New insights on Antarctic gorgonians' age, growth and their potential as paleorecords

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Highlights

  • Longevity in Antarctic gorgonians was confirmed, with lifespans of hundreds of years.

  • RGR of Thouarella species were the lowest ever reported for any gorgonian species.

  • SEM microanalyses identified carbonate-rich and organic-rich layers in the skeletons.

Abstract

Antarctic benthic communities have long been regarded as relicts of the past, since they have developed in a very stable environment and are formed by slow-growing and extraordinary long-lived organisms. However, little is known about the life history traits of gorgonian species, which are considered key components of the Antarctic benthos. In this study, age, Radial Growth Rates (RGR) and skeletal composition of Thouarella variabilis, Fannyella abies and Fannyella rossii colonies (Octocorallia, Primnoidae) that inhabit Antarctic shelf waters were examined. The radioisotopes 14C and 210Pb used for dating revealed that these colonies are long-lived, with ages spanning from 50 to 1100 years, thus confirming the archaic character of the Antarctic ecosystem. Some RGR obtained are among the lowest rates ever reported for primnoid species and gorgonians as a whole, with Thouarella species showing rates of 5.08 µm yr−1. Growth ring deposition seemed to occur every 2–3 years on average, although this result cannot be confirmed. Irregularities in the growth rings could be observed under the Scanning Electron Microscope (SEM) as fluctuations in the skeletal composition, which may be indicative of changes in the environmental conditions, most possibly primary production.

Introduction

Antarctic benthic communities are archaic in structure and function, and can be compared to Paleozoic and deep-sea assemblages in their ecological functioning (Aronson et al., 2007). Primnoid gorgonians are, next to sponges, key components of such communities, playing an important role in structuring those habitats (Brandt et al., 2007). Indeed, an astonishingly diverse fauna of ophiuroids, asteroids, echinoids, pycnogonids, isopods, amphipods, nemerteans and gastropods can be found living in association with these sessile organisms (Arntz et al., 1992). However, and despite their key role in those benthic communities, gorgonians are among the least studied group of Antarctic macrofauna and little is known about their life history traits beyond taxonomic features (Gili et al., 2001).

Like any other modular organism, Primnoids – and octocorals in general – grow through the iterated replication of individual modules to form large, integrated individuals or colonies (Lasker et al., 2003). Estimation of age and growth rates of gorgonian species has generally been carried out by analysing the skeleton density bands observed in thin cross-sections at the base of the colony. Primnoids deposit a 2-part skeleton of calcium carbonate (CaCO3) and gorgonin at different densities, resulting in apparent rings or bands (Barnes and Lough, 1993, Goldberg, 1976, Sherwood et al., 2005b). The reasons for such variations have been speculated upon, for which different suggestions have been made: (1) greater food availability during certain times of the year (Sherwood et al., 2005a, Sherwood et al., 2005b), (2) variations in the extent of the protein tanning (Goldberg, 1976) or even (3) structural requirements of the species (Lewis et al. 1992). An annual periodicity in the deposition of these bands has been reported in many species worldwide, like Muricea californica and Muricea fructicosa in Californian waters (Grigg, 1974), Plexaura sp. from Florida Reefs (Ward-Paige et al., 2005) and the Mediterranean red coral Corallium rubrum (Marschal et al., 2004; Weinbauer et al., 2000). More recently, radiometric dating techniques applied to the skeleton of the Primnoid species Primnoa resedaeformis, or the antipatharians Stauropathes artica and Keratosis ornata, revealed that these organisms are extraordinary long-lived and display a very defined pattern regarding the deposition of annual rings (Sherwood and Edinger, 2009, Sherwood et al., 2005b). Although no study has ever focused on Antarctic gorgonian's longevity, many marine sponges dwelling in Antarctic waters have proven to be extraordinary long-lived (Arntz et al., 1992, Dayton et al., 2013, Fallon et al., 2010), suggesting similar or even higher lifespans for Primnoid gorgonians.

Previous works have revealed the likelihood that long-lived gorgonians and corals may have in explaining past environmental conditions through chemical traces left in their skeletons (Druffel, 1997, Sherwood et al., 2009, Thresher et al., 2010). In this sense, skeleton chemistry analyses performed over tropical species have revealed differences in daily light fluctuations (Lewis et al., 1992), lunar cycles and monthly tidal pressures (Risk et al., 2002, Tracey et al., 2007), surface productivity variations (Sherwood et al., 2005b) and annual seawater temperature oscillations (Thresher et al., 2010, Weinbauer et al., 2000).

Following the possibilities brought up by modern technologies, this study aims to investigate the longevity of Antarctic gorgonians through the analysis of their skeleton, understanding at the same time their growth patterns by analysing the skeletal composition of three Primnoid species that inhabit the shelf waters of the Antarctic realm.

Section snippets

Study area

Gorgonians used in this study were sampled over the continental shelf of Weddell and Ross Seas (Fig. 1). The Antarctic continental shelf covers an area of over 4 million sq km, with depths ranging between 400 and 500 m, although depths over 1000 m have been recorded in specific regions (Dayton, 1990). The unusual depth of the Antarctic continental shelf resulted from ice grounding and scouring during the last glacial maximum and the consequent isostatic depression of the continent (Clarke, 1996).

Radiometric dating

Radiocarbon analyses estimated an age of 1100±112 yr for the gorgonian TV6388, corresponding to the species Thouarella variabilis (Table 2, Table 3). Specimens of Fannyella abies (FA6329) and Fannyella rossii (FR6336) also resulted to be very old, with ages of 329±10 and 354±24 yr respectively. The core of one Fannyella rossi specimen (FR6312-2) with a BP age of 1345±34 minus the Delta-R value of 928±29 years, gave a corrected (but not calibrated) age of 417 yr BP, which is very close to the

Radiometric dating

Results yielded by this study provide convincing evidence that Antarctic gorgonians are extraordinary long-lived organisms, with lifespans that probably range between a few to several hundreds of years (Fig. 5). Longevity of Antarctic marine invertebrates has been recognised for a long time (Arntz et al., 1992), although most of benthic research in Antarctica has generally focused in sponge species, probably since they constitute one of the most abundant taxa. In this sense, the Antarctic

Conclusions

We conclude that results presented here support the long-standing idea of Antarctic benthos longevity as the gorgonians examined – keystone species of the benthic communities – are indeed long-lived and show growth rates among the slowest ever reported for gorgonian species. These features could only be explained as a result of different environmental characteristics: long-term stability, low predation pressure and high quality food supply.

In addition, these preliminary results on the

Acknowledgements

We thank Polarstern and Tangaroa crew and Pablo López-González for providing the speciments. We are also grateful with the Marine Benthic Ecology and Conservation group from the Marine Science Institute of Barcelona, especially to Stefano Ambroso, Enrique Isla and SEM responsible José-Manuel Fortuño. We thank the radioisotopes technicians Dr. Santiago Hurtado and Francisco Javier Santos for their assistance in dating process, and technicians at the Faculty of Geology Alejandro Gallardo, Dolors

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