Effects of temperature on the embryonic cleavage rates and larval metabolism of Antarctic invertebrates

Abstract

Global climate change is set to disrupt global ecosystems with changes to both biotic and abioticenvironmental factors. The world’s oceans are warming at unprecedented rates, with temperature increases of between +1.4 °C and +4.4 °C expected by 2100. These increases in temperature particularly threaten the biota and ecosystems in the high Antarctic regions of Southern Ocean where temperatures have been cold (~ -1.8 °C) and thermally stable for over 30 million years. Warming temperatures can disrupt the biochemical reactions and physiological processes within an individual organism, with potential follow-on effects on populations and ecosystems. The organisms that inhabit the Southern Ocean are adapted to life within a very cold and narrow temperature range and are believed to have limited ability to cope with temperature stress. In this dissertation, I examine how temperature impacts early embryonic cleavage and metabolism, processes that are common to all metazoans. Our study subjects were four species of benthic Antarctic ectotherms, two pycnogonids (Nymphon australe and Ammothea glacialis), and two dendronotid nudibranchs (Tritoniella belli and Tritonia challengeriana). I first investigated the effects of temperature on the early cleavage phase. I found that for all four species, embryonic cleavage rate increased rapidly as temperature increased from -1.8 °C (ambient) to +3.5 °C. Consistent with other rate processes that have been measured in Antarctic marine ectotherms, the thermal sensitivity of cleavage rate was high. We also found that overall, thermal sensitivity was very high within the species’ natural temperature range (-1.8 to ~0 C), but cleavage rate was less affected by temperature increases above the natural temperature range. This suggests that organisms haven’t fully adapted to polar conditions potentially due to the limits of protein synthesis in extremely cold temperatures. Second, I investigated the effects of temperature on the metabolic rate (as estimated from oxygen consumption) of early, middle, and late larval stages from the same four species. I found that the thermal sensitivity of oxygen consumption was high for the majority of stages, with 8/12 exhibiting Q10 values higher than the 2-4 generally seen for most biological functions. Specific stages of development did not seem to affect thermal sensitivity. Lastly, I investigated the ability of larvae of one of the four species (Nymphon australe) to acclimate to temperature. In most Antarctic ectotherms tested to date, acclimation was completely absent or slow, requiring months to acclimate. I found that after 24 days at +1.0 °C, III larvae N. australe had lower overall oxygen consumption rates than those of larvae incubated at - 1.8 °C for the same period, a classic sign of thermal acclimation. This is the first time that acclimation has been shown in Antarctic invertebrate larvae. Signs of acclimation occurred in weeks as opposed to months shown by adults of Antarctic invertebrates. Larvae of N. australe may be able to optimize their metabolism to match environmental temperature fluctuations and predicted warming on an ecologically relevant time scale. Together, this work shows that the two essential processes of early cleavage and larval metabolism are thermally sensitive to small increases in temperature. However, if particularly sensitive stages, such as early larval stages, can acclimate to warming waters as shown here, Antarctic ectotherms may be more robust to warming than previously thought.