Mouthpart morphology of three calanoid copepods from Australian temporary pools: Evidence for carnivory

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1 New Zealand Journal of Marine and Freshwater Research ISSN: (Print) (Online) Journal homepage: Mouthpart morphology of three calanoid copepods from Australian temporary pools: Evidence for carnivory John D. Green & Russell J. Shiel To cite this article: John D. Green & Russell J. Shiel (1999) Mouthpart morphology of three calanoid copepods from Australian temporary pools: Evidence for carnivory, New Zealand Journal of Marine and Freshwater Research, 33:3, , DOI: / To link to this article: Published online: 30 Mar Submit your article to this journal Article views: 261 Citing articles: 8 View citing articles Full Terms & Conditions of access and use can be found at

2 New Zealand Journal of Marine and Freshwater Research, 1999, Vol. 33: /99/ $7.00 The Royal Society of New Zealand Mouthpart morphology of three calanoid copepods from Australian temporary pools: evidence for carnivory JOHN D. GREEN Department of Biological Sciences University of Waikato Private Bag 3105 Hamilton, New Zealand RUSSELL J. SHIEL CRC for Freshwater Ecology Murray-Darling Freshwater Research Centre P. O. Box 921, Albury NSW 2640, Australia Abstract The mandibles, first and second maxillae, and maxillipeds of Boeckella major, B. pseudochelae, and Hemiboeckella searli from temporary pools of the upper River Murray catchment were dissected off and examined by light microscopy for features associated with carnivorous feeding. In B. major adaptations for carnivory are enlarged ventral mandibular teeth, strong falciform medial setae on the second maxillae, falciform endopodal setae on the maxilliped, large body size and large mouthpart size in relation to body size. Its mandibular edge index is 772, in the upper omnivore range. B. major is predicted to be an omnivore with strong carnivorous tendencies and able to handle large prey items. Carnivorous features in H. searli are enlarged ventral mandibular teeth, a mandibular edge index of 1395, and strong unguiform and falciform setae on the second maxillae. It is predicted to be an omnivore with moderate carnivorous tendencies, but This paper is dedicated to Dr Ann Chapman on the occasion of her retirement. JDG expresses his thanks to Ann for stimulating his interest in calanoid copepods and the intricacies of their structure and function. M98046 Received 20 July 1998; accepted 5 October 1998 unable to handle prey as large as can B. major. In B. pseudochelae the only adaptations for carnivory are an edge index of 1080 and falciform setae on the maxilliped. It is predicted to be an omnivore with herbivorous tendencies. Examination of gut contents confirmed these predictions. B. major guts contained 19 animal taxa, mainly planktonic cladocerans, copepods and rotifers, H. searli 12 taxa, mainly copepods and rotifers, and B. pseudochelae 8 taxa, mainly rotifers. All had consumed algae. We suggest that predation by B. major may be an important factor affecting community structure in fishless Australian temporary pools. Keywords calanoid copepod; carnivorous; predation; temporary pool; Australia INTRODUCTION Temporary waters which vary widely in size, salinity, and periodicity are characteristic of Australia. Williams (1988) emphasised the biological importance of these ephemeral waters and hypothesised that predictably temporary habitats (i.e., those that dry every year) have most likely been the evolutionary foci of Australia's freshwater fauna. Throughout much of New South Wales and Victoria the most common temporary habitats are small freshwater pools that annually fill in winter and dry in summer. The few published studies (e.g., Morton & Bayly 1977; Lake et al. 1989) indicate that these pools have extremely diverse invertebrate faunas, that fish appear to be absent, and that frogs and their tadpoles are the only vertebrates present. We have found similar communities in a survey of temporary pools on the floodplain of the upper River Murray and its tributaries (Shiel et al. 1998). Calanoid copepods are an important element in these pools, and many species may co-occur. Of particular note are three species that stand out because of their very large size Boeckella major Searle, 1938 (body length up to 4.4 mm), B. pseudochelae Searle, 1912 (body length up to 2.9 mm), and Hemiboeckella searli Sars,

3 New Zealand Journal of Marine and Freshwater Research, 1999, Vol. 33 B Fig. 1 The three copepods examined, showing differences in body size. A, Boeckella major, B, Boeckella pseudochelae; and C, Hemiboeckella searli (body length up to 2.5 mm) (Fig. 1). North American calanoids of this size (e.g., Limnocalanus macrurus, Epischura lacustris, Senecella calanoides, Hesperodiaptomus shoshone (Wong 1984)) are usually voracious carnivores that can have marked top-down effects on planktonic communities (e.g., Nero & Sprules 1986; O'Brien & Luecke 1988; Paul et al. 1995). We were thus interested to determine whether the three boeckellids had similar carnivorous tendencies. Mouthpart morphology of calanoid copepods has been shown in many instances to give a good general indication of a species' diet (e.g., Anraku & Omori 1963; Anderson 1967; Arashkevich 1969; Itoh 1970; Jerling & Woolridge 1994). The correlation between morphology and structure is not perfect (Wong 1984), but invariably species with very spinose maxillae and maxillipeds and sharply denticulate mandibular cutting-edges are carnivores that are capable of grasping and masticating prey of similar size to themselves (Anraku & Omori 1963; Arashkevich 1969). A lack of these features, however, is not definitive evidence of a lack of carnivorous tendencies and calanoids with "herbivore" mouthpart morphology are now known to ingest animals, although generally such prey items (e.g., rotifers) are small in relation to the size of the predator (e.g., Williamson & Butler 1986). In fact, the view that truly herbivorous calanoids exist is probably a thing of the past. Rather, the modern concept is that calanoids are fundamentally omnivorous with different species exhibiting varying degrees of herbivory or carnivory (e.g., Vanderploeg 1994). As a first approach to assessing the carnivorous capabilites of B. major, B. pseudochelae, and H. searli we describe here the structure of their mouthparts. To check the predictions from mouthpart morphology we also present a preliminary assessment of the species' diet from a qualitative analysis of their gut contents.

4 Green & Shiel Mouthpart morphology of calanoid copepods 387 STRUCTURE OF CALANOID MOUTHPARTS IN RELATION TO DIET The characteristics of the mouthparts of calanoid copepods have been described in detail for various marine species by Anraku & Omori (1963) and Arashkevich (1969), and for some North American freshwater species by Wong (1984). Distinctive morphological features of the mandibles (especially the cutting edges), first maxillae, second maxillae, and maxillipeds were found to be correlated with diet as determined from gut contents, and these relationships are summarised in Table 1. Aspects associated particularly with carnivory are the development of thickened spine-like and dagger-like setae on the distal ends and medial lobes of these appendages, features that are interpreted as adaptations for grasping prey. Itoh (1970) developed a quantitative edge index, based on measurements of the cutting edge of the mandible (Fig. 2), and showed that the value of the index correlated well with observed diet <500 in herbivorous species, in omnivorous species, and >900 in carnivorous species. Wong (1984) criticised the validity of these correlations between morphology and diet because they were made in the absence of a detailed understanding of the functioning of individual mouthparts. However in the light of recent knowledge of the mechanisms of copepod feeding (e.g., as summarised by Vanderploeg 1994) they do, in fact, seem reasonable. It is now realised that calanoid copepods are fundamentally raptorial suspension feeders rather than filter feeders and that they use appendages such as the second maxilla, which was once thought to act as a sieve, as paddles to grab particles and/or direct their movement. In the capture of very small particles, the mouthparts continue to vibrate and particles are passively funnelled by the second maxillae towards the mouth (e.g., Price & Paffenhofer 1986). Larger particles, including animals, are captured more actively by grasping movements of the maxillipeds and "fling and clap" movements of the second maxillae (e.g., Anderson 1967; Kerfoot 1977; Koehl & Strickler 1981; Strickler 1984; Wong 1984). Animal prey is usually held in the basket formed by the posterior maxillipeds and lateral maxillae and these appendages may rotate the prey into an orientation suitable for chewing by the mandibles (Anderson 1967; Kerfoot 1978; Wong 1984). Clearly, in carnivorous copepods the requirement for such manipulations is likely to lead to selection for more pronounced development of structures (e.g., solid spines on the distal and medial sections of the maxillipeds and second and first maxillae) for grasping and/or piercing prey than in herbivorous species. Table 1 Correlation between the structure of copepod mouthparts and their mode of feeding (modified after Arashkevich 1969). Mouth appendages Herbivore Carnivore Mandible Cutting edge Crowns Maxilla I General features Setae: of external margin of 1 st masticatory lobe of 2nd and 3rd masticatory lobes Plumose of endopodite Plumose Maxilla I! General description Endopodite Setae Maxilliped Setae Low broad teeth Multicusped, of masticatory type Strong development of lobes of external margin Plumose, strong Plumose and aculeate Strong development of endites and setae of proximal portion Five-segmented Plumose Plumose High pointed teeth Narrow, acinaciform, of cutting type Strong development of lobes of internal margin Plumose, weak Plumose and aculeate Dagger-shaped Unguifonn Strong development of endopodite and setae of distal portion Two-segmented Unguifonn and aculeate Unguifonn, aculeate and dagger-shaped

5 388 New Zealand Journal of Marine and Freshwater Research, 1999, Vol. 33 II 1 O no a' ^"O O Edge Index. x( --10 IW H "I E o o o o Fig. 2 Mandible cutting edge showing measurements and formula used in calculation of the edge index. (W = total length of the cutting edge; H = height of the ventral tooth; h( = depth of the inter-cusp depression, measured from a point midway between adjacent cusps to the base of the depression; w. = distance between peaks of adjacent cusps. After Itoh (1970).) METHODS Specimens were collected from a number of temporary pools on the floodplains of the upper River Murray and its tributaries (Table 2). All ponds were shallow, ranging in depth from 10 to 50 cm. Samples were taken by sweeping a plankton net (mouth diameter 20 cm, mesh size 37 or 50 mm) through the pond. A number of sweeps were made, taking in both marginal and central areas, and shallow and deeper water. Samples were preserved in 4% formaldehyde or 70% alcohol. Several adult females of each species were extracted from the samples indicated in Table 2. Their mouthparts (mandibles, first and second maxillae, maxillipeds) were dissected off using fine tungsten needles under a Zeiss SV-8 stereomicroscope at X magnification, and mounted in polyvinyl alcohol-lactophenol (Chapman & Lewis 1976) stained with lignin pink. Drawings were made using a drawing tube and both bright field and Nomarski differential interference contrast optics at magnifications of 200x and 400x. Fine details were checked using oil immersion (1 OOOx). Feathering on setae has been omitted from diagrams. Terminology of appendages follows that of Huys & Boxshall (1991) as outlined in Fig. 3. Mouthpart sizes (lengths) and body lengths were measured from the drawings in Fig. 1, 3, 4, 7, 8, and 9. Mouthpart ca ;- o p "5. 3 E c & II OO " II - QJ 2 ts P C p ^~ 5 c i d I e - ID No g ON as S? 2 2 : O s OsOsONONOs 8-R-8-& J"SovS~a o t- r-~ os (N 'A f'l O N N ^ fn (N (N CN <N (N OO ^- - t^ ^- (N >O O > O O so t^ SO SO SO SO f^~ ai c/3 00 CO C> c^l r^ OJ ro N g u-i o ;. J3, 60 : 3 53 = : 1 gj (U flj IT3 ^ -O 8" 8" 8" (N (N O N (N S2 g

6 Green & Shiel Mouthpart morphology of calanoid copepods 389 ENDOPOD BASIS \ COXA ENDOPOD COXA J\ Coxal Epipo- endit dite COXA Arthrite ALLOBASIS- PRAECOXA- Fig. 3 Tenninology of the segments of the mouthparts, based on Huys & Boxshall (1991). lengths used were: mandible length of coxa; mandible cutting edge W in Fig. 2; maxilla 1 base of praecoxa to distal endopod segment; maxilla 2 base of praecoxa to distal endopod segment; maxilliped base of coxa to distal endopod segment. Body length was measured from the front of the cephalothorax to the tips of the urosomal setae. Following Green & Shiel (1992) guts were dissected from at least 28 individuals of each species (sites shown in Table 2). Gut contents were mounted

7 390 New Zealand Journal of Marine and Freshwater Research, 1999, Vol. 33 in glycerine jelly, stained with lignin pink and examined using Nomarski differential interference contrast optics at magnifications of 400x and 800x. Each gut was scored for presence of plant and animal remains. Animal remains were identified to the lowest possible taxonomic level usually genus, and sometimes species. RESULTS Relative size of mouthparts The mouthparts of B. major are considerably larger than those of the other two species (Fig. 4, 5, 7-9), in keeping with its larger size. However, differences in mouthpart sizes are not simply in proportion to body size and in general the mouthparts of B. major are also relatively considerably larger (Table 3). Exceptions are the mandible cutting edge of H. searli, which is relatively as large as that of B. major, and the maxilliped ofh. searli, which is relatively much smaller than those of the other two species. Mandible (Fig. 4-6) The mandible is made up of a biramous palp and a coxa with a toothed cutting edge (gnathobase) (Fig. 3). The palps of all species are very similar, but the mandible cutting edges vary (Fig. 4 and 5). All have eight teeth and a dorsal seta, but the relative size of the teeth and the configuration of the tooth rows differ. In B. pseudochelae the ventral tooth is relatively shorter and closer to the adjacent tooth than in the other species. Teeth 4-8 have small accessory cusps. In B. major, the ventral tooth is relatively larger and separated from the rest of the tooth row by a diastema, although all the teeth are in more-orless the same alignment, as in B. pseudochelae. Teeth 2-8 of B. major have one or two accessory cusps. In H. searli, however, the ventral tooth lies below the line of the other teeth, but is widely separated from them. As a result the cutting edge of//, searli is lengthened and is relatively as long as that of B. major (Table 3). As in B. pseudochelae teeth 4-8 have one or two accessory cusps. Mean edge indices are 772 (range , n = 16), 1080 (range , n = 11), and 1395 (range , n = 14) for B. major, B. pseudochelae, and//, searli, respectively (Fig. 6). Those of//, searli and B. pseudochelae are not significantly different (Kruskal-Wallis test, P > 0.05) and lie at the bottom of the carnivore range defined by Itoh (1970). That of B. major is significantly lower (Kruskal-Wallis test, P < 0.01) and is at the high end of the omnivore range. First maxilla (Fig. 7) There are only minor differences in the morphology of the first maxillae between species. The large dagger-like spines on the arthrite of the praecoxa, particularly the distal ones, are relatively more robust in B. major and H. searli than in B. pseudochelae, and in B. major and B. pseudochelae the setae of the coxal and basal endites are more solid and falciform than in H. searli. In B. pseudochelae, unlike the other two species, the long setae of the coxal epipodite become suddenly thinner about one third of their length from the base. In all three species the lobes of the inner margin (praecoxal arthrite, coxal and basal endites, basis and endopod) are relatively larger than those of the outer margin (coxal epipodite, endopod). Second maxilla (Fig. 8) In all species the setae and endites of the proximal portion (praecoxa, coxa, and allobasis) of the second Table 3 Relative mouthpart sizes (mouthpart length as a proportion of total body length). (Mouthpart lengths used: mandible length of coxa; mandible cutting edge W in Fig. 2; maxilla 1 base of praecoxa to distal endopod segment; maxilla 2 base of praecoxa to distal endopod segment; maxilliped base of coxa to distal endopod segment. Lengths measured from diagrams in Fig. 1,4, 5, 7, 8, and 9.) Mandible Mandible cutting edge Maxilla 1 Maxilla 2 Maxilliped Boeckella major Hemiboeckella searli Boeckella pseudochelae

8 Green & Shiel Mouthpart morphology of calanoid copepods 391 Fig. 4 Mandibles. A, Boeckella major, B, Boeckella pseudochelae; and C, Hemiboeckella searli. maxilla are more strongly developed than the endopod. The setae are generally more robust in B. major, and the inner setae on the proximal preaecoxal endite, coxal and allobasal endites differ considerably between species. In B. pseudochelae these four setae are fine and weakly chitinised, but in B. major and H. searli they are heavily chitinised and falciform, and in H. searli the most proximal is enlarged and aculeate with four sharp lateral spinules. Maxilliped (Fig. 9) The maxillipeds of B. major and B. pseudochelae are similar both in overall structure and relative size. The endopodal setae are the largest and five of these in B. major and three in B. pseudochelae are heavily chitinised and falciform. In H. searli, by contrast, the setae of the coxa and basis are the largest and the endopodal setae are very delicate. In both B. major and B. pseudochelae the maxillipeds are about twice the length of the second maxillae, but in H. searli the two appendages are of about the same length. Gut contents In this study the gut contents analysis gives a minimum indication of the degree of carnivory by the three calanoids. Gut contents are dependant not only on the ability of a predator to eat a particular prey item, but also on the item's availability (presence/ absence, relative abundance) in the habitat, which is influenced by, for example, seasonal changes in abundance, predator density etc. Such aspects were not assessed in this study, so items which may have been eaten but which were absent from the habitat were missed. We attempted to reduce the uncertainty of the analysis by using 10 sites and sampling over a restricted time period (Table 2), and in many of the sites two of the species co-occurred which further

9 392 New Zealand Journal of Marine and Freshwater Research, 1999, Vol. 33 Fig. 5 Mandible coxae, showing details of the gnathobase cutting edges. A, Boeckella major, B, Boeckella pseudochelae; and C, Hemiboeckella searli Carnivores CD Omr ivc res HerL ivores T Bm Bp Hs Fig. 6 Edge indices (mean + SD). Bm, Boeckella major (n = 16); Bp, Boeckella pseudochelae (n = 11); Hs, Hemiboeckella searli (n = 14). Edge index ranges for herbivores, omnivores, and carnivores determined by Itoh (1970) are also shown. improves the comparability of diets between species. However, determination of the complete diets and degree of selectivity between food items requires further detailed study. The gut contents data showed that all three species are omnivorous but that the degree of carnivory differs markedly between them. B. major is clearly the most carnivorous and B. pseudochelae the least (Tables 4 and 5). B. major had eaten the widest range of animal taxa (19 in all), including large cladocerans (Daphnia spp.), calanoid and cyclopoid copepods (both nauplii and copepodite stages), rotifers (the most common group), and mites (Table 5). H. searli had consumed 12 different taxa, and there were fewer rotifer species than in B. major and cladocerans were absent. Unlike B. major, H. searli had eaten harpacticoids and tardigrades. This may indicate that H. searli feeds nearer the bottom of pools, where harpacticoids and tardigrades are likely to be more abundant, than does B. major which may

10 Green & Shiel Mouthpart morphology of calanoid copepods 393 Fig. 7 First maxilla. A, Boeckella major, B, Boeckella pseudochelae; and C, Hemiboeckella searll. feed more in open water, where Daphnia is usually most abundant. B. pseudochelae had ingested only 8 taxa, mainly rotifers, but also including cladocerans and calanoid nauplii. No calanoid, cyclopoid, or harpacticoid copepodites were recorded among its food. Its diet perhaps suggests open water feeding. DISCUSSION The mouthparts of Boeckella major show a number of features reported in calanoid copepods of carnivorous tendencies. For example, its mandibular blade, with two enlarged ventral teeth and a multi-cusped tooth row, is similar to those of the freshwater species Diaptomus shoshone, Epischura lacustris, and Limnocalanus macrurus (Wong 1984), and the marine forms Metridia princeps and Spinocalanus similis (Arashkevich 1969) and Centropages typicus and C. hamatus (Anraku & Omori 1963). As well, B. major's edge index, although within the omnivorous range, is close to that characteristic of carnivores. The first maxilla of B. major is similar to those of D. shoshone, Senecella calanoides, E. lacustris, and-l macrurus (Wong 1984), Labidocera aestiva, C. typicus, and C. hamatus (Anraku & Omori 1963) and Metridia longipes (Arashkevich 1969). All these species feed on animals and have solid spines on the arthrite and medial endites of the first maxilla that are considered useful for handling animal prey. However, this appendage is still rather generalised in B. major and there are none of the extreme modifications (e.g., reduction of outer elements and development of massive spines) characteristic of totally carnivorous species such as Tortanus discaudatus (Anraku & Omori 1963) and Candacia columbiae and Heterorhabdus tanneri (Arashkevich 1969). The robust falciform setae on the endites of the second maxilla of B. major are structures that would enhance its ability to grasp animal prey and the orientation of these setae, pointing toward the mouth, should aid in pushing prey

11 394 New Zealand Journal of Marine and Freshwater Research, 1999, Vol. 33 Fig. 8 Second maxilla. A, Boeckella major, B, Boeckella pseudochelae; and C, Hemiboeckella searli. Setae shown in solid black are very heavily chitinised. towards the mandibles and in stopping its escape. The massive development of these setae does not seem to have been reported previously in freshwater calanoids, in which they are usually weakly developed (e.g., Diaptomus kenai (Chapman 1982) but similar structures are found in the marine species M. princeps and Lucicutia macrocera, both of which include animals in the diet (Arashkevich 1969). As in the instance of the first maxilla, however, extreme modifications of the second maxilla (e.g., reduction of proximal elements and the development of very large aculeate and unguiform setae) that occur in such obligate carnivores as T. discaudatus (Anraku & Omori 1963), L. macrurus (Wong 1984), and Paraeuchaeta rubra and C. columbiae (Arashkevich 1969) are not present. The enlarged solid falciform endopodal setae of the maxilliped of B. major are also probably adaptations for carnivory, and could assist in grasping animals and pushing them towards the mouth. In these respects the maxillipeds of B. major are similar to those of M. princeps and L. macrocera, but are not as extremely modified for carnivory as those of E. lacustris and L. macrurus (Wong 1984) or Cornucalanus indicus (Arashkevich 1969), all of which have small numbers of extremely enlarged aculeate or unguiform setae on the endopods. The very large body size of B. major, and its proportionately large mouthparts, are features that will enable it to feed on larger prey items than H. searli and B. pseudochelae. Overall, the mouthpart morphology of B. major suggests that it is likely to be an omnivore with carnivorous tendencies and the capability of feeding on relatively large animals. These predictions are borne out by the gut contents analysis. In H. searli, features associated with carnivory are evident mainly in the mandible and second maxilla. The edge index is within the carnivorous range

12 Green & Shiel Mouthpart morphology of calanoid copepods 395 Fig. 9 Maxilliped. A, Boeckella major, B, Boeckella pseudoche/ae; and C, Hemiboeckella searli. Setae shown in solid black are very heavily chitinised. mainly because of the enlarged ventral tooth and the large diastema between it and the rest of the tooth row. These features are also found, for example, in L. macrurus (Wong 1984) and D. kenai (Chapman 1982), both of which feed on animals (Wong 1984). The enlarged medial setae on the endites of the second maxilla, particularly the very enlarged distal aculeate one, are the most obvious carnivorous adaptations in H. searli. Even more than in B. major, these structures would help grasp prey and push it towards the mouth. The presence of a large aculeate seta does not appear to have been recorded previously in a freshwater calanoid, but is known from such marine species as Spinocalanus similis and Pseudochirella polyspina, both of which are classified as mixed feeders (Arashkevich 1969). The short weak maxilliped of H. searli is not adapted for carnivory and the only features of the first maxilla that could be associated with predation are the robust setae of the praecoxal arthrite. The mouthparts of H. searli thus indicate an omnivorous diet, with carnivorous tendencies. However, because of the smaller body size and lack of an enlarged spinose maxilliped, H. searli is likely to be restricted to smaller prey than is B. major. These predictions are generally in line with the gut content analysis although, as noted above, the analysis gives a conservative estimate of dietary range and H. searli may be more carnivorous than indicated by our relatively restricted sample size. The presence of harpacticoid copepods in the gut contents of//, searli is suggested to be an indication that it might feed near the bottom

13 396 New Zealand Journal of Marine and Freshwater Research, 1999, Vol. 33 of pools. The shortened maxilliped could be an ad- (Arashkevich 1969). As in B. major, the maxilliped aptation that enables a closer approach to the bot- has well-developed falciform setae that would be torn and so allowing the second maxilla to directly useful for grasping prey, but the first and second grasp prey. maxillae do not show any carnivorous features. On Of the three species, B. pseudochelae has the the basis of its mouthparts, B. pseudochelae would fewest carnivorous adaptations in its mouthparts. Its thus seem to be an omnivore with herbivorous tenedge index is moderately high, but the morphology dencies, a prediction that is largely confirmed from of the cutting edge of the mandible is more like that examination of its gut contents, of species with herbivorous or weakly carnivorous We conclude that overall the mouthpart morpholtendencies, such as Diaptomus sicilis and S. ogy of these copepods gives a good indication of calanoides (Wong 1984), and Calanus cristatus their diet. Features of the maxillae and maxillipeds Table 4 Occurrence of animals and algae in the gut contents of the three copepods. Boeckella major Hemiboeckella searli Boeckella pseudochelae % with animals % with algae n Table 5 Animals recorded in the gut contents. indicates presence. Food categories Boeckella major Hemiboeckella searli Boeckella pseudochelae Cladocera Chydoridae Daphnia spp. Copepoda Calanoid nauplii Calanoid copepodites Cyclopoid nauplii Cyclopoid copepodites Harpacticoid nauplii Harpacticoid copepodites Rotifera Bdelloid Conochilus cf. natans Filinia cf. grandis Keratella sp. Keratella cf. procurva Lecane sp. a Lecane sp. b Lepadella sp. Lepadella cf. patella Notommata sp. Rotifer (indet.) Trichocerca sp. Trichocerca (Diurella) sp. Trichocerca cf. grandis Trichocerca cf. inermis Testudinella sp. Others Mite Peritrich Tardigrade Total

14 Green & Shiel Mouthpart morphology of calanoid copepods 397 are particularly useful but the mandible edge index appears to be less discriminative here than suggested by Itoh's (1970) study, possibly because there is a gradual transition from omnivory to carnivory with increasing index and the three boeckellids lie within this transitional range. In Itoh's study strict carnivores (e.g., in the families Candaciidae and Heterorhabdidae) had very high edge indices between 1500 and 2700, well above those found in the present study. Examination of mouthpart morphology is thus likely to have utility for determining the trophic position of other calanoid copepods in studies of Australian freshwater habitats when, as is often the case, only preserved material is available. As well it is clear that all the species examined do consume animals. In order of apparent carnivorous tendencies their rank is B. major>h. searli>b. pseudochelae, although this ranking must be regarded as an initial estimate only because of the conservative nature of our dietary analysis. The only other Australian calanoid copepod known to be carnivorous is Boeckella triarticulata. Kobayashi (1991, 1993) found that it had ingested rotifers in Wallerawang and Lyell reservoirs, although it was predominantly herbivorous in these habitats, and Maly & Maly (1997) in laboratory trials showed it could consume Calamoecia tasmanica. Other species are likely to be carnivorous, however, especially those of temporary pools. In such habitats being carnivorous is probably a good strategy for a calanoid copepod, especially in the early stages of pool development, because of the lack of algae but abundance of animals emerging from resting stages (Lake et al. 1989). It appears that B. major in particular has a considerable capacity for carnivory, and we speculate that in the fishless temporary pools where it occurs (Lake et al. 1989; Shiel et al. 1998) it has the potential to be the main predator, as is Heterocope septentrionalis in arctic pools (Luecke & O'Brien 1983). Heterocope predation markedly alters the zooplankton community size structure of such pools and it would be of interest to know whether B. major can produce a similar effect in Australian fresh waters. ACKNOWLEDGMENTS JDG is grateful to the Murray-Darling Freshwater Research Centre for extending facilities and hospitality during this study, and to the University of Waikato Leave Committee for granting a period of sabbatical leave. We are also grateful to Yoshi Kobayashi who provided a translation of parts of Itoh's paper and to Kathryn and Bruce Hicks for providing congenial conditions during the preparation of the manuscript. Two anonymous referees made valuable suggestions for improving the manuscript. REFERENCES Anderson, R. S. 1967: Diaptomid copepods from two mountain ponds in Alberta. Canadian Journal of Zoology 45: Anraku, M.; Omori, M. 1963: Preliminary survey of the relationship between the feeding habit and the structure of the mouthparts of marine copepods. Limnology and Oceanography 8: Arashkevich, Y. G. 1969: The food and feeding of copepods in the north-western Pacific. Oceanology 9: Chapman, M. A. 1982: A study of the mouthparts of some Diaptomus species (Copepoda: Calanoida). Journal of Natural History 16: Chapman, M. A.; Lewis, M. H. 1976: An introduction to the freshwater Crustacea of New Zealand. Auckland and London, Collins Bros. & Co. Ltd. Green, J. D.; Shiel, R. J. 1992: A dissection method for determining the gut contents of calanoid copepods. Transactions of the Royal Society of South Australia 116: Huys, R.; Boxshall, G. A. 1991: Copepod evolution. The Ray Society. 414 p. Itoh, K. 1970: A consideration on feeding habits of planktonic copepods in relation to the structure of their oral parts. Bulletin of the Plankton Society of Japan 17: Jerling, H. L.; Woolridge, T. H. 1994: Comparative morphology of the feeding appendages of four mesozooplankton species in the Sunday's River estuary. South African Journal of Zoology 29: Kerfoot, W. C. 1977: Implications of copepod predation. Limnology and Oceanography 22: Kerfoot, W. C. 1978: Combat between predatory copepods and their prey: Cyclops, Epischura, and Bosmina. Limnology and Oceanography 23: Kobayashi, T. 1991: Body lengths and maximum gut food-particle sizes of the dominant cladocerans and calanoid copepods in Wallerawang Reservoir, New South Wales. Australian Journal of Marine and Freshwater Research 42: Kobayashi, T. 1993: Resource partitioning of Calamoecia lucasi Brady and Boeckella triarticulata (Thomson) (Copepoda: Calanoida) in an Australian reservoir. Hydrobiologia 254:

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