Abstract
Mate location and recognition are essentially asymmetrical processes in the reproductive biology of calanoid copepods with the active partner (the male) locating and catching the largely passive partner (the female). This behavioural asymmetry has led to the evolution of sexual dimorphism in copepods, playing many pivotal roles during the various successive phases of copulatory and post-copulatory behaviour. Sexually dimorphic appendages and structures are engaged in (1) mate recognition by the male; (2) capture of the female by the male; (3) transfer and attachment of a spermatophore to the female by the male; (4) removal of discharged spermatophore(s) by the female; and (5) fertilization and release of the eggs by the female. In many male calanoids, the antennulary chemosensory system is enhanced at the final moult and this enhancement appears to be strongly linked to their mate-locating role, i.e. detection of sex pheromones released by the female. It can be extreme in calanoids inhabiting oceanic waters, taking the form of a doubling in the number of aesthetascs on almost every segment, and is less expressed in forms residing in turbulent, neritic waters. Mate recognition is a process where chemoreception and mechanoreception presumably work in conjunction. The less elaborate male chemosensory system in the Centropagoidea is counterbalanced by females playing a more active role in generating hydromechanical cues. This is reflected in females in the shape of the posterior prosomal margin, the complexity of urosomal morphology and the size of the caudal setae. Visual mate recognition may be important in the Pontellidae, which typically show sexual dimorphism in eye design. The most distinctive sexual dimorphism is the atrophy of the mouthparts of non-feeding males, illustrating how copepod detection systems can be shifted to a new modality at the final moult. In the next phase, the male captures the female using the geniculate antennule and/or other appendages. Three types of antennulary geniculations are recognized, and their detailed morphology suggests that they have originated independently. Grasping efficiency can be enhanced by the development of supplemental hinges. The scanty data on capture mechanisms in males lacking geniculate antennules are reviewed. It is suggested that the loss of the antennulary geniculation in many non-centropagoidean calanoids has evolved in response to increasing predator pressure imposed on pairs in amplexus. Spermatophore transfer and placement are generally accomplished by the modified leg 5 of the male. In some males, leg 5 consists of both a chelate grasping leg and a spermatophore-transferring leg, whereas in others, only the latter is developed. Tufts of fine setules/spinules and/or sclerotized elements on the terminal portion of the leg are involved in the transfer and attachment of the spermatophore. The configuration of gonopores, copulatory pores and their connecting ducts in the female genital double-somite is diversified in the early calanoid offshoots such as Arietellidae and Metridinidae, whereas in more derived groups, it is constant and invariable, with paired gonopores and copulatory pores located beneath a single genital operculum. The absence of seminal receptacles in most Centropagoidea limits the fermale’s ability to store sufficient sperm for multiple egg batches, suggesting that repeated mating is necessary for sustained egg production. Discharged spermatophores are usually removed by the female leg 5 and/or specialized elements on other legs. In Tortanus (Atortus) Ohtsuka, which has rudimentary fifth legs in the female and complex coupling devices in the male, a spermatophore supposedly remains on the female urosome, since eggs appear to be released from a ventral opening of the spermatophore. The type of sexual dimorphism is closely related to habitat and biology. Some hyperbenthic families never show multiplication of aesthetascs on the male antennule, whereas families of the open pelagic realm such as the Aetideidae always have non-feeding males exhibiting secondary multiplication of antennulary aesthetascs. The various aspects and diversity of calanoid sexual dimorphism are herein considered in an evolutionary context.
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References
Andronov, V. N., 1970. Some problems of taxonomy of the family Paracalanidae (Copepoda). Zool. Zh. 49: 980–985 (in Russian with English abstract).
Andronov, V. N., 1974. Phylogenetic relations of large taxa within the suborder Calanoida (Crustacea, Copepoda). Zool. Zh. 53: 1002–1012 (in Russian with English abstract).
Andronov, V. N., 1992. Ryocalanus admirabilis sp. n. (Copepoda, Calanoida, Ryocalanidae) from the central-eastern Atlantic. Zool. Zh. 71: 140–144 (in Russian with English abstract).
Atkinson, A., 1991. Life cycles of Calanoides acutus, Calanus simillimus and Rhincalanus gigas (Copepoda: Calanoida) within the Scotia Seas. Mar. Biol. 109: 79–91.
Barthélémy, R.-M., 1999. Functional morphology and taxonomic relevance of the female genital structures in the Acartiidae (Copepoda: Calanoida). J. mar. biol. Ass. U.K. 79: 857–870.
Barthélémy, R.-M., C. Cuoc, D. Defaye, M. Brunet & J. Mazza, 1998. Female genital structures in several families of Centropagoidea (Copepoda: Calanoida). Phil. Trans. r. Soc. Lond. B 353: 721–736.
Blades, P. I., 1977. Mating behaviour of Centropages typicus (Copepoda: Calanoida). Mar. Biol. 40: 57–64.
Blades, P. I. & M. J. Youngbluth, 1979. Mating behavior of Labidocera aestiva (Copepoda: Calanoida). Mar. Biol. 51: 339–355.
Blades, P. I. & M. J. Youngbluth, 1980. Morphological, physiological and behavioural aspects of mating in calanoid copepods. In Kerfoot W. C. (ed.), Evolution and Ecology of Zooplankton Communities. The University Press of New England, Hanover (N.H.): 39–51.
Blades-Eckelbarger, P. I., 1991. Functional morphology of spermatophores and sperm transfer in calanoid copepods. In Bauer R. T. & J. W. Martin (eds), Crustacean Sexual Biology. Columbia University Press, New York: 246–270.
Bowman, T. E. & J. G. Gonzalez, 1961. Four new species of Pseudocyclops (Copepoda: Calanoida) from Puerto Rico. Proc. U.S. natn. Mus. 113: 37–59.
Boxshall, G. A., 1985. The comparative anatomy of two copepods, a predatory calanoid and a particle-feeding mormonilloid. Phil. Trans, r. Soc. Lond. B 311: 303–377.
Boxshall, G. A. & R. Huys, 1998. The ontogeny and phylogeny of copepod antennules. Phil. Trans. r. Soc. Lond. B 353: 765–786.
Boxshall, G. A., J. Yen & J. R. Strickler, 1997. Functional significance of sexual dimorphism in the cephalic appendages of Euchaeta rimana Bradford. Bull. mar. Sci. 61: 387–398.
Bradford, J. M., 1988. Review of the taxonomy of the Calanidae (Copepoda) and the limits to the genus Calanus. Hydrobiologia 167/168: 73–81.
Bradford, J. M., L. Haakonssen & J. B. Jillett, 1983. The marine fauna of New Zealand: pelagic calanoid copepods: families Euchaetidae, Phaennidae, Scolecithricidae, Diaixidae and Tharybidae. Mem. N.Z. oceanogr. Inst. 90: 1–150.
Bradford, J. M. & J. B. Jillett, 1980. The marine fauna of New Zealand: pelagic calanoid copepods: family Aetideidae. N.Z. oceanogr. Inst. Mem. 86: 1–102.
Bradford-Grieve, J. M., 1994. The marine fauna of New Zealand: pelagic calanoid Copepoda: Megacalanidae, Calanidae, Paracalanidae, Mecynoceridae, Eucalanidae, Spinocalanidae, Clausocalanidae. Mem. Z. Z. oceanogr. Inst. 102: 1–160.
Bradford-Grieve, J. M., 1999. The marine fauna of New Zealand: pelagic calanoid Copepoda: Bathypontiidae, Arietellidae, Augaptilidae, Heterorhabdidae, Lucicutiidae, Metridinidae, Phyllopodidae, Centropagidae, Pseudodiaptomidae, Temoridae, Candaciidae, Pontellidae, Sulcanidae, Acartiidae, Tortanidae. Mem. N.Z. oceanogr. Inst. 111: 1–268.
Braga, E., R. Zardoya, A. Meyer & J. Yen, 1999. Mitochondrial and nuclear rRNA based copepod phylogeny with emphasis on the Euchaetidae (Calanoida). Mar. Biol. 133: 79–90.
Cuoc, C., D. Defaye, M. Brunet, R. Notonier & J. Mazza, 1997. Female genital structures of Metridinidae (Copepoda, Calanoida). Mar. Biol. 129: 651–665.
Damkaer, D. M., 1975. Calanoid copepods of the genera Spinocalanus and Mimocalanus from the central Arctic Ocean, with a review of the Spinocalanidae. NOAA tech. Rep. NMFR Circ. 391: 1–88.
Deevey, G. B., 1973. Bathypontia (Copepoda: Calanoida): six species, one new, from the Sargasso Sea. Proc. biol. Soc. Wash. 86: 357–372.
Ferrari, F. D., 1978. Spermatophore placement in the copepod Euchaeta norvegica Boeck 1872 from deepwater dumpsite 106. Proc. biol. Soc. Wash. 91: 509–521.
Ferrari, F. D. & A. Benforado, 1998. Setation and setal groups on antenna 1 of Ridgewayia klausruetzleri, Pleuromamma xiphias and Pseudocalanus elongatus (Crustacea: Copepoda: Calanoida) during the copepodid phase of their development. Proc. Biol. Soc. Wash. 11: 209–221.
Ferrari, F. D. & M. Dojiri, 1987. The calanoid copepod Euchaeta antarctica from Southern Ocean Atlantic sector midwater trawls, with observations on spermatophore dimorphism. J. crust. Biol. 7: 458–180.
Fleminger, A., 1973. Pattern, number, variability and taxonomic significance of integumental organs (sensilla and glandular pores) in the genus Eucalanus (Copepoda, Calanoida). Fishery Bull. natn. ocean. atmos. Adm. 71: 956–1010.
Fleminger, A., 1975. Geographical distribution and morphological divergence in American coastal-zone planktonic copepods of the genus Labidocera. In Cronin L. E. (ed.), Chemistry, Biology and the Estuarine System. Estuar. Res. 1: 392–419.
Fleminger, A., 1985. Dimorphism and possible sex change in copepods of the family Calanidae. Mar. Biol. 88: 273–294.
Fleminger, A. & K. Hulsemann, 1977. Geographical range and taxonomic divergence in North Atlantic Calanus (C. helgolandicus, C. finmarchicus and C. glacialis). Mar. Biol. 40: 233–248.
Fosshagen, A., G. A. Boxshall & T. M. Iliffe, 2001. The Epacteriscidae, a cave-living family of calanoid copepods. Sarsia 86, in press.
Frost, B. W. & A. Fleminger, 1968. A revision of the genus Clausocalanus (Copepoda: Calanoida) with remarks on distributional patterns in diagnostic characters. Bull. Scripps Inst. Oceanogr., tech. Ser. 12: 1–235.
Giesbrecht, W., 1892. Systematik und Faunistik der pelagischen Copepoden des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna Flora Golf. Neapel 19: 1–831.
Greene, C. H. & M. R. Landry, 1985. Patterns of prey selection in the cruising calanoid predator Euchaeta elongata. Ecology 66: 1408–1416.
Grice, G. D. & K. Hulsemann, 1965. Abundance, vertical distribution and taxonomy of calanoid copepods at selected stations in the north-east Atlantic. J. Zool., Lond. 146: 213–262.
Griffith, A. M. & B. W. Frost, 1976. Chemical communication in the marine planktonic copepods Calanus pacificus and Pseudocalanus sp. Crustaceana 30: 1–8.
Heberer, G., 1932. Untersuchungen über Bau und Funktion der Genitalorgane der Copepoden. I. Der männliche Genitalapparat der calanoiden Copepoden. Z. mikrosk. anat. Forsch. 31: 250–424.
Herring, P. J., 1988. Copepod luminescence. Hydrobiologia 167/168: 183–195.
Hopkins, C. C. E., J. Mauchline & D. S. McLusky, 1978. Structure and function of the fifth pair of pleopods of male Euchaeta norvegica (Copepoda: Calanoida). J. mar. biol. Ass. U.K. 58: 631–637.
Hulsemann, K. & A. Fleminger, 1990. Taxonomic value of minute structures on the genital segment of Pontellina females (Copepoda: Calanoida). Mar. Biol. 105: 99–108.
Huys, R. & G. A. Boxshall, 1991. Copepod evolution, The Ray Society, London: 468 pp.
Jacoby, C. A. & M. J. Youngbluth, 1983. Mating behavior in three species of Pseudodiaptomus (Copepoda: Calanoida). Mar. Biol. 76:77–86.
Katona, S. K., 1973. Evidence for sex pheromones in planktonic copepods. Limnol. Oceanogr. 18: 574–583.
Katona, S. K., 1975. Copulation in the copepod Eurytemora affinis (Poppe,1880). Crustaceana 28: 89–94.
Kimoto, K., J. Nakashima & Y. Morioka, 1988. Direct observations of copepod swarm in small inlet of Kyushu, Japan. Bull. Seikai reg. Fish. Res. Lab. 66: 41–58.
Land, M. F., 1984. Crustacea. In Ali M. A. (ed.), Photoreception and Vision in Invertebrates. NATO ASI Series A, Life Sciences 74: 401–438.
Land, M. F., 1988. The functions of eye and body movements in Labidocera and other copepods. J. exp. Biol. 140: 381–391.
Landry, M. R. & V. L. Fagerness, 1988. Behavioral and morphological influences on predatory interactions among marine copepods. Bull. mar. Sci. 43: 509–529.
Lee, C. M., 1972. Structure and function of the spermatophore and its coupling device in the Centropagidac (Copepoda: Calanoida). Bull. mar. Ecol. 8: 1–20.
Markhaseva, E. L., 1996. Calanoid copepods of the family Aetideidae of the world ocean. Proc. Zool. Inst. russ. Acad. Sci. 268: 1–331.
Markhaseva, E. L. & F. D. Ferrari, 1996. Three new species of Ryocalanus from the eastern tropical Pacific (Crustacea, Copepoda: Ryocalanidae). Zoosystematica Rossica 4: 63–70.
Matthews, J. B. L., 1964. On the biology of some bottom-living copepods (Aetideidae and Phaennidae) from western Norway. Sarsia 16: 1–46.
Mauchline, J., 1998. The biology of calanoid copepods. Adv. mar. Biol. 33: 1–710.
Miller, C. B., B. W. Frost, H. P. Batchelder, M. I. Clemons & R. E. Conway, 1984. Life histories of large, grazing copepods in a subarctic ocean gyre: Neocalanus plumchrus, Neocalanus cristatus and Eucalanus bungii in the northeast Pacific. Prog. Oceanogr. 13: 201–243.
Nishida, S., 1989. Distribution, structure and importance of the cephalic dorsal hump, a new sensory organ in calanoid copepods. Mar. Biol. 101: 173–185.
Ohman, M. D. & A. W. Townsend, 1998. Egg strings in Euchirella pseudopulchra (Aetideidae) and comments on constraints on egg brooding in planktonic marine copepods. J. mar. Syst. 15: 61–69.
Ohtsuka, S., 1992. Calanoid copepods collected from the near-bottom in Tanabe Bay on the Pacific coast of the Middle Honshu, Japan. IV. Pseudocyclopiidae. Publ. Seto mar. biol. Lab. 35: 295–301.
Ohtsuka, S., G. A. Boxshall & H. S. J. Roe, 1994. Phylogenetic relationships between arietellid genera (Copepoda: Calanoida), with the establishment of three new genera. Bull. nat. Hist. Mus. Lond. (Zool.) 60: 105–172.
Ohtsuka, S., A. Fosshagen & S. Putchakarn, 1999. Three new species of the demersal calanoid copepod Pseudocyclops from Phuket, Thailand. Plankton Biol. Ecol. 46: 132–147.
Ohtsuka, S. & K. Kimoto, 1989. Tortanus (Atortus) (Copepoda: Calanoida) of southern Japanese waters, with description of two new species, T. (A.) digitalis and T. (A.) ryukyuensis, and discussion on distribution and swarming behaviour of Atortus. J. crust. Biol. 9: 392–408.
Ohtsuka, S. & J. W. Reid, 1998. Phylogeny and zoogeography of the planktonic copepod genus Tortanus (Calanoida: Tortanidae), with establishment of a new subgenus and descriptions of two new species. J. crust. Biol. 18: 774–807.
Ohtsuka, S., H. S. J. Roe & G. A. Boxshall, 1993. A new family of calanoid copepods, the Hyperbionycidae, collected from the deep-sea hyperbenthic community in the northeastern Atlantic. Sarsia 78: 69–82.
Ohtsuka, S., H. Y. Soh & S. Nishida, 1997. Evolutionary switching from suspension feeding to carnivory in the calanoid family Heterorhabdidae (Copepoda). J. crust. Biol. 17: 577–595.
Othman, B. H. R., 1987. Two new species of Tortanus (Crustacea, Copepoda) from Sabah, Malaysia. Malayan nat. J. 41: 61–73.
Park, T., 1986. Phylogeny of calanoid copepods. Syllogeus 58: 191–196.
Price, H. J., G.-A. Paffenhöfer & J. R. Strickler, 1983. Modes of cell capture in calanoid copepods. Limnol. Oceanogr. 28: 116–123.
Sars, G. O., 1902. Copepoda Calanoida. An Account of the Crustacea of Norway, with short descriptions and figures of all the species 4: 29–144, pls. 17–96.
Schnack-Schiel, S. B & E. Mizdalski, 1994. Seasonal variations in distribution and population structure of Microcalanus pygmaeus and Ctenocalanus citer (Copepoda: Calanoida) in the eastern Weddell Sea, Antarctica. Mar. Biol. 119: 357–366.
Schulz, K., 1990. Pterochirella tuerkayi, a new genus, new species, an unusual calanoid copepod from the deep Gulf of Aden (Indian Ocean). Mitt. hamb. zool. Mus. Inst. 87: 181–189.
Snell, T. W. & M. J. Garmona, 1994. Surface glycoproteins in copepods: potential signals for mate recognition. Hydrobiologia 292/293: 255–264.
Snell, T. W. & P. D. Morris, 1993. Sexual communication in copepods and rotifers. Hydrobiologia 255/256: 109–116.
Soh, H. Y., 1998. Phylogenetic studies of the calanoid copepod superfamily Arietelloidea, with notes on distribution and feeding habits. Doctoral thesis, Hiroshima University, Hiroshima.
Soh, H.Y., S. Ohtsuka, H. Imabayashi & H.-L. Suh, 1999. A new deep-water calanoid copepod and the phylogeny of the genus Nullosetigera nom. nov. in the Nullosetigeridae nom. nov. (pro Phyllopus: Phyllopodidae) from Japanese waters. J. nat. Hist.: 1581–1602.
Strickler, R. & A. K. Bal, 1973. Setae of the first antennae of the copepod Cyclops scutifer (Sars): their structure and importance. Proc. natn. Acad. Sci., U.S.A. 70: 2656–2659.
Suárez-Morales, E. & T. M. Iliffe, 1996. New superfamily of Calanoida (Copepoda) from an anchialine cave in the Bahamas. J. crust. Biol. 16: 754–762.
Svensson, J. E., 1992. The influence of visibility and escape ability on sex-specific susceptibility to fish predation in Eudiaptomus gracilis (Copepoda, Crustacea). Hydrobiologia 234: 143–150.
Tanaka, O., 1956. Rare species of Copepoda Calanoida taken from the Izu region. Breviora 64: 1–8.
Tsuda, A., 1995. “The paradox of the plankton” and species diversity in plankton communities: a review. Bull. Plankton Soc. Japan 42: 105–121 (in Japanese with English abstract).
Tsuda, A. & C. B. Miller, 1998. Mate finding behavior in Calanus marshallae Frost. Phil. Trans. r. Soc. Lond. B353: 713–720.
Tsukagoshi, A., 1988. Reproductive character displacement in the ostracod genus Cythere. J. crust. Biol. 8: 563–575.
Tsukagoshi, A., 1989. The character of male copulatory organ and the distributional pattern of normal pore canals in the ostracod genus Cythere. Bull. Jap. Assoc. Benthol. 35/36: 89–96 (in Japanese with English abstract).
Ueda, H., A. Kawahara, M. Tanaka & M. Azeta, 1983. Underwater observations on copepod swarms in temperate and subtropical waters. Mar. Ecol. Prog. Sen 11: 165–171.
Van Duren, L. A. & J. J. Videler, 1996. The trade-off between feeding, mate seeking and predator avoidance in copepods: behavioral responses to chemical cues. J. Plankton Res. 18: 805–818.
Van Duren, L. A., E. J. Stamhuis & J. J. Videler, 1998. Reading the copepod personal ads: increasing encounter probability with hydromechanical signals. Phil. Trans. r. Soc. Lond. B353: 691–700.
Vaupel Klein, J. C. von, 1982. A taxonomic review of the genus Euchirella Giesbrecht, 1888 (Copepoda, Calanoida). II. The type-species, Euchirella messinensis (Claus, 1863). A. The female of f. typica. Zool. Verh. Leiden 198: 1–131.
Vaupel Klein, J. C. von, 1998. Interpretation of character phylogenies in calanoid copepods by implementing Dollo’s law. J. crust. Biol. 18: 153–160.
Walter, T. C., 1989. Review of the New World species of Pseudodiaptomus (Copepoda: Calanoida), with a key to the species. Bull. mar. Sci. 45: 590–628.
Yen, J., 1988. Directionality and swimming speeds in predator-prey and male-female interactions of Euchaeta rimana, a subtropical marine copepod. Bull. mar. Sci. 43: 395–403.
Yen, J. & J. R. Strickler, 1996. Advertisement and concealment in the plankton: what makes a copepod hydrodynamically conspicuous? Invert. Biol. 115: 191–205.
Yen, J., M. C. Weissburg & M. H. Doall, 1998. The fluid physics of signal perception by mate-tracking copepods. Phil. Trans. r. Soc. Lond. B 353: 787–804.
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Ohtsuka, S., Huys, R. (2001). Sexual dimorphism in calanoid copepods: morphology and function. In: Lopes, R.M., Reid, J.W., Rocha, C.E.F. (eds) Copepoda: Developments in Ecology, Biology and Systematics. Developments in Hydrobiology, vol 156. Springer, Dordrecht. https://doi.org/10.1007/0-306-47537-5_39
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