Larval and thermal ecology of Antarctic marine invertebrates: It's pretty cool

Abstract

The Southern Ocean surrounding Antarctica is one of the coldest and most thermally stable marine environments on the planet and hosts a diverse and highly endemic array of life. Cold-blooded organisms that have evolved in these waters share traits such as high temperature sensitivity, slow pace of growth and development, large eggs, and prevalence of brooding. Little is known about the reproductive ecology of one of its inhabitants, the Antarctic pycnogonid, or sea spider. We investigated patterns of organic mass loss during early development in two species of brooding sea spiders (Ammothea glacialis and Nymphon australe) and found that development is largely fueled by yolk reserves, though later larval stages in N. australe may supplement nutrition through exogenous feeding while brooded. Due to climate change, the Antarctic has become one of the fastest-warming regions on Earth, and the stenothermal organisms that inhabit the Southern Ocean are now faced with developmental and physiological challenges caused by rising temperatures. We examined the effects of small increases in temperature (-1.8, -0.4, +1 and +4 °C) on survival, energetic content, and developmental timing of the embryos and larvae of the same two species of sea spider as above, and two additional species of nudibranch (Tritoniella belli and Tritonia challengeriana). We found that, while sea spiders exhibited minimal mortality across treatments, nudibranch survival declined sharply at higher temperatures. Energetic content of embryos and larvae was generally lower with warming, attributed to lower protein reserves, and developmental length was shortened at higher temperatures. The estimated cost of development was lowest at 0.4 °C or +1 °C for most species, suggesting that current ambient temperatures (-1.8 °C) may be suboptimal for energetic efficiency of embryonic or larval development, and that future warming beyond +1°C could lead to metamorphosis with lower energetic reserves. Climate change is also predicted to increase both the frequency and intensity of marine heatwaves in the Southern Ocean, where a severe event in 2022 saw temperature fluctuations of nearly 2°C in a single week. We tested the ability of adult Antarctic snails (Neobuccinum eatoni) to acclimate to short-term warming, using noninvasive infrared heart rate sensors. Following a two-week exposure to 4°C, snails exhibited increased cardiac performance at warmer temperatures, demonstrating physiological plasticity on a shorter timescale than previously recorded in other Antarctic taxa. Together, these findings suggest that Antarctic marine invertebrates may exhibit resilience to moderate warming up to +1°C, but higher temperatures could reduce energetic efficiency of early development, with potential implications for juvenile survival and ecosystem stability under future climate scenarios.