Reproductive success in Antarctic marine invertebrates

Abstract

The nearshore Antarctic marine environment is unique, characterised by low but constant temperatures that contrast with an intense peak in productivity. As a result of this stenothermal environment, energy input has a profound ecological effect. These conditions have developed over several millions of years and have resulted in an animal physiology that is highly stenothermal and sometimes closely coupled with the seasonal food supply, e.g. reproductive periodicity and food storage. Therefore, Antarctic marine animals are likely to be amongst the most vulnerable species worldwide to environmental modifications and can be regarded as highly sensitive barometers for change. Reproductive success is a vital characteristic in species survival and evaluation of change in reproductive condition with time key to identifying vulnerable taxa. Characterising reproductive success with time is a major requirement in predicting species response to change and the early stages of species loss.

Some invertebrates are highly abundant in shallow water sites around the Antarctic and form conspicuous members of the Antarctic benthos. Three common echinoderms and one nemertean were sampled from sites adjacent to the British Antarctic Survey’s Rothera Research Station, Adelaide Island, on the West Antarctic Peninsula between 1997-2001. Reproductive patterns were determined by histological analyses of gonad tissue.

This study provided further evidence for inter-annual variation in Antarctic gametogenic development, which appeared to be driven to some extent by trophic position and reliance on the seasonal phytoplankton bloom. The largest variation in reproductive condition was demonstrated for the detritivorous brittle star, Ophionotus victoriae. The seasonal tempos of this echinoderm have been attributed in part, to the seasonal sedimentation events common in the high Antarctic. The reproductive patterns in the scavenging starfish, Odontaster validus and the predatory nemertean, Parborlasia corrugatus showed less inter-annual variation. The de-coupling of these invertebrates from the intensely seasonal phytoplankton bloom appeared to partially account for the reproductive trends observed. The lack of inter-annual variation in the reproduction of the filter-feeding sea-cucumber, Heterocucumis steineni, was somewhat counterintuitive, although problems with sample processing probably accounted for the majority of this anomaly.

Echinoderms were also collected during the Antarctic summer field seasons in 2003 and 2004. A series of fertilisation success studies were undertaken comparing the adaptations in an Antarctic and an equivalent temperate starfish to achieve optimal numbers of fertilised eggs, and elemental analyses were used to estimate the nutritional and energetic condition of the bodily and reproductive tissues in two Antarctic echinoderms.

Fertilisation studies indicated that Antarctic invertebrates require 1-2 orders of magnitude more sperm to ensure optimal fertilisation success. These sperm tended to be long-lived and capable of fertilising eggs 24+ hours after release. The study suggested that synchronous spawning, aggregations and specific pre-spawning behaviour are employed to help counter the deleterious effects of sperm limitation. The Antarctic eggs and sperm were also highly sensitive to even small modifications in temperature and salinity, affecting the number of eggs fertilised. Such stenothermy is of particular relevance if the 1-2ºC rise in global temperature, predicted over the next century, is realised.

Biochemical composition of body components of two species of Antarctic echinoderm indicated a significant difference in the composition between the male and female gonad, particularly in the Antarctic brittle star Ophionotus victoriae. The ovaries contained a much larger proportion of lipid compared to the testes, and demonstrated a distinct seasonality in composition. Higher levels of lipid were observed in the ovary during the austral winter coincident with a period of reproductive investment and maturing oocytes in the gonad. O. victoriae exhibited lower amounts of lipid in the late austral spring suggesting the removal of mature oocytes from the ovary through spawning. The seasonality in composition and the high levels of lipid and protein measured in the ophiuroid gut tissue, suggested the gut might play a role in providing material and energy for metabolic function and possibly gametogenesis; higher lipid levels were apparent during the period of seasonal phytodetrital flux. The role of the pyloric ceaca in asteroids as a nutrient storage organ was also evident in the high levels of both protein and lipid observed in this bodily component in the star fish, Odontaster validus.

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ORCID for L.J. Grange: orcid.org/0000-0001-9222-6848

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