Copepoda: Calanoida - Springer Link

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George Allen and Unwin Ltd., London, p. 313-334. Giesbrecht, W. (1892). Systematik and Faunistik der pelagischen. Copepoden des Golfes von Neapel und ...
Marine Biology 11 i, 213-225 (1991)

Marine ........ Biology @ Springer-Verlag 1991

Relationship between mouthpart structures and in situ feeding habits of species of the family Pontellidae (Copepoda: Calanoida) S. Ohtsuka and T. Onb~ Faculty of Applied Biological Science, Hiroshima University, 4-4, Kagamiyama 1-chome, Higashi-Hiroshima 724, Japan Date of final manuscript acceptance: August 2, 1991. Communicated by M. Anraku, Suva

Abstract. Pontellid copepods were collected from the surface waters o f a tidal front region in the Bungo Channel (the Inland Sea of Japan) in June 1986 to examine the relationship between the m o r p h o l o g y of cephalic appendages and gut contents. In particular, two dominant species, Labidocera japonica Mori and Pontellopsis yamadae Mori, were c o m p a r e d in detail. Large setae on the second maxillae of L. japonica possessed two rows of setules at right angles to each seta along its inner margin except a terminal part which was serrated, whereas the inner margin of those setae of P. yamadae was entirely serrated. Judging f r o m the structure of the mouthparts, especially the second maxillae, the former species seems to employ b o t h suspension and raptorial feeding modes, in contrast to the latter, which m a y use only the raptorial m o d e o f feeding. In P. yamadae, the first maxilla and the maxilliped are also modified for carnivory. G u t content analysis supported the morphological evidence for feeding differences, and revealed that P. yamadae is a carnivore preying mainly on copepodids while L. japonica feeds omnivorously on copepod nauplii and phytoplankton particles. Since the m o u t h p a r t structures of congeners are quite similar to each other, the feeding behavior and habits might also be similar. Within the family Pontellidae, the genera Anomalocera, Calanopia, Epilabidocera, and Pontella have m o u t h p a r t structures similar to those o f Labidocera, whereas the genus Pontellina resembles Pontellopsis. Morphological similarities would suggest that the first group o f genera employs both suspension and raptorial feeding modes, and that Pontellina is a carnivore like Pontellopsis.

Introduction The family Pontellidae (Copepoda: Calanoida) has been thought to contain typical carnivorous species (Wickstead 1962, Gauld 1966, Mullin 1966, Itoh 1970). In laboratory studies, pontellid copepods have been found to prey voraciously on fish larvae and copepod nauplii

(Lebour 1925, Lillelund and Lasker 1971, Landry 1978, Turner etal. 1985). Turner (1977, 1978), however, showed by both feeding experiment and fecal pellet analysis that three species of this family, Labidoeera aestiva Wheeler, Pontella meadi Wheeler and Anomalocera ornata Sutcliffe, fed directly on small diatoms. On the basis o f observations of m o u t h p a r t structure and gut contents, Ohtsuka et al. (1987a) suggested that Pontella rostraticauda Ohtsuka, Fleminger and Onb6 can employ the m o d e of suspension feeding like Aeartia clausii (Rosenberg 1980) and feeds on particles such as diatoms. The family Pontellidae contains seven genera,

Calanopia, Labidoeera, Pontella, Epilabidocera, Anomalocera, Pontellopsis and Pontellina. The present study reveals the difference in m o u t h p a r t structures and in situ feeding habits a m o n g several species o f pontellid copepods collected in the western area of the Inland Sea of Japan, with special reference to Labidocerajaponica Mori and Pontellopsis yamadae Mori.

Materials and methods Pontellid copepods were collected from 11 stations in the tidal front region in the Bungo Channel (see Yanagi 1990, p. 28-32) on 17 and 18 June 1986 with an ORI neuston net (Matsuo et al. 1976; mesh size 0.33 mm) (Fig. 1). The neuston net, consisting of two nets designed to collect two layers of surface water (0 to 10 cm and 10 to 30 cm depth), was towed for 10 min at a speed of ca. 2 knots by T./R.V. 'Toyoshio-maru', Hiroshima University. Adult pontellids collected by the upper net (0 to 10 cm depth) were used for the observations of mouthparts and gut contents, with the exception of one species, Pontellopsisregalis(Dana), which was found only in the 10 to 30 cm layer (see Table 1). Observations focused on the two dominant species, Labidocerajaponica and Pontellopsis yamadae. Mouthpart structures and gut contents of pontellids were examined using both a differential interference microscope and a scanning electron microscope (JEOL JSM-T20). The procedures were essentially the same as those described by Turner (1978) and Ohtsuka et al. (1987a). Twenty individuals of each sex of Labidocera japonica and Pontellopsis yamadae were randomly selected from a sample at each station to examine the frequency of occurrence of food items (if a sample contained less than 19 individuals, all individuals were examined for gut content analysis). All intact individuals of the other species of Pontellidae were examined.

S. Ohtsuka and T. Onb6: Mouthparts and feeding of pontellids

214 Results

Twenty-three species belonging to four genera of the family Pontellidae were collected from the tidal front region in the Bungo Channel (Table 1). Labidocerajaponica and Pontellopsis yarnadae were dominant at all stations, comprising 59 to 97% of all adult pontellids (Uye et al. 1990). L. japonica, P. yamadae and P. f e r a [including two types distinguished by Zheng et al. (1982)] occurred at all stations, but other species appeared only at some stations. Comparison of cephalic appendages We first compared the first antennae of females of Labidocera japonica (Fig. 2A, B) and Pontellopsis ya-

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Species

Location

Labidocera acuta (Dana) L. acutifrons (Dana) L. bataviae Scott L. detruncata (Dana) L. japonica Mori

El, W3 E2, E3, C3, W2 El, E2, E3, C1, C2, W1, W3 El, E2, E3, C3, Wl, W2 El, E2, E3, C1, C2, C3, C4, C5, Wl, W2, W3 W1 E3, C4 El, E2, W1

L. kroyeri (Brady) L. minuta Giesbrecht L. rotunda Mori Pontella chierchiae Giesbrecht P. fera Dana P. kieferi Pesta P. princeps Dana P. rostraticauda Ohtsuka, Fleminger and Onb6 P. securifer Brady Pontellopsis armata (Giesbrecht) P. krameri (Giesbrecht) P. macronyx Scott P. regalis (Dana) a P. tenuicauda (Giesbrecht) P. villosa Brady P. yarnadae Mori

~'~

Pontellina morii Fleminger and Hiilsemann P. plumata (Dana)

BungoChannel ~

Table 1. Species of the family Pontellidae occurring in the tidal front region in Bungo Channel, the Inland Sea of Japan, and location of occurrence of each species in the upper layer (0-10cm depth). See Fig. 1 for station locations

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33°00"N

El, E2, E3, C2, C3, C4, W1, W2 El, E2, E3, C1, C2, C3, C4, C5, WI, W2, W3 C1, C4, W1, W2 C4 C1 El, E3, C2, Wl, W2 El, E2, E3, C2 W2 El, W2 W3 El, CI, C2, C4, W2 El, E3, C2, C5, W2, W3 El, E2, E3, C1, C2, C3, C4, C5, Wl, W2, W3 C4, C5, W1, W2, W3 El, C1

Pontellopsis regalis occurred only in the lower layer (10 to 30 cm depth)

a

Fig. 1. Station locations. Isobaths indicated in meters

A,B

A s s

C

Fig. 2. Female Labidocera japonica (A, B) and Pontellopsis yamadae (C). (A, C) Right first antenna. Hairy row on second segment of right antenna of L. japonica, detached. (B) Basal two segments

of left first antenna, setae and aesthetascs omitted. S: seta with setules. Aesthetascs are covered with dots; setae without 'S' are setae without setules. Scale bars = 0.2 mm

S. Ohtsuka and T. Onb6: Mouthparts and feeding of pontellids

madae (Fig. 2 C). The former species possesses a row of hairs from the 2nd to l l t h segment along the posterior margin of both the right and left first antennae. The male of L. japonica has a row of hairs on the same segments of the left first antenna, but the right antenna bears no hairs. The segments with hairs generally have setae with setules (indicated by 'S' in Fig. 2A) and aesthetascs. Neither sex of P. yamadae has rows of hairs on the first antenna. The proximal and terminal segments of the first antenna of P. yamadae bear numerous setae, as do those of L. japonica. Fig. 3 shows the mouthparts of Labidocera japonica (Fig. 3 A, C) and Pontellopsis yamadae (Fig. 3 B, D) in ventral and ventro-lateral views. Neither sex of these two species showed reduced mouthparts, with no sexual dimorphism except for a slightly different location of the maxillipeds in L. japonica. A pair of maxillipeds of the female of L. japonica is located slightly behind between the right and left second maxillae, whereas that of the male is situated behind the posterior ends of the second maxillae. Second maxillae of both species shown in Fig. 3 are normally in a closed position. Basal parts of the right and left second maxillae of L. japonica (Fig. 3A) are separated from each other, while those of P. yamadae (Fig. 3B) are closed along the ventral midline. In L.japonica, setal tips of the second maxilla reach at most the middle of the labrum (Fig. 3 A, C), whereas in P. yamadae they are elongated anteriorly beyond the labrum (Fig. 3 B, D). The structures of the first maxillae of both species are also quite different. The second inner lobe of P. yamadae is swollen, and its setae are developed and reach beyond the mouth (indicated by an arrow in Fig. 3 D). Such a specialization is not observed in the first maxilla of L.japonica (indicated by an arrow in Fig. 3 C). Figs. 4 and 5 show the feeding appendages of Labidocera japonica females (Figs. 4A, C and 5A, C) and Pontellopsis yamadae females (Figs. 4B, D and 5B, D): the mandibular cutting edge (Fig. 4A, B), inner lobes of the first maxilla (Fig. 4C, D), the second maxilla (Fig. 5 A, B), and the maxilliped (Fig. 5 C, D). The most contrasting features of the mandibular cutting edges are the structures of C1 and C2 teeth (see Fig. 1 A in Turner 1978) and spinules near the base of teeth ( = dagger-like spines; see Turner 1978). In L. japonica, C1 and C2 teeth are divided terminally into two conical tips (Fig. 4A, indicated by arrows), while in P. yamadae both CI and C2 teeth are furnished with a plate-like structure and a conical tip (Fig. 4 B, indicated by arrows). Spinules near the base of teeth are much longer in P. yamadae than in L. japonica. The cutting edge of L. japonica is relatively broader than that of P. yamadae, and the diastema of the former is comparatively deeper than that of the latter. Inner lobes of the first maxillae differ between the species. The first inner lobe of Pontellopsis yamadae ('11' in Fig. 4 D) has setae thicker than those of Labidocera japonica ('11' in Fig. 4C), and bears numerous minute spinules near the base of these setae on its inner surface, whereas that of the latter is devoid of such spinules. Setae are sparsely distributed on the relatively expanded first inner lobe of P. yamadae; those of L. japonica are densely distributed along its inner margin. The second inner lobe

215 is considerably developed in P. yamadae, with three thick, serrate setae at the tip ('12' in Fig. 4D). The three setae at the tip of the inner lobe in L. japonica are not so thick as in P. yamadae. A number of fine hairs are borne on the inner surface of the second inner lobe of P. yamadae, while the counterpart of L. japonica is naked ('12' in Fig. 4 C). Long setae on the endopod and inner lobes of basipods of the second maxilla in Labidocerajaponica are furnished with two rows of setules at right angles to the seta along the inner margin, except for the terminal serrate part (Figs. 5A and 6A). In contrast, the setae of Pontellopsis yamadae are serrated entirely along the inner margin (Fig. 6B), and some have a terminal hook (Fig. 5 B, indicated by arrows). As on the second maxillae, the first basipod segment of the maxilliped of L.japonica has long setae with two rows of setules at right angles to each seta (Fig. 5 C, indicated by arrows), while the setae of P. yamadae are serrated (Fig. 5 D, indicated by arrows). Gut contents The main food items detected in the guts of pontellids collected from the Bungo Channel are listed in Table 2, along with the number of individuals examined. Copepodids of Acartia spp. (Fig. 7B), Euterpina acutifrons (Fig. 7 C), paracalanids, pontellids, Corycaeus spp. and Oncaea spp. were frequently found in the guts. Species of the genera Pontella and Pontellopsis were found to feed on a wide variety of prey copepodids compared with Labidocera species. Copepod and cirriped nauplii (mainly copepod nauplii) were detected in almost all the guts of pontellids (Fig. 7 A). Other prey zooplankters such as larvaceans, cladocerans (Fig. 7D), polychaetes (Fig. 7E), rotifers (Fig. 7 F), and coelenterates (Fig. 8 B) were also found in their guts. Tintinnids were discovered in the guts of 11 species. Diatoms (Fig. 8 A), armoured dinoflagellates and silicoflagellates were detected in almost all the guts of pontellids. Unidentified remains found in all the guts consisted of small particles mingled with sticky substances which may have been either derived indirectly from prey organisms or directly consumed. Frequency of occurrence of main food items in both sexes of Labidocerajaponica and Pontellopsis yamadae is illustrated in Fig. 9. Copepodids were much more frequently detected in P. yamadae (female: 92%; male: 69 %) than in L. japonica (female: 11%; male: 0%). Identified copepodids found in the guts were Acartia spp. (Fig. 7 B), Euterpina acutifrons (Fig. 7 C), paracalanids, pontellids, oithonids, Oncaea spp. and Corycaeus spp. Acartia spp. and E. acutifrons were most frequently detected in female (71%) and male (32%) of P. yamadae, respectively. On the other hand, copepod nauplii comprised the most important prey zooplankton in L. japonica (female: 57%; male: 36%). In both species, copepodids and copepod nauplii were followed in order of frequency of occurrence by tintinnids, larvaceans, coelenterates (nematocysts) (Fig. 8 B), and cladocerans (Fig. 7 D). Diatoms and dinoflagellates were also frequently detected in the guts of both species. In Pontellopsis ya-

216

Fig. 3. Female Labidocera japonica (A, C) and male Pontellopsis yamadae (B, D). Mouthparts. (A, B) Ventral view. lb: labrum; a2: second antenna; mxl: first maxilla; rex2: second maxilla; mxp: max-

S. Ohtsuka and T. Onb& Mouthparts and feeding of pontellids

illiped. (C, D) Ventro-lateral view from fight side, first maxilla indicated by an arrow. Scale bars=O.1 mm

S. Ohtsuka and T. Onb6: Mouthparts and feeding of pontellids

Fig. 4. Female Labidocerajaponica (A, C) and female Pontellopsis yamadae (B, D). Mouthpart appendages. (A, B) Mandibular cutting edge, the first (C1) and second (C2) central teeth indicated by ar-

217

rows. (C, D) First maxilla. 11: first inner lobe; 12: second inner lobe. Scale bars=0.01 mm (A, B), 0.05 mm (C) and 0.1 mm (D)

218

Fig. 5. Female Labidocerajaponica (A, C) and female Pontellopsis yamadae (B, D). Mouthpart appendages. (A, B) Second maxilla, terminal hook of seta indicated by arrows. (C, D) Maxilliped, devel-

S. Ohtsuka and T. Onb6: Mouthparts and feeding of pontellids

oped, long setae on basipod I with two rows of setules (C) or with serrate part (D) indicated by arrows. Scale bars=0.1 mm

S, Ohtsuka and T. Onb& Mouthparts and feedingof pontellids

219

Fig. 6. FemaleLabidocerajaponica (A) and femalePontellopsisyarnadae (B). Inner margin of setae on secondmaxillae.Scalebars = 0.1 mm

madae, epizoic pennate diatoms (Fig. 8 A) attached to the body of prey copepodids were also found in the guts. In Labidocera japonica, centric and pennate diatoms found in the guts of females and males ranged from 9 to 41 gm in diameter and from 10 to 55 gm in length, and from 4 to 24 ~tm in diameter and from 8 to 54 gm in length, respectively. In P. yamadae, they varied from 4 to 20 lam in diameter and from 9 to 56 gm in length, and from 5 to 20 gm in diameter and from 14 to 76 gm in length, respectively. Centric diatoms found in the guts of P. yamadae were smaller than those in L. japonica. Discussion

Types of mouthpart structures, and swimming and feeding behaviors The differences and similarities in mouthpart morphology allow us to separate the genera of the family Pontellidae into two groups (Types I and II). The several morphological characteristics of Labidocerajaponica mouthparts define Type I genera, while those of Pontellopsis yamadae characterize Type II genera. Observations of other genera within the family PonteUidae permit us to make the following groupings: Type I: Labidocera, Anomalocera, Calanopia,

Epilabidocera, Pontella; Type II: Pontellopsis, Pontellina. The mouthpart structures, particularly second maxillae, of Labidocera and Pontella (Type I) are distinctly different from those of Pontellopsis and Pontellina (Type II). The second maxilla of Type I is similar to those of Acartia clausii (Acartiidae) and Centropages typicus (Centropagidae), which are suspension feeders (Rosenberg 1980, Cowles and Strickler 1983), whereas that of Type II re-

sembles those of Tortanus spp., typical raptorial feeders (Ambler and Frost 1974, Ohtsuka et al. 1987b). In Type I, the stout setae of the second maxilla with two rows of setules along the inner margin (Fig. 5 A) may function in the suspension feeding process. Other suspension feeders such as Acartia clausii and Centropages typicus have such setae on their second maxillae (Rosenberg 1980, Cowles and Strickler 1983). The setae also have an apical serrate part, which is most likely used in grasping relatively large prey (Davis 1977, Alcaraz et al. 1980). Long terminal setae on basipod 1 of the maxilliped (Fig. 5 C) may work together with those of the second maxilla in suspension feeding because these setae are located between the right and left maxillae and are furnished with two rows of setules, as observed in setae on the second maxilla. Inner lobes of the first maxilla may carry particles collected by the second maxilla toward the mouth, as described for Eucalanus spp. (Paffenh6fer et al. 1982) and C. typicus (Cowles and Strickler 1983). Visual observations with a video system revealed that adult female Labidocera rotunda employ suspension feeding as Acartia clausii and Centropages typicus do (Rosenberg 1980, Cowles and Strickler 1983). The second maxillae intermittently open and close to gather food particles, and swimming legs draw a quantity of water containing particles into a feeding basket formed by the second maxillae (Ohtsuka unpublished data). In addition to suspension feeding, Type I pontellid copepods definitely employ a raptorial feeding mode using the second maxillae (cf. Lillelund and Lasker 1971, Landry 1978, Turner et al. 1985). The serrated part of the terminal stout setae on the second maxillae possibly functions in prey capture. The shape of teeth on the mandibular cutting edges varies in structure among species in Type I: Pontella princeps and P. securifer have teeth sharper than those of any other species in Type I, and their C1 to C3 teeth are

S. Ohtsuka and T. Onb6: Mouthparts and feeding of pontellids

220

cirriped nauplii, (9) cladocerans, (10) unidentified crustacean fragments, (11) larvaceans, (12) polychaetes, (13) rotifers, (14) coelenterates, (15) tintinnids, (16) eggs, (17) diatoms, (18) dinoflagellates, (19) silicoflagellates,(20) unidentified remains. ( + ) indicates occurrence of food item

Table 2. Main food items of pontellid copepods collected from the

tidal front region in Bungo Channel, the Inland Sea of Japan. Number in parentheses after sex shows number of individuals examined. Food items: (1-7) copepodids [(1) Acartia spp., (2) paracalanids, (3) pontellids, (4) Euterpina acutifrons, (5) Oithona spp., (6) Corycaeus spp. and Oncaea spp., (7) others], (8) copepod and Species

Sex (n)

Food items 1

Labidocera acuta L. acutifrons L. bataviae L. detruncata L. japonica L. kroyeri L. minuta L. rotunda Pontella chierchiae P. fera P. kieferi P. princeps P. rostraticauda P.: securifer Pontellopsis arrnata P; P. P. P.

krameri macronyx regalis tenuicauda

P. villosa P. yamadae Pontellina morii P. plumata

6` (1) ~ (3) 6` (5) ~ (3) 6` (5) ~ (10) 6` (22) ~ (140) 6` (191) 6' (6) 6` (2) 2 (2) 6` (9) ~_ (9) 6` (26) ~ (7) 6` (11) ~ (2) 6` (1) 6` (1) ~ (1) ~ (1) 6` (3) 2 (2) 6` (9) ~ (1) 6` (2) 9 (1) ~ (3) 6` (3) ~ (5) 6` (9) ~ (155)

2

4

5

6

7

+ + +

+

+ + + + +

+ +

+ + +

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+

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+ + + +

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8

+ + + + + + + + + + + + + + + + + + + + + + + + + +

9

+ +

+

+

6` (186)

+

+

6` ~

+ +

10

11

12

13

14

+ + + +

+ + + +

+ + +

+

+ +

+ + + +

+

+

+ + + +

+ +

+ + + + +

+ + +

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+ + + + + +

+ + + +

+ + + + + + +

17

+ + + + + + + + + + + + + + + + + + + +

18

19

+ + +

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m o n o c u s p e d , w h e r e a s c e n t r a l teeth o f o t h e r species in Type I a r e b i c u s p e d , like m o l a r s ( O h t s u k a u n p u b l i s h e d data). This seems to i n d i c a t e t h a t the d e p e n d e n c e o f each species o n c a r n i v o r y is different (cf. I t o h 1970, S c h n a c k 1989). I n the p r e s e n t study, no species b e l o n g i n g to the gene r a Calanopia, Epilabidocera a n d Anomaloeera were exa m i n e d , b u t these three g e n e r a c a n be assigned to Type I b e c a u s e their m o u t h p a r t a p p e n d a g e s a r e similar to t h o s e o f Labidocera a n d Pontella. These g e n e r a all possess a relatively b r o a d m a n d i b u l a r c u t t i n g edge, a n u n s w o l l e n s e c o n d i n n e r l o b e o f the first m a x i l l a , setae o f the s e c o n d m a x i l l a a n d the first b a s i p o d o f m a x i l l i p e d w i t h two r o w s o f setules a l o n g the i n n e r m a r g i n o f each seta (cf. Giesb r e c h t 1892, P a r k 1966, T u r n e r 1978). I n a d d i t i o n to m o r p h o l o g i c a l o b s e r v a t i o n s o f feeding a p p e n d a g e s , feeding e x p e r i m e n t s o r analysis o f gut o r fecal pellet c o n t e n t s has suggested t h a t these three g e n e r a p o s s i b l y e m p l o y b o t h

+

+

+

+ +

+

+

+

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+

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20

+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +

+

+

+

16

+

+ + + + + +

15

+

+

+ +

(8) (3)

3

+ + +

+ + + + +

+

+

+ +

+ +

s u s p e n s i o n a n d r a p t o r i a l feeding m o d e s ( P a r k 1966, T u r n e r 1978, 1984, 1985, O h t s u k a u n p u b l i s h e d data). Labidocera, Pontella a n d Epilabidocera possess a r o w o f fine hairs a l o n g the p o s t e r i o r p r o x i m a l m a r g i n o f the first a n t e n n a , w h i c h suggests t h a t these c o p e p o d s s w i m r a p i d l y a n d s m o o t h l y a n d search actively for m o t i l e p r e y o r g a n i s m s ( L a n d r y a n d F a g e r n e s s 1988). A c c o r d i n g to L a n d r y a n d F a g e r n e s s (1988), rows o f hairs a l o n g the p r o x i m a l p o s t e r i o r e n d o f the first a n t e n n a f u n c t i o n to ' r e d u c e the s e p a r a t i o n o f the b o u n d a r y l a y e r a n d shedd i n g o f vortices as the a n t e n n a passes t h r o u g h the w a t e r to e n h a n c e the sensitivity o f r e c e p t o r s ' . O n the o t h e r h a n d , Calanopia has no such h a i r y row, a n d m a y swim a n d feed in a m a n n e r different f r o m the f o r m e r three genera. A n a m b u s h p r e d a t o r (Tortanus diseaudatus) a n d relatively s l o w - s w i m m i n g p a r t i c l e feeders (Calanuspaeificus a n d Neocalanus cristatus) ( M u l l i n 1979, L a n d r y a n d F a g e r n e s s 1988) are also d e v o i d o f such a r o w o f hairs.

S. Ohtsuka and T. Onb6: Mouthparts and feeding of pontellids

Pig. 7. Gut contents of pontellid copepods. (A) Copepod nauplius in the gut of female Labidocera detruncata. (B) Acartia omorii in the gut of female Pontellopsis yamadae. (C) Euterpina acutifrons in the gut of male Pontella princeps. (D) Evadne sp. in the gut of female

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Pontellopsis yamadae. (E) Polychaete in the gut of female Pontella chierchiae. (F) Mastax trophi of rotifer in the gut of male Pontellopsis yarnadae. Scale bars=0.1 mm (A to D) and 0.05 mm (E, F)

S. Ohtsuka and T. Onb6: Mouthparts and feedingof pontellids

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Fig. 8. Gut contents of pontellid copepods. (A) Epizoic pennate diatoms attached to setae of prey copepod detected in the gut of female Pontellopsis yamadae. (B) Nematocystsin the gut of male Pontella chierchiae. Scale bars = 0.05 mm

Frequency (%)

Rows of hairs along the posterior proximal margin of the first antenna are found in Euchaetidae (females only), hyperbenthic Paramisophria (Arietellidae), and Pleuromamma (Metridinidae) (Landry and Fagerness 1988, Ohtsuka unpublished data). Species of the family Euchaetidae and the genus Paramisophria are known to swim fast and continuously, and to be typical predatory copepods preying mainly on copepods (Ohtsuka 1985 b, Landry and Fagerness 1988, Ohtsuka and Mistuzumi 1990). However, Pleuromamma spp. are basically particle-feeders feeding on phytoplankters, microzooplankters and fecal pellets (Hattori 1989). Therefore the presence of a row of hairs on the first antenna may indicate that the copepod swims rapidly (3.2 to 13.9mm s-a; Landry and Fagerness 1988, Hattori 1989) and continuously, but may not always indicate that the copepod is carnivorous. Therefore the swimming speed of Calanopia might be slower than that of Labidocera and Pontella. In contrast to the Type I pontellids, Type II organisms may use only raptorial feeding because the second maxillae have only serrated setae terminally. Some setae possess a hook at the tip. Stout serrate setae on the first and second inner lobes of the first maxilla and on first basipod of the maxilliped may supplement the grasping of prey by the second maxilla. These stout serrated setae may function as chopsticks in catching and grasping relatively large prey organisms such as copepodids (Alcaraz et al. 1980, Boxshall 1985). In Type II, the second maxillae are also likely to be used as a scoop net (Gauld 1966, Ambler and Frost 1974) for small prey, based on the similarity to Tortanus discaudatus, which uses its second maxillae properly for prey organisms of different sizes (Ambler and Frost 1974). Pontellopsis yamadae ingested small tintinnids (22 to 137 gm in lorica length) (Ohtsuka 1985 a, present study), which may have been captured by scooping rather than with the chopstick method.

Frequency (%)

100

r--

'0 Copepodids

i

]

lO0

Acartia Euterpina Paraealanids

Labidocera iaponica

Pontellopsis yamadae

Pontellids I

Oncaea,Corycaeus

Copepod nauplii

m

Cladocerans

Female

[]

L____

Male

Larvaceans Coelentrates Tintinnids

I

Diatoms Dinoflagellates

m

I

Fig. 9. Labidocerajaponica and Pontellopsisyamadae. Frequency of occurrence of main food items. Number of individuals examined: 140 femaleand 191 male L. japonica; 155 femaleand 186 male P. yamadae. 'Copepodids' includes all prey copepod species

S. Ohtsuka and T. Onb& Mouthparts and feeding of pontellids Both Pontellopsis and Pontellina lack a row of hairs along the posterior proximal margin of the first antenna, and may swim slowly and in a random darting motion like Tortanus discaudatus (Ambler and Frost 1974). Judging from their cephalic appendage structures, these copepods are most likely ambush predators. The relatively narrow mandibular cutting edge of Type II with sharp teeth suits predatory copepods which pierce and cut their prey (cf. Ohtsuka and Onb6 1989). Numerous long setules near the base of teeth may function for grooming. Such setules are also observed in Tortanus erabuensis (see Fig. 1 E in Ohtsuka et al. 1987b).

Feeding habits of pontellid copepods Pontellid copepods have so far been regarded as typical carnivores (Lowndes 1935, Wickstead 1962, Gauld 1966, Mullin 1966, Itoh 1970). Gut content or fecal pellet analyses and laboratory feeding experiments, however, revealed that Labidocera, Epilabidocera, Pontella and Anomalocera are omnivores, feeding on both zoo- and phytoplankters (Lebour 1925, Marshall 1924, Park 1966, Turner 1977, 1978, 1984, 1985, Conley and Turner 1985, Ohtsuka et al. 1987 a). Although Pontellopsis and Pontellina were known to prey on zooplankters (Lillelund and Lasker 1971, Fleminger and Hfilsemann 1974, Ohtsuka 1985 a), it was not obvious whether or not they can feed on phytoplankters. The present observations of their mouthpart structures, and gut content analysis, suggested these copepods to be typical predatory carnivores like tortanids, euchaetids and candaciids (Wickstead 1959, 1962, Ambler and Frost 1974, Mullin 1979, Yen 1985, Ohtsuka et al. 1987 b, Landry and Fagerness 1988, Ohtsuka and Onb6 1989, Ohtsuka 1990). Diatoms detected in the guts of Pontellopsis yamadae seem to have been derived indirectly from prey organisms: either from prey gut contents or from epizoic diatoms attached to bodies of prey copepods (Fig. 8 A). Gut content analysis clearly demonstrated that Labidocera japonica primarily ingested copepod nauplii and particles such as diatoms and dinoflagellates. Landry (1978) showed by experiments that Labidocera trispinosa Esterly preferred late copepod naupliar stages to copepodid stages, because late naupliar stages were easier for the predator to detect, and copepodids could evade the predator more easily than nauplii. His experimental result supported our gut content analysis of the congeneric species L. japonica. Moreover, Conley and Turner (1985) found that another congener, L. aestiva, ingested more carbon in the form of animal food than plant material. Turner (1984) also suggested from fecal pellet analysis that L. aestiva was primarily a raptorial feeder rather than a typical suspension feeder. All of these results indicate that species of the genus Labidocera are typical omnivores, feeding mainly on copepod nauplii and phytoplankton particles, rather preferring zooplankters to phytoplankters as food. Two other Type I genera, Pontella and Anomalocera, are also known to feed on both zoo- and phytoplankters (Lebour 1922, 1925, Marshall 1924, Lowndes 1935,

223 Wickstead 1962, Gauld 1966, Turner 1977, 1978, 1985, Turner et al. 1985, Ohtsuka et al. 1987a, Ohtsuka 1990). Their feeding habits are, however, likely to be slightly different from those of Labidoeera. Pontella rostraticauda collected from surface waters in the Inland Sea of Japan in summer frequently fed on macrozooplankters such as copepodids and cladocerans, in addition to copepod nauplii, diatoms and dinoflagellates (Ohtsuka et al. 1987 a). P. rostraticauda is larger than Labidocera japonica, and probably can attack larger prey zooplankters than Labidocera (Ohtsuka 1990). On the other hand, Anomalocera ornata from continental shelf and slope waters of the Gulf of Mexico in winter did not ingest crustaceans at all, and was suggested to behave primarily as an opportunistic grazer (Turner 1985). This species preyed on fish larvae in the laboratory (Turner et al. 1985) and fed on both diatoms and crustaceans in situ (Turner 1978). In contrast, Anomalocera patersoni Templeton fed on copepods in the field (Lebour 1922, Marshall 1924, Lowndes 1935). Therefore, Anomaloeera may change its food items more opportunistically than do Labidocera and Pontella. There has been little information on in situ feeding habits of Pontellopsis and Pontellina, but the present study has revealed that these copepods prey primarily on copepodids and supplementarily on other macro- and microzooplankters. The actual density and composition of prey species in the study area were not known. However, Pontellopsis yamadae seems to have attacked copepodids in the ambient water column opportunistically because prey copepods such as Acartia spp., Euterpina acutifrons and paracalanids are common in early summer in the Inland Sea of Japan and its neighbouring waters (Hirota 1961, 1964, 1968, 1979, Ueda 1980, 1982). An adult female P. yamadae collected off Kii Peninsula also preyed voraciously on copepodids of Euterpina (Ohtsuka 1985a). Pontellopsis occidentalis was found to ingest Labidocera copepodids in the laboratory (Lillelund and Lasker 1971), while Pontellina seems to prefer Oncaea to other copepodids (Fleminger and Hfilsemann 1974, Ohtsuka unpublished data). Nematocysts of coelentrates were found in the guts of some pontellid copepods, indicating that small hydrozoans are readily ingested by copepods which employ raptorial feeding. Coelenterates were also detected in the guts of a wide variety of deep-sea calanoid copepods (Arashkevich 1969, Harding 1974). The relative size of coelenterates and copepods determines which organism is the predator. Predation by pontellid copepods on fish eggs and larvae was observed in the laboratory (Lebour 1925, Lillelund and Lasker 1971, Turner et al. 1985), and Turner et al. (1985) suggested that copepod predation could occur readily in surface windrows and slicks where both copepods and fish eggs and larvae are concentrated by physical mechanisms. However, such predation seldom occurred in this tidal front region, where a wide variety of particles including plankton were concentrated (Yanagi 1990). Only one adult female Pontella rostraticauda collected at Stn C1 had ingested a fish egg in the present study. Although bodies of fish larvae are easy to digest, pigments and a quantity of amorphous materials derived

224

form the larvae possibly remain in copepod guts (cf. Bailey and Yen 1983). We did not observe such materials in our study, and have no evidence for the predation by pontellids on fish larvae. Acknowledgements. We express our sincere thanks to Dr. T. J. Cowles for his critical reading of the manuscript, and to Prof. T. Yanagi for giving us the opportunity to join the research project on the tidal front. Thanks are due to the captain and crew of T./R.V. "Toyoshio-maru" for cooperation at sea. This study was partly supported by the grants from the Ministry of Education, Science and Culture of Japan (Nos. 61030057, 61760164) and by the Nissan Science Foundation (1990).

Literature cited Alcaraz, M., Paffenh6fer, G.-A., Strickler, J. R. (1980). Catching the algae: a first account of visual observations on filter-feeding calanoids. In: Kerfoot, W. G. (ed.) Evolution and ecology of zooplankton communites. University Press, New England, p. 241-248 Ambler, J. W., Frost, B. W. (1974). The feeding behavior of a predatory planktonic copepod, Tortanus discaudatus. Limnol. Oceanogr. 19:446-451 Arashkevich, Ye. G. (1969). The food and feeding of copepods in the northwestern Pacific. Oceanology, Wash. 9:695-709 Bailey, K. M., Yen, J. (1983). Predation by a carnivorous marine copepod, Euchaeta elongata Esterly, on eggs and larvae of the Pacific hake, Merluceius produetus. J. Plankton Res 5:71-82 Boxshall, G. A. (1985). The comparative anatomy of two copepods, a predatory calanoid and a particle-feeding mormonilloid. Phil. Trans. R. Soc. (Ser. B) 311:303-377 Conley, W. J., Turner, J. T. (1985). Omnivory by the coastal marine copepods Centropages hamatus and Labidocera aestiva. Mar. Ecol. Prog. Ser. 21:113-120 Cowles, T. J., Strickler, J. R. (1983). Characterization of feeding activity patterns in the planktonic copepod Centropages typieus Kroyer under various food conditions. Limnol. Oceanogr. 28: 106-115 Davis, C. C. (1977). Sagitta as food for Aeartia. Astarte 10:1-3 Fleminger, A., Hfilsemann, K. (1974). Systematics and distribution of the four sibling species comprising the genus Pontellina Dana (Copepoda, Calanoida). Fish. Bull. U.S. 72:63-120 Gauld, D. T. (1966). The swimming and feeding of planktonic copepods. In: Barnes, H. (ed.) Some contemporary studies in marine science. George Allen and Unwin Ltd., London, p. 313-334 Giesbrecht, W. (1892). Systematik and Faunistik der pelagischen Copepoden des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna Flora Golf. Neapel 19:1-831 Harding, G. C. H. (1974). The food of deep-sea copepods. J. mar. biol. Ass. U.K. 54:141-155 Hattori, H. (1989). Bimodal vertical distribution and diel migration of the copepods Metridia pacifiea, M. okhotensis and Pleuromamma seutullata in the western North Pacific Ocean. Mar. Biol. 103:39-50 Hirota, R. (1961). Zooplankton investigations in the Bingo-nada region of the Setonaikai (Inland Sea of Japan). J. Sci. Hiroshima Univ. (Ser. B, Div. 1) 20:83-145 Hirota, R. (1964). Zooplankton investigationsin Hiuchi-nada in the Setonaikai (Inland Sea of Japan). I. The seasonal occurrence of copepods at the three stations in Hiuchi-nada. J. oceanogr. Soc. Japan 20:24-31 Hirota, R. (1968). Zooplankton investigations in the Setonaikai (Inland Sea of Japan). I. Occurrence of zooplankton in the western half of the Setonaikai in June, 1963. J. oceanogr. Soc. Japan 24:203-211 Hirota, R. (1979). Seasonal occurrence of zooplankton at a definite station off Mukaishima from July of 1976 to June of 1977. Publs Amakusa mar. biol. Lab. 5 : 9 - 1 7

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225 Uye, S., Ohtsuka, S., Onb6, T. (1990). The distribution and biological process of zooplankton in a tidal front in the Bungo Channel. In: Yanagi, T. (ed.) The science of shiome. Kouseisya-kouseikaku, Tokyo, p. 78-94 (in Japanese) Wickstead, J. H. (1959). A predatory copepod. J. Anim. Ecol. 28: 69-72 Wickstead, J. H. (1962). Food and feeding in pelagic copepods. Proc. zoo1. Soc. London 139:545-555 Yanagi, T. (1990). The physical process in tidal fronts. In: Yanagi, T. (ed.) The science of shiome, Kouseisya-kouseikaku, Tokyo, p. 25-36 (in Japanese) Yen, J. (1985). Selective predation by the carnivorous marine copepod Euehaeta elongata: laboratory measurements of predation rates verified by field observations of temporal and spatial feeding patterns. Limnol. Oceanogr. 30:577-597 Zheng, Z., Li, S., Li, S.-J., Chen, B. (1982). Marine pelagic copepods from Chinese water, Vol. II. Shang-hai Scientific and Technological Publisher, Shang-hai, p. 1-162 (in Chinese)