Polar Biology

, Volume 32, Issue 3, pp 399–402

Lack of acclimation in Ophionotus victoriae: brittle stars are not fish

Authors

  • Lloyd S. Peck
    • British Antarctic SurveyNatural Environment Research Council
  • Alison Massey
    • British Antarctic SurveyNatural Environment Research Council
  • Michael A. S. Thorne
    • British Antarctic SurveyNatural Environment Research Council
    • British Antarctic SurveyNatural Environment Research Council
Original Paper

DOI: 10.1007/s00300-008-0532-y

Cite this article as:
Peck, L.S., Massey, A., Thorne, M.A.S. et al. Polar Biol (2009) 32: 399. doi:10.1007/s00300-008-0532-y

Abstract

Acclimation is possibly the most important criterion deciding an animal’s ability to survive change. Species with poor abilities to acclimate to small environmental change are likely to be the most vulnerable in future warming scenarios. Two separate assemblages of Ophionotus victoriae were slowly acclimated from 0°C to either +2 or +3°C and then held at these higher temperatures over a prolonged timescale. None of the animals were able to acclimate; with failure occurring from day 19 at +3°C and day 24 at +2°C, indicating that this species is very sensitive to small long-term seawater temperature increases. These data indicate that O. victoriae has probably the poorest ability to acclimate to elevated temperatures of any species studied to date. Given previous data showing some Antarctic fish can acclimate to +4°C, the predicted effects of increased seawater temperatures on the Antarctic food web and ecology must be assessed at the individual species level and interpreted with care.

Keywords

OphiuroidAntarcticTemperatureClimate changeAcclimationVulnerability

Introduction

Antarctic organisms are markedly stenothermal (Somero and DeVries 1967; Peck et al. 2004). Most live within a 4°C temperature range or less in their natural environment and have adapted to life in the cold with an equally restricted thermal metabolic envelope. Experimental manipulation of seawater temperatures has shown that Antarctic invertebrates, in particular, are extremely sensitive to temperature changes, with short-term survivable temperature envelopes of only between 5 and 12°C above the minimum sea temperature of −1.86°C (Peck and Conway 2000; Peck 2002). Whilst many die at temperatures below +10°C (Peck 1989; Peck et al. 2002; Pörtner 2002), they lose critical biological functions with temperature elevations of only 1–2°C above current summer maximum seawater temperatures (between 0 and +1.8°C) (Peck et al. 2004). This stenothermality combined with the markedly slowed life histories of most Antarctic marine ectotherms (Arntz et al. 1994) and reduced numbers of eggs produced per female compared to temperate species suggests that if change occurs, Antarctic animals have fewer chances with which to adapt (Peck 2005).

However, such experimental predictions of capacity to cope contrast with ecological evidence, which suggest the potential exists for thermal adaptation plasticity. For example, some Antarctic species living at their geographical extremes (such as at South Georgia) do live in wider temperature regimes (2°C above normal Antarctic sea temperatures, Barnes et al. 2006) and many typically marine species have also now been found in the Antarctic inter-tidal zone, which is a much more extreme thermal environment (Waller et al. 2006). Furthermore many Antarctic taxa are not endemic to Antarctica and occur in wider thermal conditions at cool temperate latitudes (Barnes and Griffiths 2008). The true measure of an organism or species capacity to cope with elevated environmental temperatures and adapt almost certainly lies somewhere between the above extremes.

With this in mind, one fundamental criterion of importance is the rate of temperature change. Recently acclimation capacity has been suggested to be the most important mechanism for surviving change (Stillman 2003). A few studies of Antarctic fish have shown a wide-ranging capacity to acclimate to temperatures as high as +4°C (Seebacher et al. 2005; Podrabsky and Somero 2006; Jin and DeVries 2006). These results are clearly at odds with acute responses for some Antarctic marine invertebrates (Peck et al. 2004). There is now a clear need for more long-term investigations of acclimation.

The dominant ophiuroid in coastal waters around the Antarctic Peninsula is Ophionotus victoriae (Sáiz-Salinas et al. 1997; Arnaud et al. 1998). Found at depths between 5 and 1,266 m (Madsen 1967) and designated as a primary scavenger (Fratt and Dearborn 1984), it clearly occupies a key role in the Antarctic benthic ecosystem. This organism therefore provides an ideal candidate for acclimation studies.

Materials and methods

All O. victoriae were collected at Rothera Research Station, Adelaide Island (67°07″34′S, 68°07′30″W) by SCUBA divers during the austral summer. The +3°C experiment consisted of the animals being placed into three separate baskets in a large jacketed tank fitted with a protein skimmer and filter system with water at ambient temperature (0.4°C), attached to a thermocirculator. They were left for 24 h to acclimatise before slowly raising the temperature to +3°C over a 6-day period. A proportion of the water was changed daily. The +2°C experiment was originally set up in a jacketed tank similar to that described for the +3°C animals; however, after 10 days they were moved to a flow through system heated with 0.5 kW fluoropolymer coated immersion heaters with a PT100 probe (supplied by Dryden Aquaculture) to ensure high water quality standards. Animals were checked daily and point of death identified when there was no movement of the mouthparts. Upon death the disc size was measured with vernier callipers.

Results

+3°C experiment

Mortality first occurred 19 days after the initial temperature rise. All animals died within 32 days (Table 1) and mean survival time was 24.4 days.
Table 1

Disc size and survival time following temperature rise (day) for the two trials

+3°C

+2°C

Day

Disc diameter

Day

Disc diameter

+19

28

+24

26

+20

27

+26

20

+20

21

+32

22

+21

30

+32

26

+21

22

+33

28

+22

25

+36

25

+22

24

+36

18

+22

27

+36

28

+22

21

+36

27

+22

28

+36

23

+22

25

+37

26

+23

24

+37

27

+23

29

+38

25

+23

15

+39

24

+25

29

+41

23

+25

16

+41

23

+25

26

+41

15

+25

21

+41

25

+26

16

+43

20

+27

23

+45

30

+27

16

+46

18

+27

21

+48

31

+27

21

+51

21

+28

22

+53

22

+28

23

+58

25

+28

26

+62

25

+28

23

+62

23

+28

23

+68

21

+28

30

+139

21

+28

26

  

Mean 24.4

Mean 23.6

Mean 45.4

Mean 23.7

SD 2.995

SD 4.199

SD 28.86

SD 3.654

+2°C experiment

Mortality first occurred 24 days after the initial temperature rise (Table 1) All animals bar one died within 68 days (mean survival time for this cohort = 42 days). The final individual lasted 139 days. Adding this last individual into the +2°C cohort slightly increased the overall mean survival time to 45.4 days. Temperature significantly affected survival time (P value <0.01). The disc sizes of the individuals in each experiment were not significantly different with means of 23.6 mm for the 3°C animals and 23.7 mm for the 2°C animals. There was no correlation of survival rate with size of animal (analysis not shown). In both experiments, spontaneous autotomy took place when the temperatures were raised and occurred over the period of the experiment. A control set of brittle stars were held over the same time periods and had no mortalities or autotomy.

Discussion

The data presented here, combined with a previous +3°C brittle star acclimation experiment over the winter of 2005 where no specimens survived more than 40 days (Clark, unpublished), provide the first evidence for the extreme stenothermality of O. victoriae. Whilst this species can tolerate short-term heat shocks with a mean upper lethal temperature of 12°C (a single individual survived up to 15.2°C) (Peck et al. 2008b), they cannot acclimate to a temperature 10°C lower. However, these animals can cope for short periods at positive seawater temperatures in the wild. Seawater temperatures at 15 M around Rothera varied between −1.8 and +1.8°C between 1997 and 2006 (Fig. 1) with temperatures only briefly rising above +1°C in some summers (5 out of the 10 years). Summer water temperatures in the Rothera aquarium (January–March) do not generally reach above 1°C. In 2006, temperatures reached above 0°C for 10 days (not continual), reaching a maximum of +0.5°C for approximately 24 h (data not shown). In 2007 temperatures were continually above 0°C for 66 days (in excess of +0.5°C for 47 of those days), reaching a maximum of 1°C for two periods of 48 h and 5 days (data not shown). Thus, control animals in these experiments experienced periods of positive temperatures and appear capable of acclimating to +0.5°C without mortalities. Whilst in our experiments survival at 2°C was approximately double that of 3°C, mean survival was still just over a month. This is possibly the poorest acclimation ability of any species on record. Survival for this short time at such low temperatures is perhaps indicative of a critical threshold being crossed, the reasons behind which are currently unclear, but which proposed molecular studies are addressing. The fact that one individual in the +2°C assemblage survived almost twice as long as any other provides an indicator of the range of variability of response within this species to seawater warming. It indicates the importance of individual variation within a population and the contribution of functional biodiversity to species adaptation and survival in the face of environmental perturbation.
https://static-content.springer.com/image/art%3A10.1007%2Fs00300-008-0532-y/MediaObjects/300_2008_532_Fig1_HTML.gif
Fig. 1

Ten year time course series of annual seawater temperature fluctuations around Rothera Research Station at 15 M (SCUBA operation) depth. Data provided by Professor Andrew Clarke from the RaTS (Rothera Time course Series) Long-Term Monitoring Programme

This data contrasts strongly with recently published work on Antarctic fish acclimation, where animals survived at +4°C for periods in excess of 16 weeks (Gonzalez-Cabrera et al. 1995; Lowe and Davison 2005; Seebacher et al. 2005; Podrabsky and Somero 2006; Jin and DeVries 2006; Campbell unpublished) and the Antarctic sea star, O. validus at +6°C (Peck et al. 2008a), but matches that for scallops (Bailey et al. 2005) and the clam Laternula elliptica that could not acclimate to +3°C (S Morley, personal communication).

It is not yet possible to answer why Antarctic fish and some invertebrates are able to acclimate and brittle stars, scallops and clams cannot. One factor that could allow fish to survive higher acclimation temperatures would be an enhanced oxygen supply system. Their higher concentrations of blood oxygen pigment, and more efficient circulatory systems could be a key factor. Recent data (Peck et al. 2008b) has shown that in a cross-taxa review of upper lethal temperatures, more active animals survive longer than inactive ones, but the physiological mechanism behind this phenomenon has yet to be defined.

Acclimation trials are laboratory-based experiments and these are different to acclimatisation that occurs in the natural environment. However, the former is useful in predicting whether animals can acclimatise to a changing environment. Ecological data documents some Antarctic species living at their geographical extremes where temperature regimes are significantly wider than at higher Antarctic latitudes (+2°C above Antarctic Peninsula sea temperatures) and in the inter-tidal zones (Barnes et al. 2006; Waller et al. 2006). This indicates that some taxa can adapt to higher temperatures. The critical questions surround the rate of this adaptation and timescale required. Regional climate change along the Antarctic Peninsula has been rapid. Sea temperature along the west coast of the Antarctic Peninsula in the Bellingshausen’s Sea has risen 1°C in 50 years (Meredith and King 2005). Oceanic sea temperatures are predicted to rise 2°C over the next 100 years (Murphy and Mitchell 1995) which is a rate faster than anything seen over the past million years or on record over the last glacial cycles (Zachos et al. 2003). This rate of temperature increase is therefore intermediate between acclimation experiments and normal evolutionary timescales. More acclimation experiments (comprising different taxa and feeding guilds, plus over longer time periods) are needed to enable us to predict how Antarctic marine animals will survive regional climate change. The fact that some taxa survive at higher environmental temperatures should not engender complacency, as the evolutionary timescales over which this adaptation occurred are not the same as the rates at which climate change is increasing local seawater temperatures and several invertebrate taxa may be more sensitive to such temperature rises compared to the fish, significantly impacting on both biodiversity and the food web structure.

Acknowledgments

This paper was produced within the BAS Q4 BIOREACH/BIOFLAME core programmes. The authors would like to thank all members of the Rothera Dive Team for providing samples. Overall diving support was provided by the NERC National Facility for Scientific Diving at Oban.

Copyright information

© Springer-Verlag 2008