Title Morphological Comparison of Feeding Appendages of and

Author(s) YAMAGUCHI, Atsushi; DALPADADO, Padmini; IKEDA, Tsutomu

Citation 北海道大学水産科学研究彙報, 54(3), 59-65

Issue Date 2003-12

Doc URL http://hdl.handle.net/2115/21984

Type bulletin (article)

File Information 54(3)_P59-65.pdf

Instructions for use

Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP Bull. Fish. Sci. Hokkaido Univ. 54(3), 59-65, 2003.

Morpbological Comparison of Feeding Appendages of Calanus and Neocalanus Copepods

l 2 Atsushi YAMAGUCHI ), Padmini DALPADAD0 ) and Tsutomu IKEDA l )

Abstract

Morphological comparison of feeding appendages was made for copepods dominating in some regions in world oceans; including Calanus ftnmarchicus (C6 females) and C. hyperboreus (C6 females) in the subarctic Atlantic, C. marshallae (C5), C. pacijicus (C6 females), (CI-C5) and N. jfemingeri (C2- C5), and N. cristatus (CI-C5) in the subarctic Pacific, and N. tonsus (C5 and C6 females) in the subantarctic Pacific. Cluster analysis based on the length measurements of 11 parts of the appendages revealed admixture of four distinct groups (Group A to D). Of the four groups, the two (Groups A and C) are for Calanus spp. and the other two (B and D) are for Neocalanus spp. The two groups of each are characterized by smaller (Groups A and B) and larger (C and D) appendages relative to the prosome length. Possible functional relation­ ships between the relative size of appendages and feeding activity, growth rate and generation length are discussed.

Key words: Feeding appendages, Copepods, , Calanus, Neocalanus

Introduction and Neocalanus species (N. robustior and N. gracilis; Mullin and Evans, 1976). Since the feeding mechanism Copepods belonging to the genera Calanus and of the species within the family Calanidae appears to be Neocalanus (: Calanidae) include large­ more or less similar, the size of mouthparts might bear a sized species and are the dominant component of zoo­ more direct relationship to their preference for foods, i.e., plankton biomass in high latitude seas. F or example, larger mouthparts being necessary to feed on larger Calanus jinmarchicus alone occupy 40-80% of particles (Mullin, 1969; Mullin and Evans, 1976). On biomass at OWS I in the North Atlantic (Williams and this basis, we compared mouthpart morphology of a Conway, 1988), Neocalanus spp. together with total of 20 copepodid stages of 8 Calanidae copepods : Eucalanus bungii make up 70-80% of the zooplankton e.g., Calanus jinmarchicus (Gunnerus) and C. hyperbor­ biomass in summer of the Bering Sea (Heinrich, 1962). eus Kr0yer from the North Atlantic; and Calanus Because of such the high abundance and large body size, pacificus Brodsky, C. marshallae Frost, Neocalanus Calanidae copepods are considered to exert a significant plumchrus (Marukawa), N. jfemingeri Miller, and N. impact on the structure of food webs through their cristatus (Kr0yer) from the subarctic Pacific and grazing on microplankton (Harris, 1996), predation by Neocalanus tonsus (Brady) from the subantarctic Pacific. at higher trophic levels (Beamish et aI., 1999), While morphological differences between the genera and mediating vertical fluxes of biogenic particulate and Calanus and Neocalanus are subtle (Bradford and dissolved materials (cf. Morales, 1999; Bradford-Grieve Jillett, 1974) the validity of the separation has been et aI., 2001). supported by the recent nucleotid sequence data of Calanidae copepods have been known as omnivores, nuclear 18S rONA and mitochondrial 16SrDNA genes and feed on a wide size-spectrum of organisms occur­ (Taniguchi et aI., unpublished data). ring in nature (Gifford, 1993; Harris, 1996). Morphol­ ogy of feeding appendages of Calanidae is considered to Materials and Methods be evolved to suit capturing small particles (Anraku and Omori, 1963; Arashkevich, 1969; Minoda, 1971). Details about samplings of the specimens of 4 Functional relationships between mouth part morphol­ Calanus spp. and 4 Neocalanus spp. are given in Table ogy and feeding patterns have been studied on sympatric 1. The specimens were preserved with 5% borax­ Calanus (c. tenuicornis and C. lighti; Mullin, 1969) buffered formalin. A total of 20 copepodid stages of 8

1) Laboratory of Marine Biodiversity, Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minatomach~ Hakodate, Hokkaido 041-8611, Japan (e-mail: [email protected]) (~t#ijJ!i:*~*~~7Hn4~iUf~f4~~'I1:~~~llIIf~) 2) Institute of Marine Research, P.O. Box 1870 Nordnes, 5817 Bergen, Norway

- 59- Bull. Fish. Sci. Hokkaido Univ. 54(3), 2003.

Table 1 Sampling data of copepods analyzed. Abbreviations of species (Abb.) are shown in the parentheses. Observed copepodid stages are indicated by open circles.

Calanus/ Copepodid stage Abb. Date Location Position Depth (m) Net Neocalanus CI C2 C3 C4 C5 C6F C6M

C. finmarchicus (Ct) 24 Sep/ 2000 Barents Sea 76'26'N, 22'OO'E 0-235 WP2 0 C. hyperboreus (Ch) 23 Sep/ 2000 Barents Sea 76'52'N, 20'OO'E 0-150 WP2 0 C. marshaUae (Cm) II JuI! 1995 Gulf of Alaska 58'4O'N, 145'OO'W 0-150 NORPAC 0 C. pacijicus (Cp) 30 Oct/ 1995 NW Pacific 42'OO'N, 141'30'E 0-450 NORPAC 0 N. cristatus (Nc) 4 Jun/ 1997 NW Pacific 41'30'N, 145'47'E 0-500 PCP 0 0 0 0 0 N. jlemingeri (Nt) 4 Jun/ 1997 NW Pacific 41'30'N, 145'47'E 0-500 PCP 0 0 0 0 N. plumchrus (Np) 4 Jun/ 1997 NW Pacific 41'30'N, 14S'47'E 0-500 PCP 0 0 0 0 0 N. tonsus (Nt) 17 Oct/ 1996 SW Pacific 45' 46'N, 171 '02'E 0-80 I m ring 0 0

1------1 A I------~I B Fig. 1. Diagrams showing the prosome length (PL) and 11 parts of feeding appendages measured for interspecific comparisons (abbreviations are shown in the parentheses): A2 endopods (A2 En), A2 exopods (A2 Ex), Md cutting blade (Md Blade), Md endopods (Md En), Md exopods (Md Ex), Mxl arthrite (Mxl Art), Mxl epipodite (Mxl Epi), length of Mx2 (Mx2 L), inter-seta spacing of near the tip of strong spine on Mx2 basis (Mx2 I-S), Mxp coxa (Mxp C), and Mxp basis (Mxp B). Scale bar (both in 1 mm) A is for whole body (Neocalanus plumchrus C5) and B for feeding appendages (except for strong spine on Mx2 basis). species (, C hyperboreus, C stages. C 1 of N. plumchrus could not be distinguished marshaOae, C pacijicus, , N. ftemin­ from that of N. ftemingeri morphologically (Tsuda et aI., geri, N. plumchrus, and N. tonsus) were selected for this 1999). study (Table 1). For Calanus species and N. tonsus Five specimens for each copepodid stage were selected only C5 or C6 females were observed because of arbitrary, and their prosome lengths (PL) were measured insufficient numbers of the other stages. For the North under a dissecting microscope with eye-piece microme­ Pacific sympatric Neocalanus spp. (N. ftemingeri, N. ter to the nearest 50 j.lm, then their Antenna (A2), plumchrus, and N. cristatus) Cl to C5 specimens were Mandible (Md), Maxillule (Mxl), Maxilla (Mx2), and examined. It is noted that C6F and C6M stages of Maxilliped (Mxp) were dissected off (Fig. 1). Each these three species have reduced feeding appendages (cf, feeding appendage was mounted on slides in gum-chlor­ Miller, 1988) thereby no observation was made for these al. Under a light microscope, the linear dimension of

- 60- YAMAGUCHI et al.: Feeding Appendages of Calanus and Neocalanus Copepods

II parts of the feeding appendages (Fig. I) was read of Mauchline (1998), and the measured II parts of the using a digital microscopic software "Mac Scope" appendages include (abbreviations in the parentheses) : (Mitani Corporation Co. Ltd) with a precision of 0.24 to A2 endopods (A2 En), A2 exopods (A2 Ex), Md 2.4,um (depend on the magnification between 40x and cutting blade (Md Blade), Md endopods (Md En), Md 4OOx). Terminology used in this study is followed that exopods (Md Ex), MxI arthrite (Mxl Art), MxI epipodite (MxI Epi), length of Mx2 (Mx2 L), inter-seta 92% spacing of near the tip of strong spine on Mx2 basis .------t-----Ch C6F (Mx2 I-S), Mxp coxa (Mxp C), and Mxp basis (Mxp B) ...-----NeC5 NeC2 (Fig. 1). NeC3 The linear dimension data of each part of feeding NeC4 NfC3 appendages were expressed as the proportion to the PL NfC4 B (each length [,um]/PL [mm]) of the same specimens .----NfC5 (Mullin, 1969; Mullin and Evans, 1976). Since the L...---NpC2 NpC3 differences between the readings of left and right append­ NpC4 ages of the same specimens were not significant (p> 0.05, '----NpC5 paired t-test), a total of 10 data (= left and right parts of ,------Cp C6F CfC6F 5 specimens) were pooled for each stage of a given CmC5 species to calculate a mean. Using the mean values '----NtC5 thus derived, intra- and inter-specific differences were .-----NfC2 .---- NeCl examined by cluster analysis in conjunction with the '---- NpCl Bray-Curtis similarity index (Field et aI., 1982). In ______..!.!:::======<, Nt C6F these analyses, log transformation [loglO eX + 1)] of 80 90 100 variable (X) is a common practice to reduce the bias due Bray-Curtis similarity (%) to extremely abundant species and to eliminate zero Fig. 2. Results of cluster analyses based on Bray-Curtis values. However, no transformation was made in this similarity indices (%) of feeding appendages of study since the variances of the data were relatively Calanus and Neocalanus copepods. Four Groups (A, B, C, and D) are identified at the similarity of 92%. stable. For species abbreviation, see Table 1.

--- 200 ...... ]" A2En A2Ex MdBlade MdEn MdEx Mx2L

150 J.:.l ~..... ~ r- -f J.1 ~ .-= --e a: ~ .: ~ 100 r- r:- .A. .J: _a:- r-.- r- -co r- - ..2= 50 .J: ~ CI) '-' 0 I ~ A B C D A B C D A B C D A B C D A B C D A B C D B

- 61- Bull. Fish. Sci. Hokkaido Univ. 54(3), 2003.

Results CfC6F I-O-i The prosome length of various copepodid stages of 4 ChC6F 1-0-1 Calanus and 4 Neocalanus spp. ranged from 0.70 mm CmC5 '-0-4 (N. plumchrus CI) to 7.02 mm (N. cristatus CS) (data CpC6F t-O-l not shown). The linear dimension of each appendage NeCl 101 part relative to the PL (each length [,urn] /PL [mm]) NeC2 101 ranged from 98.7 to 167.9 for A2 En, 81.9 to 156.S for A2 NeC3 ~Oi Ex, 47.4 to 87.0 for Md Blade, 74.3 to 132.8 for Md En, rO-l 67.0 to 121.2 for Md Ex, 36.S to 66.0 for Mxl Art, 43.6 NeC4 to 61.9 for Mxl Epi, 81.2 to 160.8 for Mx2 L, 0.84-4.00 i NeC5 1-0-1 ~ fIl NfC2 0 for Mx2 I-S, 68.9 to 122.2 for Mxp C, and 67.0 to 106.6 .2 () for Mxp B. Thus the variability of the linear dimension 4) NfC3 0 relative to the PL was the greatest for Mxp I-S (varia­ en!:I. NfC4 0 tions in 4.8 times) among the other parts (1.4-2.0 times). NfC5 ~Oi Cluster analysis based on the relative dimensions of 11 NpCl parts of these feeding appendages revealed a high simi­ NpC2 larity within a total of 20 copepodid stages of 8 species (87% similarity, Fig. 2), confirming that the feeding NpC3 pattern of the species of Calanidae is similar as a whole NpC4 (cf. Marshall, 1973). However, they could be separated NpC5 into four species/stage groups at the similarity level of NtC5 92% (dashed line, Fig. 2). The species designated to NtC6F Group A was C6F whose feeding appendages are all small (Fig. 3). Group B was com­ o 2 4 6 8 10 12 posed of Neocalanus cristatus C2-C5, N. jlemingeri Mx2I-S (~) C3-CS, and N. plumchrus C2-C5 whose feeding append­ ages are medium size. Group C contained C. pacijicus Fig. 4. Between species/stages comparison of inter-seta spacing at near the tip of strong spine on Mx2 basis C6F, C. finmarchicus C6F, C. marshallae CS, and N. (Mx2 I-S). Circles and horizontal bars denote means tonsus CS, all of which are featured by having larger A2, and I standard deviations. For species abbreviation, Md and Mx2 I-S (Fig. 3). Group D was consisted of see Table I. C 1 and C2 stages of Neocalanus spp. and N. tonsus C6F; all of them equipped with the largest feeding marshallae, C. pacijicus and N. tonsus were relatively appendages (Fig. 3). large (5-8 ,urn) as compared with those oflarge-sized N. The proportion of Mx2 I-S to PL was consistently jlemingeri and N. plumchrus (s S ,urn) greater in early copepodid stage in a given species (Figs. 2 and 3). This indicates that the smaller developmental Discussion changes in Mx2 I-S relative to that in the PL. Since the intersetule distance of maxillary setae is indicative of the The present cluster analysis based on the linear dimen­ size of particles that can be removed from the water sions of 11 parts of the feeding appendages identified (Marshall, 1973; Frost et aI., 1983), the absolute dimen­ successfully four distinct groups (Fig. 2). All cope­ sion (,urn) of Mx2 I-S of each stage of Calanus or podids of Calanus spp. were classified into Groups A Neocalanus spp. were presented as Fig. 4. It is noted and C, and those of Neocalanus spp. were into Groups that the inter-setae distance of Mx2 increased progres­ Band D (as only exception N. tonsus CS was designated sively with development within the species, with an as Group C). Group C, to which three Calanus exception for C5 of Neocalanus cristatus (Fig. 4). pacijicus C6F, C. finmarchicus C6F, and C. marshallae Sympatric pairs (Calanus finmarchicus and C. hyper­ C5 classified, is characterized by relatively large feeding boreus in the North Atlantic, and N. cristatus, N. appendages and large inter-setae of Maxilla (Fig. 3). jlemingeri and N. plumchrus in the North Pacific) These Calanus species and Neocalanus tonsus are showed some differences in Mx2 I-S. In the North known to have relatively shorter generation time; 2-3 Pacific species, Mx2 I-S was the smallest for N. plum­ generations per year for C. pacijicus (depending geo­ chrus and largest for N. cristatus with N. jlemingeri graphical locations, cf. Osgood and Frost, 1994), 1-4 being between the two. The inter-setae distances of C. generations per year for C. finmarchicus (Conover,

- 62- YAMAGUCHI et al.: Feeding Appendages of Calanus and Neocalanus Copepods

Table 2 Results of statistical tests (one-way ANOVA and (1987) noted that there are inter-specific differences in Fisher's PLSD) between groups. Any two groups not morphology of feeding appendages: upon molting to underscored by the same line are significantly different. Significant levels: 'p<0.05, "p

- 63- Bull. Fish. Sci. Hokkaido Univ. 54(3), 2003.

N. cristatus are overlapped their developmental season copepod Neocalanus tonsus makes to downward carbon with N. ftemingeri and N. plumchrus. However, since flux in the Southern Ocean. J. Plankton Res., 23, 963- 975. the Mx2 I-S of N. cristatus is larger than them (Fig. 4), Campbell, M.H. (1934) The life history and postem­ feeding niche separation may allow them to occur in the bryonic development of the copepods Calanus tonsus same season. Spatial separation in vertical distribution Brady and Euchaeta japonica Marukawa. J. Biol Res. of these species is also has a function of relaxation of Bd. Can., 1, 1-65. competition of these sympatric species (Mackas et ai., Conover, RJ. (1967) Reproductive cycle, early develop­ 1993). ment, and fecundity in laboratory popUlations of the copepod Calanus hyperboreus. Crustaceana, 13,61-72. Compared with description-oriented studies on feed­ Conover, R.J. (1988) Comparative life histories in the ing appendages of copepods in the past (e.g. Anraku and genera Calanus and Neocalanus in high latitudes of the Omori, 1963; Arashkevich, 1969; Minoda, 1971), the northern hemisphere. Hydrobiogia, 167/168, 127-142. present results indicate clearly that cluster analysis based Field, J.G., Clarke, K.R. and Warwick, RM. (1982) A practical strategy for analyzing multispecies distribution on Bray-Curtis similarity index is a powerful tool to patterns. Mar. Ecol Prog. Ser., 8, 37-52. differentiate copepodid stages of different copepod Frost, B.W., Landry, M.R. and Hassett, RP. (1983) Feed­ species into distinct groups. Four groups identified in ing behavior of large calanoid copepods Neocalanus this study could be interpreted by different magnitudes cristatus and Neocalanus plumchrus from the subarctic of feeding activity; all deduced from development stage­ Pacific Ocean. Deep-Sea Res., 3OA, 1-13. Fulton, J. (1973) Some aspects of the life history of growth rate relationship, generation length, and feeding/ Calanus plumchrus in the Strait of Georgia. J. Fish. spawning couplings of each copepod. The advantage Res. Bd. Can., 30,811-815. of the present technique lies on the fact that information Gifford, OJ. (1993) Protozoa in the diet of Neocalanus about feeding activity of a given copepodid stage can be spp. in the oceanic subarctic Pacific Ocean. Prog. obtained without feeding experiments. For example, Oceanog., 32, 223-237. Harris, RP. (1996) Feeding ecology of Calanus. Ophelia greater feeding activities of Neocalanus Cl are expected 44: 85-109. than C2-C5 of the same species because of greater size of Heinrich, A.K. (1962) On the production of copepods in every feeding appendages of the former (Table 2). the Bering Sea. Int. Revue ges. Hydrobiol., 47, 465- Possibly, feeding rates of copepods can be estimated by 469. measuring feeding appendage indices if the relationship Hirche, H.-J. (1996) The reproductive biology of the marine copepod, Calanus jinmarchicus- A review. between feeding rates and feeding appendage indices is Ophelia, 44, 111-128. established in future study. Hirche, H.-J. (1997) Life cycle of the copepod Calanus hyperboreus in the Greenland Sea. Mar. Bioi., 128,607- 618. Acknowledgements Jillett, J.B. (1968) Calanus tonsus (Copepoda, Calanoida) We wish to express our sincerely thanks to Dr. Janet in southern New Zealand waters with notes on the male. Aust. J. Mar. Freshwat. Res., 19, 19-30. M. Bradford-Grieve of NIWA (New Zealand) for pro­ Mackas, D.L., Sefton, H., Miller, C.B. and Raich, A. (1993) viding Neocalanus tonsus specimens to the present Vertical habitat partitioning by large calanoid copepods study. in the oceanic subarctic Pacific during spring. Prog. Oceanog., 32, 259-294. Marshall, S.M. (1973) Respiration and feeding in cope­ Literature cited pods. Adv. Mar. Bioi. 11, 57-120. Mauchline, J. (1998) The biology of calanoid copepods. Anraku, M. and Omori, M. (1963) Preliminary survey of Adv. Mar. Bioi., 33,1-710. the relationship between the feeding habit and the struc­ Miller, c.B. (1988) Neocalanus jlemingeri, a new species ture of the mouth-parts of marine copepods. Limnol of Calanidae (Copepoda: Calanoida) from the subarctic Oceanogr., 8, 116-126. Pacific Ocean, with a comparative redescription of Arashkevich, Ye.G. (1969) The food and feeding of cope­ Neocalanus plumchrus (Marukawa) 1921. Prog. pods in the northwestern Pacific. Oceanology, 9, 695- Oceanogr., 20, 223-273. 709. Miller, c.B. and Clemons, M.J. (1988) Revised life history Beamish, RJ., Leask, K.D., Ivanov, O.A., Balanov, A.A., analysis for large grazing copepods in the subarctic Orlov, A.M. and Sinclair, B. (1999) The ecology, distri­ Pacific Ocean. Prog. Oceanog., 20, 293-313. bution, and abundance of mid water fishes of the subarctic Minoda, T. (1971) Pelagic copepoda in the Bering Sea and Pacific gyres. Prog. Oceanog., 43, 399-442. the northwestern North Pacific with special reference to Bradford, J.M. and Jillett, J.B. (1974) A revision of the their vertical distribution. Mem Fac. Fish., Hokkaido generic definitions in the Calanidae (Copepoda, Univ., 18, 1-74. Calanoida). Crustaceana, 27, 5-16. Morales, C.E. (1999) Carbon and nitrogen fluxes in the Bradford-Grieve, J.M., Nodder, S.D., Jillett, J.B., Currie, K. oceans: the contribution by zooplankton migrants to and Lassey, K.R (2001) Potential contribution that the active transport in the North Atlantic during the Joint

- 64- YAMAGUCHI et al.: Feeding Appendages of Calanus and Neocalanus Copepods

Global Ocean Flux Study. J. Plankton Res., 21, 1799- Osgood, K.E. and Frost, B.W. (1994) Comparative life 1808. histories of three species of planktonic calanoid copepods Mullin, M.M. (1969) Distribution, morphometry, and in Dabob Bay, Washington. Mar. Bioi., 118, 627-636. seasonai biology of the planktonic copepods, Calanus Tanaka, O. (1956) Further note on Calanus tonsus Brady, tenuicornis and C. lighti in the Pacific Ocean. Pac. Sci., in Japanese waters. J. Oceanogr. Soc. Japan, 12, 49-52. 23, 438-446. Tsuda, A., Saito, H. and Kasai, H. (1999) Life histories of Mullin, M.M. and Evans, P.M. (1976) Distribution, mor­ Neocalanus jlemingeri and Neocalanus p/umchrus phometry, and seasonal biology of the planktonic cope­ (Calanoida: Copepoda) in the western subarctic Pacific. pods Neocalanus robustior and Neocalanus gracilis in Mar. Bioi., 135, 533-544. the Pacific Ocean. Pac. Sci., 30, 119-130. Vervoort, W. (1957) Copepods from Antarctic and Ohman, M.D. (1987) Energy sources for recruitment of the Subantarctic plankton samples. B.A.N.Z. Antarct. Res. subantarctic copepod Neocalanus tonsus. Limnol. Exped. 1929-31. Rep. Ser. B (Zool and Bot.), 3, 1-160. Oceanogr., 32, 1317-1330. Williams, R. and Conway, D.V.P. (1988) Vertical distri­ Ohman, M.D., Bradford, J.M. and Jillett, J.B. (1989) bution and seasonal numerical abundances of the Seasonal growth and lipid storage of the circumglobal, Calanidae in oceanic waters to the south-west of the subantarctic copepod, Neocalanus tonsus (Brady). British Isles. Hydrobi%gia, 167/168,151-159. Deep-Sea Res., 36A, 1309-1326.

- 65-