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Rare sexual anomalies in Temora stylifera (Dana, 1849) (Copepoda: Calanoida).

Temora stylifera (Dana, 1849) is one of the most abundant species of calanoid copepods in neritic waters off Brazil (e.g. Neumann-Leitao et al., 1999). This species has a circumglobal distribution in tropical and subtropical waters (Bradford-Grieve et al., 1999), and has been studied in several aspects such as morphology, feeding ecology and reproductive biology (see Turner et al., 2001).

Antennule (A1), fifth leg (P5), genital somite complex and urosome somites usually contain distinguishable sexual characters that display dimorphism in the order Calanoida. In most calanoid species the geniculated A1 is used for mate recognition and initial capture of the female, by grasping its caudal rami or setae (Ohtsuka and Huys, 2001). Generally, the right side is the geniculate and prehensile appendage, presenting one or two hinged joints, which enables the antennule to fold back upon itself (Blades-Eckelbarger, 1991), a common pattern in numerous families including the Temoridae. In Temora stylifera (Dana, 1849), antennular segments 17 to 19 are modified and segments 18 and 19 are separated by a hinge that allows extension and flexion, used for clasping the female (Corni et al., 2001). The male urosome of calanoid copepods is characterized by having five or, less frequently, four somites and the absence of fusion forming complexes. Females generally display only three or four articulating elements, the first corresponding to a dilated genital double somite, formed by the fusion of the genital and first abdominal somites (Ferrari and Dahms, 2007).

Numerous morphological and sexual anomalies including congenital malformation, intersexuality, gynandromorphism, parasitic castration and sex change have been described in calanoid copepods (e.g. Bayly and Shiel, 2008). Nevertheless, double geniculation of A1 was not documented in extant calanoid and intersex or gynandromorphic individuals of Temora stylifera (Dana, 1849) have not been described until this moment. We report two anomalous specimens found in the Southern Brazilian Bight (Table 1), showing distinct abnormalities in sexually relevant morphological features. Voucher and anomalous specimens were deposited at the Museu de Zoologia at Universidade de Sao Paulo (MZ USP number 18856).

1) Gynandromorphic individual: the animal had a female genital somite and reproductive structures including ovary and oviducts. The remaining sexual characters such as A1 and fifth leg (P5) were typically male (Figure 2); and

2) Male bearing geniculation in both antennules: the specimen was observed alive in microcosms and displayed similar swimming behavior when compared to normal males. This animal did not show any other morphological abnormalities in addition to the double geniculation of A1 (Figure 1). The antennules were symmetrical, showing an identical number of segments, geniculation pattern and size. The configuration of the setae and modified segments follows that described by Corni et al. (2001) for both specimens.

The gynandromorphic individual anomaly was not induced by parasites since detailed examination showed no evidence of infections. How the anomalous characters found in this study had developed remains unknown. Intersexuality is often found in P5 (e.g. Ianora et al., 1987), or A1 (e.g. Flemminger, 1985) rather than on the genital somite. Intersex individuals were described in species of Acartidae, Calanidae, Diaptomidae, Euchaetidae, Metridinidae and Paracalanidae (Ferrari, 1985 among others). Similar data has not been found for the Temoridae and we cannot confirm that the gynandromorphic specimen is an intersex. The fact that A1 and P5 are identical to male appendages is not an ordinary pattern in intersex individuals as well.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Geniculation in both antennules is common in cyclopoid families, such as Fratiidae, Cyclopidae and Cyclopinidae (Boxshall and Halsey, 2004), but not in calanoids. This is the first report of geniculation on both male antennules. The rare geniculation anomaly found here could be interpreted as evolutionary evidence, as it resembles the copepod ancestral condition (Boxshall and Huys, 1998; Huys and Boxshall, 1991). Few studies have documented sexual anomalies in copepods and their causes. Intersexuality is a widespread phenomenom in copepods and might be related to food limitation (Gusmao and McKinnon, 2009 accepted). Aberrant animals are often taken as sexually non-functional individuals, meaning that their occurrence might have consequences to copepod population dynamics. Further research must be carried out on these abnormalities and their behavioral consequences to fully understand their ecological impact. Acknowledgements--We express our gratitude to Frank Ferrari, Geoff Boxshall, Tagea Bjornberg, Janet Reid, Felipe Gusmao, Carlos Rocha and Eduardo Masami for their help at different stages of this work.

Received September 5, 2008--Accepted October 8, 2008--Distributed May 31, 2009 (With 2 figures)

References

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BLADES-ECKELBARGER, PI., 1991. Functional morpholgy of spermatophores and sperm transfer in calanoid copepods. In

BAUER, RT. and MARTIN, JW. (Eds.). Crustacean sexual biology. New York: Columbia University Press. p. 246-270.

BOXSHALL, GA. and HALSEY, SH., 2004. An introduction to copepod diversity. London: Ray Society. 966p.

BOXSHALL, GA. and HUYS, R., 1998. The ontogeny and phylogeny of copepod antennules. Philosophical Transactions of the Royal Society of London B: biological sciences, vol. 353, no. 1369, p. 765-786.

BRADFORD-GRIEVE, JM., MARKHASEVA, EL., ROCHA, CEF. and ABIAHY, B., 1999. Copepoda. In BOLTOVSKOY, D. (Ed.). South Atlantic Zooplankton. Leiden: Backhuys Publishers. p. 869-1098.

CORNI, MG., VIGONI, V. and SCANABISSI, F., 2001. Some ultrastructural features of the reproductive morphology and spermatophore placement of Temora stylifera Dana, 1849 (Copepoda: Calanoida). Crustaceana, vol. 74, no. 1, p. 79-90.

FERRARI, F., 1985. Postnaupliar development of a looking glass copepod, Pleurommama xiphias (Giesbrecht, 1889), with analyses of distributions of sex assimetry. Smithsoniam Contributions to Zoology, no. 420, p. 1-55.

FERRARI, F. and DAHMS, HU., 2007. Post-embryonic development of the Copepoda. Leiden; Boston: BRILL ed. Crustaceana monographs 8.

FLEMMINGER, A., 1985. Dimorphism and possible sex change in copepods of the family Calanidae. Marine Biology, vol. 88, no. 3, p. 273-294.

GUSMAO, LFM. and MCKINNON, DA. 2009. Sex ratios, intersexuality and sex change in copepods. Journal of Plankton Research, accepted)

HUYS, R. and BOXSHALL, GA., 1991. Copepod evolution. London: Ray Society. 468p.

IANORA, A., MAZZOCHI, MG. and SCOTTO Di CARLO, B., 1987. Impact of parasitism and intersexuality on Mediterranean populations of Paracalanus parvus (Copepoda: Calanoida). Diseases of Aquatic Organisms, vol. 3, p. 29-36.

NEUMANN-LEITAO, SN., GUSMAO, LMO., SILVA, TA., NASCIMENTO-VIEIRA, DA. and SILVA, AP., 1999. Mesozoplankton biomass and diversity in coastal and oceanic waters off North-Eastern Brazil. Archive of Fishery and Marine Research, vol. 47, no. 2-3, p. 153-165.

OHTSUKA, S. and HUYS, R., 2001. Sexual dimorphism in calanoid copepods: morphology and function. Hydrobiologia, vol. 453-454, no. 1, p. 441-466.

TURNER, JT., IANORA, A., MIRALTO, A., LAABIR, M. and ESPOSITO, F., 2001. Decoupling of copepod grazing rates, fecundity and egg-hatching success on mixed and alternating diatom and dinoflagellate diets. Marine Ecology Progress Series, vol. 220, p. 187-199.

Martinelli-Filho, JE. *, Melo-Junior M., Cunha, DR. and Lopes, RM.

Departamento de Oceanografia Biologica, Instituto Oceanografico--IO, Universidade de Sao Paulo--USP, Praca do Oceanografico, 191, Cidade Universitaria, CEP 05508-120, Sao Paulo, SP, Brazil * e-mail: zedumar@usp.br
Table 1. Collection details and sampling sites in the
Southern Brazilian Bight where the anomalous specimens
were found.

                     Specimen 1              Specimen 2

Coordinates          23[degrees] 07' 85" S   23[degrees] 31' 37" S
                     and                     and
                     43[degrees] 56'03"W     45[degrees] 05'07"W
Local depth (m)      32                      40
Sampling depth (m)   20                      15-20
Net mesh (mm)        300                     200
Sampling date        August 2002             March 2007
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Title Annotation:NOTES AND COMMENTS
Author:Martinelli-Filho, J.E.; Melo-Junior, M.; Cunha, D.R.; Lopes, R.M.
Publication:Brazilian Journal of Biology
Date:May 1, 2009
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