Ice in the intertidal: patterns and processes of freeze tolerance in intertidal invertebrates

Many intertidal invertebrates are freeze tolerant, meaning that they can survive ice formation within their body cavity. Freeze tolerance is a fascinating trait, and understanding its mechanisms is important for predicting the survival of intertidal animals during extreme cold weather events. In this Review, we bring together current research on the ecology, biochemistry and physiology of this group of freeze-tolerant organisms. We first introduce the ecology of the intertidal zone, then highlight the strong geographic and taxonomic biases within the current body of literature on this topic. Next, we detail current knowledge on the mechanisms of freeze tolerance used by intertidal invertebrates. Although the mechanisms of freeze tolerance in terrestrial arthropods have been well-explored, marine invertebrate freeze tolerance is less well understood and does not appear to work similarly because of the osmotic differences that come with living in seawater. Freeze tolerance mechanisms thought to be utilized by intertidal invertebrates include: (1) low molecular weight cryoprotectants, such as compatible osmolytes and anaerobic by-products; (2) high molecular weight cryoprotectants, such as ice-binding proteins; as well as (3) other molecular mechanisms involving heat shock proteins and aquaporins. Lastly, we describe untested hypotheses, methods and approaches that researchers can use to fill current knowledge gaps. Understanding the mechanisms and consequences of freeze tolerance in the intertidal zone has many important ecological implications, but also provides an opportunity to broaden our understanding of the mechanisms of freeze tolerance more generally.