Demystifying Polar Gigantism: The Oxygen-Temperature Hypothesis

By Wang Jia Hua

Gigantism is a natural phenomenon which has long fascinated biologists, but its underlying mechanisms remain contentious and elusive. Examples of gigantism include insular gigantism and abyssal gigantism, in which certain island dwelling or deep-sea dwelling species are considerably greater in size than their mainland or shallow-water counterparts, respectively. Indeed, gigantism is present in most marine and terrestrial habitats and has been reported in even the most remote regions on Earth: the poles. As polar expeditions became more accessible, the recurring discoveries of unusually large taxa of marine ectotherms in the Arctic and Southern Ocean reflected a pattern systematic enough to become known as ‘polar gigantism’ (Woods & Moran, 2020). Perhaps the most remarkable example of these polar giants is the colossal squid (Mesonychoteuthis hamiltoni). Reaching weights of at least 495 kg, this Antarctic-endemic species is not only the largest of its taxonomic group by mass, but also the largest living invertebrate (Rosa et al., 2017). Similarly, polar gigantism has been recorded in many other taxa (e.g., molluscs, echinoderms, crustaceans) and within the fossil record (e.g., trilobites) (Gutiérrez-Marco et al., 2009). Notably, gigantism is a potentially powerful tool to uncover the physical, ecological, and evolutionary principles underpinning the evolution of body size—a central focus of evolutionary biology (Moran & Woods, 2012). Accordingly, the exploration of polar biodiversity and key drivers of polar gigantism is currently facilitated by growing international efforts such as the Census of Antarctic Marine Life and its polar counterpart, Arctic Ocean Diversity, which stem from the International Polar Year research effort. 

To begin, it is necessary to assign an appropriate definition to ‘polar gigantism’—and, by extension, gigantism in general. However, it is often tricky to decide upon a common metric (e.g., volume, length, body mass, dry weight) when specifying body size due to the sheer diversity of body plans adopted by marine species. For example, many suspension feeders may have dense protective shells or utilize external structures for feeding (e.g., silk/mucus nets), of which neither are metabolically active but nonetheless constitute a non-trivial proportion of their body size (Humphries, 2007). Evidently, (polar) gigantism is relative and should therefore be considered within the context of each taxonomic group. Some criteria for categorizing a species as giant hence require it to be at least twice the mean body size of its genus or have a body length within the top 5% of its taxon for a given habitat (Moran & Woods, 2012). Nevertheless, demonstrating polar gigantism via this comparative method is made particularly challenging due to a lack of detailed phylogenies and low taxon sampling. 

As organisms get larger, the reduced surface area to volume ratio typically results in inefficient oxygen uptake and increased oxygen transport distance, making it challenging to meet metabolic oxygen demands (Verberk & Atkinson, 2013). In other words, this results in an upper limit, or threshold, to body size above which diffusive oxygen supply cannot meet whole-body demand. Since body size is a key determinant of how organisms interact with their environments, understanding the unique conditions of polar oceans could offer a clue regarding the mechanisms driving, or simply permitting, polar gigantism. In particular, polar oceans are some of the coldest and most thermally stable environments on Earth, with annual variations of less than 1.5°C above the freezing point of water (−1.9°C) (Shishido et al., 2019). Correspondingly, most proposed mechanisms for polar gigantism are temperature-centered, with the oxygen-temperature hypothesis gaining the most traction over the recent years. Originally proposed by Chapelle and Peck, this hypothesis hinges on the interplay of cold-driven low metabolic rates and high (potential) oxygen availability in polar environments which allows breaching of the upper limits to body size (Chapelle & Peck, 1999). Recent studies, however, show that the bioavailability of oxygen is, in fact, lower in cold waters as the reduction in oxygen diffusivity outweighs the increase in its solubility at lower water temperatures (Verberk et al., 2011). Hence, a more refined explanation would that the freezing temperatures of polar oceans result in a high ratio of oxygen supply to demand, with a stronger influence on the latter (Woods & Moran, 2020). 

Regardless, polar giants form only a small proportion of Arctic and Antarctic marine fauna; some groups lack giants entirely or even tend towards high-latitude nanism (unusually small body size) (reviewed in Moran & Woods, 2012). Hence, the main effect of the oxygen-temperature hypothesis appears to simply increase the window of body sizes and is likely only pronounced in taxa and life history stages that are geometrically simple and/or lack developed ventilation mechanisms (Woods & Moran, 2020). Consequently, other (taxon-dependent) factors may be required to drive selection of large body sizes. For instance, the unique sea water chemistry of polar oceans can promote gigantism in certain groups but discriminate against others. Specifically, the upwelling of silica-rich deep water in the Southern Ocean may contribute to the large sizes of silica-incorporating organisms such as the giant Antarctic glass sponge (Anoxycalyx joubini) (Moran & Woods, 2012). Conversely, dissolution rates of calcium carbonate levels are much higher in cold polar waters due to acidification from increased CO2 solubility. This makes calcification energetically costly and may account for the various small calcifying species present (McClintock et al., 2009). Interestingly, as polar oceans are highly isolated and exhibit island-like characteristics, they may thus mirror certain aspects of insular gigantism such as the ecological release from historically large predators and competitors. The reduced predation pressure, due to the absence of durophagous (shell-crushing) predators particularly in the Southern Ocean, may allow certain lineages to grow larger than their tropical and sub-tropical counterparts (Moran & Woods, 2012). Finally, in addition to the release from physiological constraints, other mechanisms that have been proposed range hierarchically from biogeographic and ecological elements to life history tradeoffs and overarching evolutionary processes.

Currently, it is unclear whether this phenomenon of polar gigantism is due to the excessive, but understandable, attention paid to a few unusual outliers, or if it is due to actual systemic shifts in body sizes across latitude. As such, a strong comparative framework and better sampling of polar taxa are required to confirm the true strength of this pattern (Moran & Woods, 2012). Until then, unraveling the mystery of polar gigantism may remain challenging, but the current set of alternative yet non-exclusive mechanisms suggests that it is likely to be caused by a combination of both mutual and taxon-specific factors, of which temperature is a strong causal agent. In this view, understanding the biology of these giants will also have implications on monitoring the impact of climate change and ocean warming in polar communities. 

References:

Chapelle, G. & Peck, L. S. (1999) Polar gigantism dictated by oxygen availability. Nature. 399 (6732), 114-115. Available from: doi: 10.1038/20099.  

Gutiérrez-Marco, J. C., Sá, A. A., García-Bellido, D. C., Rábano, I. & Valério, M. (2009) Giant trilobites and trilobite clusters from the Ordovician of Portugal. Geology. 37 (5), 443-446. Available from: doi: 10.1130/G25513A.1. 

Humphries, S. (2007) Body size and suspension feeding. In: Hildrew, A. G., Raffaelli, D. G. & Edmonds-Brown, R. (eds.). Body Size: The Structure and Function of Aquatic Ecosystems. [e-book] Cambridge, Cambridge University Press. pp. 16-32. 

McClintock, J. B., Angus, R. A., Mcdonald, M. R., Amsler, C. D., Catledge, S. A. & Vohra, Y. K. (2009) Rapid dissolution of shells of weakly calcified Antarctic benthic macroorganisms indicates high vulnerability to ocean acidification. Antarctic Science. 21 (5), 449-456. Available from: doi: 10.1017/S0954102009990198. 

Moran, A. L. & Woods, H. A. (2012) Why might they be giants? Towards an understanding of polar gigantism. The Journal of Experimental Biology. 215 (12), 1995. Available from: doi: 10.1242/jeb.067066. 

Rosa, R., Lopes, V. M., Guerreiro, M., Bolstad, K. & Xavier, J. C. (2017) Biology and ecology of the world’s largest invertebrate, the colossal squid (Mesonychoteuthis hamiltoni): a short review. Polar Biology. 40 (9), 1871-1883. Available from: https://doi.org/10.1007/s00300-017-2104-5. 

Shishido, C. M., Woods, H. A., Lane, S. J., Toh, M. W. A., Tobalske, B. W. & Moran, A. L. (2019) Polar gigantism and the oxygen–temperature hypothesis: a test of upper thermal limits to body size in Antarctic pycnogonids. Proceedings of the Royal Society B: Biological Sciences. 286 (1900), 20190124. Available from: doi: 10.1098/rspb.2019.0124. 

Verberk, W. C. E. P. & Atkinson, D. (2013) Why polar gigantism and Palaeozoic gigantism are not equivalent: effects of oxygen and temperature on the body size of ectotherms. Functional Ecology. 27 (6), 1275-1285. Available from: https://doi.org/10.1111/1365-2435.12152. 

Verberk, W. C. E. P., Bilton, D. T., Calosi, P. & Spicer, J. I. (2011) Oxygen supply in aquatic ectotherms: Partial pressure and solubility together explain biodiversity and size patterns. Ecology. 92 (8), 1565-1572. Available from: doi: https://doi.org/10.1890/10-2369.1. 

Woods, H. A. & Moran, A. L. (2020) Reconsidering the Oxygen–Temperature Hypothesis of Polar Gigantism: Successes, Failures, and Nuance. Integrative and Comparative Biology. 60 (6), 1438-1453. Available from: https://doi.org/10.1093/icb/icaa088.

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out /  Change )

Google photo

You are commenting using your Google account. Log Out /  Change )

Twitter picture

You are commenting using your Twitter account. Log Out /  Change )

Facebook photo

You are commenting using your Facebook account. Log Out /  Change )

Connecting to %s