 1963). Because the adult Body proportions: Measurements of body size depends on conditions during the naupliar proportions of Acartia hudsonica females are and copepodite stages, and because the in situ given in Table 1. There is a negative corre- generation time of A. clausi s.l. is generally a

Fig. 3. Relationship between prosome length (PL) and ratio (PL/PW) of adult female Acartia hudsonica. 130 Ueda

Fig. 4. Relationship between prosome length(PL) and genital segment ratio(GL/GW) of adult female Acartia hudsonica. Regression line pertains to the Pacific specimens only.

Fig. 5. Relationships between mean prosome length(PL) of adult female Acartia hudsonica and water temperature averaged for a month previous to sampling in Long Island Sound (1952-1953), Maizuru Bay(1978) and Akkeshi Bay(1982 and 1985). The data of PL and temperature in Long Island Sound are cited from Deevey(1960, Fig. 7 and Table 4). Redescription of Acartia hudsonica 131

month or more (Ueda, 1978), the correlation coasts of the United States, and concluded that

between the length and the temperature averaged the populations have diverged enough to be at least for a month previous to sampling is the reproductively isolated. The Atlantic copepods

most meaningful. used in their experiment are certainly considered Relationships between the mean prosome to be A. hudsonica, because it is the only

length of the female and the temperature aver- species formerly identified as A. clausi from the

aged for the previous month in Maizuru Bay Atlantic coast of the United States. However, and Akkeshi Bay are shown in Fig. 5, in which there are at least two species which could be

the relationship based on the data obtained in attributed to A. clausi on the Pacific coast Long Island Sound by Deevey (1960) is also (Bradford, 1976), and there are two forms presented. The regression curve expressed by (species) sharing the name A. clausi in Yaquina Belehradek's function for the Maizuru Bay popu- Bay (Frolander et al., 1973), where the experi-

lation was far below that for the Long Island mental copepods were collected. Carrillo et al. Sound population, indicating that copepods in described an indentation on the posterodorsal Maizuru bay are much smaller than those at margin of the fourth urosomal segment of the the same temperature in Long Island Sound. male as a distinctive character of the Pacific

Although the number of data was small, the copepods that they used for the experiment. specimens from Akkeshi Bay exhibited a quite The males of Pacific A. hudsonica examined in different size-temperature relationship. Their the present study have no such indentation, mean lengths at averaged temperatures higher suggesting that their experimental from than 16•Ž (23 August, 9 September and 5 Oc- Yaquina Bay were not A. hudsonica. However, tober 1982) were closer to those expected for considering that their interbreeding experiments the Maizuru Bay specimens, while the sizes at produced small numbers of females with sper- temperatures lower than 14•Ž (27 May 1982 and matophores, and nauplii, their copepods from

6 August 1985) were much larger than those Yaquina Bay may have partly contained A. expected for the Maizuru Bay specimens and hudsonica. Although they explained the appear- beyond even those for the Long Island Sound ance of nauplii as due to experimental error, the specimens. result also could indicate incomplete reproductive isolation between the Atlantic and Pacific popu- 4. Discussion lations of A. hudsonica. Since copepods formerly Atlantic and Pacific specimens considered here attributed to A. clausi were found round the belong to a single species, Acartia hudsonica. north coast of North America, e.g., Hudson Bay Males and females from several Atlantic and (Pinhey, 1926-he original description of A. Pacific localities exhibit variations in size, and hudsonica), Point Barrow (Johnson, 1958) and ornamentation of body and appendage segments. the South Beaufort Sea (Grainger, 1965), the In some cases (e.g. body length) these variations Atlantic and Pacific populations of A. hudsonica show discrete separation among different locali- are probably connected by populations along the ties. However there is considerable overlap Arctic coasts of North America. among specimens from both oceans. Bradford Difference in copepod size is apparent between

(1976, p. 179) noted that the Atlantic and Pacific the specimens from Long Island Sound and specimens differed in the posterior hairs on the Maizuru Bay. However, this does not neces- metasome which were absent on her Pacific sarily mean that there is a significant size differ- specimens. However, Pacific males examined ence between the Atlantic and Pacific popu- in the present study always have these hairs lations, because copepods as large as those in

(Figs. 2E and F), as have the Atlantic males, Long Island Sound occur in Akkeshi Bay at and some Atlantic females lack these hairs as the same temperature. Jakle's Lagoon on San do the Pacific females. Juan Island, the Pacific coast of the United Both Atlantic and Pacific populations of Acartia States, also produces large copepods (>0.80 mm hudsonica formerly have been identified as A. in female prosome length) of Acartia hudsonica clausi. Carrillo et al. (1974) interbred specimens (reported as A. clausii) during the winter, in attributed to A. clausi from Atlantic and Pacific spite of the extreme reduction in size (<0.60 mm) 132 Ueda during the summer(Landry, 1978). It is diffi- of the New Zealand Oceanographic Institute for cult to interpret this complex geographical size their critical reading of the manuscript and use- variation. The difference between the Long Island ful suggestions. Sound and Maizuru Bay populations may re- present a latitudinal genetic variation(Lonsdale References and Levinton, 1985). The extremely small bodies Bradford, J. M.(1976): Partial revision of the Acartia of the Pacific specimens during the warmer subgenus Acartiura(Copepoda: : season may be due to some environmental factors ). N. Z. J. Mar. Freshw. Res., 10, other than temperature or to other non-genetic 159-202. causes. Landry(1978) suggested that the length Brodsky, K. A.(1950): Calanoida of the Far Eastern of A. hudsonica in Jakle's Lagoon is limited by Seas and Polar Basin of the USSR. Key to the some mechanism related to availability or utili- Fauna of the USSR, no.35. Izdatel'stvo Akade- zation of food except during the winter and mii Nauk SSSR, Moskva-Leningrad, 440 pp. (translated from Russian by I. P. S. T., Jersalem, early spring. More investigations into the 1967) seasonal change of the length in other Atlantic Carrillo, E. B. -G., C. B. Miller and P. H. Wiebe(1974): and Pacific localities are needed to explain size Failure of interbreeding between Atlantic and variation of A. hudsonica. Pacific populations of the marine calanoid copepod Copepods formerly attributed to Acartia clausi Acartia clausi Giesbrecht. Limnol. Oceanogr., in the Northwest Pacific consist of at least two 19, 452-458. species, i.e. A. omorii and A. hudsonica. Among Deevey, G. B.(1960): Relative effects of temperature the previous descriptions of A. clausi from the and food on seasonal variations in length of Northwest Pacific, Brodsky's(1950) A. clausi marine copepods in some eastern American and may be identical with A. hudsonica, judging western European waters. Bull. Bingham Oceano- from his drawings in which the genital segment gr. Coll., 17, 54-86. Frolander, H. F., C. B. Miller, M. J. Flynn, S. C. Myers of the female is long and the inner projection on and S. T. Zimmerman(1973): Seasonal cycles of the third segment of the right fifth leg of the abundance in populations of Yaquina male has a rounded distal end; in A. omorii, Bay, Oregon. Mar. Biol., 21, 277-288. the genital segment of the female is relatively Grainger, E. H.(1965): Zooplankton from the Arctic short and the inner projection of the right fifth Ocean and adjacent Canadian waters. J. Fish. leg of the male has two unequal distal processes Res. Bd. Canada, 22, 543-564. (Bradford, 1976). Johnson, M. W.(1958): Observations on inshore plankton collected during summer 1957 at Point Acknowledgements Barrow, Alaska. J. Mar. Res., 17, 272-281. Specimens from Chesapeake Bay were made Landry, M. R.(1978): Population dynamics and pro- available by T. E. Bowman and from Long duction of a planktonic marine copepod, Acartia clausii, in a small temperate lagoon on San Juan Island Sound by F. D. Ferrari both of the Smith- Island, Washington. Int. Revue ges. Hydrobiol., sonian Institution; from San Juan Island by 63, 77-119. Gayle A. Heron of the University of Washing- Lonsdale, D. J. and J. S. Levinton(1985): Latitudinal ton(these specimens were collected by M. J. differentiation in embryonic duration, egg size, Dagg of the Louisiana Universities Marine Con- and newborn survival in a harpacticoid copepod. sortium) from Akkeshi Bay by T. Irie of the Biol. Bull., 168, 419-431. Hokkaido Regional Fisheries Research Labora- McLaren, I. A.(1963): Effects of temperature on tory; the data of temperature in Akkeshi Bay growth of zooplankton, and the adaptive value were provided by K. Kitada of the Akkeshi of vertical migration. J. Fish. Res. Bd. Canada, Marine Biological Station, Hokkaido University. 20, 685-727. I wish to thank them for their kind cooperation. Pinhey, K. F.(1926): Entomostraca of the Belle Isle Strait Expedition, 1923, with notes on other I am grateful to T. Yamasu and H. Ujiie of planktonic species. Contr. Canadian Biol. Fish., the University of the Ryukyus for their technical N. S., 3, 181-233. support in making the SEM examinations. Ueda, H. (1978): Analysis of the generations of inlet Special thanks are also due to F. D. Ferrari of copepods, with special reference to Acartia clausi the Smithsonian Institution and J. M. Bradford in Maizuru Bay, middle Japan. Bull. Plankont Redescription of Acaria hudsonica 133

Soc. Japan, 25, 55-66.(in Japanese with English characteristics and classification of inlet waters abstract) based on the plankton communities. Publ. Seto Yamazi, I.(1956): Plankton investigation in inlet Mar. Biol. Lab., 5, 157-193. waters along the coast of Japan XIX. Regional

大 西 洋 お よび太 平 洋 域 か らの 浮遊 性 カ ラ ヌ ス 目焼 脚 類Acaria kudsonicaの 再 記 載:日 本 近 海 に お け る新 記 録

上 田 拓 史*

要 旨:内 湾 性 浮 遊 性焼 脚 類Acartia hudsonicaを 北 米 東 は体の大きさと負の相関をなし,同 体長の大西洋 と太平 西 両岸 お よ び新 た に 日本近 海 か ら再記 載 し た.こ の種 は 洋産個体の間でその比に有意な違いは認め られない.太 西 部 北太 平 洋 域 に お い て これ までA.clausiと し て 同定 平洋産雌の生殖節の長さ/幅 の比は体長と正の相関をな され てい た.大 西 洋 と太 平 洋 の 個 体 群 に み られ る変 異 は し,大 西洋産雌におけるその平均的な比の値は同体長の 互 いに 重 複 し,微 細 な毛 や 棘 に お い て も両 個 体 群 を形 態 太平洋産雌の値より小さい.体 長 と水温の関係は地理的 的 に分 け る こ と はで き ない.雌 の 前体 部 の 長 さ/幅 の 比 に異なるが,大 西洋と太平洋個体群の間で個体の大きさ

*琉 球 大 学 理 学 部 海 洋 学 科 〒903-01沖 縄県 西 原 町 に遺伝的な相違があるかどうかは不明である.