Antarctic sea spiders: polar or abyssal gigantism?

It is well known that in certain situations, some species evolve to be unusually large members of their taxonomic groups - the phenomenon of gigantism. Two such situations are polar and abyssal (deep-sea) gigantism, but why do large species evolve in polar and/or deep sea waters? As we will see, the answers are not always straighforward and are not necessarily the same for both situations. To illustrate this, I want to look at sea-spiders - not actually spiders but marine arthropods in the class Pycnogonida. A brief but informative introduction to this group can be found here, but in summary they are mostly free-living and are found at all latitudes and ocean depths. Superficially resembling spiders (though their taxonomic link to other groups is unclear), they have a cephalon (head) and a 4- (sometimes 5- or 6-) segmented body, each segment with a pair of walking legs (the rear segment bears a small abdomen), while the cephalon has various feeding appendages and palps, plus in males a pair of ovigers (leg-like appendages primarily used for carrying eggs & caring for young, but also for cleaning and courtship) which are found only in the Pycnogonida. Males also have 'cement glands' which they use to form eggs into round masses that are carried on the ovigers (Barnes 1980). Their biology is poorly studied - see Arnaud & Bamber (1987) for a useful review - but they reproduce by hatching as larvae or post-larvae with some being dispersed by medusae (jellyfish) and appear to feed on sessile animal prey or algae. Having such small bodies, their guts extend into their legs and in females, eggs are carried inside the femora. Around Britain, one common sea-spider is Pycnogonum littorale, a temperate shallow-water species (distribution given here) with a body around 5mm long and hence a leg-span of around 20mm.

A display of Pycnogonum littorale at the OUMNH

In contrast, polar and/or deep-water species may have leg-spans up to 750mm, especially in the family Colossendeidae.

Colossendeis wilsoni, A large Antarctic sea-spider also in the OUMNH collection. For scale, the label font is the same size as in the photo of P. littorale above.

So, why this gigantism in polar and abyssal marine environments? As noted in the excellent Deep Sea News, it is unclear whether the cause is the same in both cases, and the two tend to be confused in scientific reporting by the media. Also, although giant sea-spiders are familiar examples of Antarctic gigantism, many are found in deep water and therefore a species may be subject to the processes of adaptation to both polar and abyssal conditions, making it difficult to separate the two effects. For example, specimens of C. wilsoni (photo above) in the Smithsonian Museum were found at depths between 36m and 801m, while the most common Antarctic species in this genus, C. megalonyx, has been found between 3m and 4,900m (Wu & Mastro 2004)! Hence, it is not clear whether gigantism in this species is polar or polar-and-abyssal.

A widely cited paper by Chapelle & Peck (1999), found that the maximum size of amphipods (shrimp-like crustaceans) was related to dissolved oxygen rather than temperature or salinity, with polar waters being high in dissolved oxygen, because water can hold more oxygen at low temperatures. Similar effects in bivalve molluscs have also been found (e.g. Pörtner et al. 2006). The reasoning behind this 'oxygen hypothesis' is that as the size of an organism increases, its surface area:volume ratio reduces. This means that larger animals have more tissue volume requiring oxygen, but relatively less surface area with which to sequester it from the surrounding water. In warmer waters, not only is their less dissolved oxygen, but the oxygen needs of animal tissues is higher. Thus polar gigantism occurs due to cold water temperatures and high levels of dissolved oxygen. However, more recent research involving the self-righting abilities of 12 different-sized species of sea-spider (Woods et al. 2008) did not fully support the oxygen hypothesis, although it did agree that oxygen availability was likely to be one important factor, just not the only one. A possible explanation is that, being an apparently early branch of sea-spider evolution (Arango & Wheeler 2007), Colossendeis species have been adapting to cold, well-oxygenated waters for a longer period that other genera and have oxygen delivery systems which are more finely tuned to such conditions. If this is the case, then climate change is a potentially serious threat to a specialist groups of species functioning with narrow oxygen safety margins i.e. warmer waters leading to higher oxygen demand and lower availability could push Colossendeis beyond these margins more quickly than it can adapt.

So, although it seems that polar gigantism is a result of oxygen availability plus other factors, abyssal gigantism is in some ways more mysterious. Firstly, as noted by Deep Sea News, much work has looked at deep sea dwarfism rather than gigantism because so many taxa show this reduction in size, suggesting that the deep ocean is primarily a small-organism habitat (McClain et al. 2005, Kaariainen & Bett 2010). Thus, the incidence of abyssal gigantism (seen particularly in crustaceans, but also a range of other taxa) contrasts strongly with what appears to be the 'normal' situation in the deep ocean.

Abyssal dwarfism has generally been attributed to low food availability, with most animal communities (away from seeps and vents) relying on the 'marine snow' of detritus sinking from the surface, with occasional larger localised inputs such as dead whales. Thus little food arrives, especially away from productive shallow coastal waters. However, several possible explanations for the rarer gigantism have been proposed e.g.:

• Higher oxygen availability (Chapelle & Peck 2001) as the amount of available oxygen determines the amount of sustainable tissue, with cell size and number both increasing with higher oxygen concentration in Drosophila fruit flies (Frazier et al. 2001) and freshwater amphipods (Peck & Chapelle 2003). In gastropods, a link between larger size and more oxygenated deep-sea sites has been noted (McClain & Rex 2001), but giant isopods Bathynomus sp. are known from low-oxygen regions in the Gulf of Mexico.
• Longer lifespans due to reduced predation (few predators) and slower growth rates in cold water with larger cell size in crustaceans (Timofeev 2001) with a similar process suggested for other taxa (e.g. Van Voorhies 1996).

However, although key effects such as the link between oxygen levels and cell size/number have been described, these are the result of work on unrelated taxa and it remains unclear precisely why Colossendeis sea-spiders (let alone giant isopods) should exhibit gigantism while others do not - and so it is tie for a little (hopefully not too idle) speculation:

• Through development of fat reserves, larger size may allow longer gaps in feeding when food is scarce (although sea-spiders do not appear to have much space for such storage) or larger foraging areas. 
• It may be that gigantism is linked to the species' evolutionary past as island biotas also show a mixture of dwarfism and gigantism related to the size of their mainland ancestors (e.g. Lomolino 2005). Could Colossendeis (or Bathynomus) be descendents of larger ancestors from warmer and/or shallower waters and thus display gigantism rather than dwarfism when adapted to polar/abyssal conditions? 
• Is their large size actually adaptive or is it simply a random evolutionary trait which happens to serve them as well as dwarfism might? 
• With many abyssal species tending towards dwarfism, might it provide a form of niche-separation and thus reduce competition?
• Does large size itself reduce predation?
• Might large size (through the ability to exploit a large food patch or larger food items) reduce the need to move and thus expend energy? Would this be a successful trade-off against the need for more energy/food to maintain a larger body size?
• With the smaller surface area: volume ratio, larger bodies can mean easier temperature regulation, but would this be sufficiently adaptive and if so, why in only a few species?
• With some hydrothermal vent and seep species such as vestimentiferan tubeworms showing great longevity (e.g. Fisher et al. 1997), and gigantism being at least partly associated with slow growth over a long period in a stable, if food-scarce environment, might gigantism be linked to an adaptive function of increased individual longevity in areas away from vents and seeps?

I suspect I could go on, but that is enough speculation for now. As always, comments and suggestions are most welcome -  this is an area of ongoing research where the processes involved are, in part, poorly understood, so this may require an update at some point in the not-too-distant future. And the answer to the original question - polar or abyssal gigantism? Well, it seems likely that both are involved and linked to some extent by the influence of oxygen availability, but the relative 'weight' of each type of gigantism can not currently be determined for certain. However, my feeling is that, for Colossendeis at least, the fact that a single species can be found anywhere from the sea surface to depths of thousands of metres suggests that it is the polar aspect that is constant and having a greater effect. Could be wrong though!


Further reading

For a key to coastal British species: King, P.E. (1986). Sea Spiders. A revised key to the adults of littoral Pycnogonida in the British Isles. Field Studies 6(3): 493-516.

References

Arango, C.P. & Wheeler, W.C. (2007). Phylogeny of the sea spiders (Arthropoda, Pycnogonida) based on direct optimization of six loci and morphology. Cladistics 23: 255–293. Arnaud, F. & Bamber, R.N. (1987). The Biology of Pycnogonida. Advances in Marine Biology 24: 1-96.
Bamber, R.N. & El Nagar, A. (eds.) (2012). Pycnobase: World Pycnogonida Database. [accessed 09/02/2012]
Barnes, R.D. (1980). Invertebrate Zoology (4th ed.). Holt-Saunders, Philadelphia.
Chapelle, G., & Peck L.S. (1999). Polar gigantism dictated by oxygen availability. Nature 399: 114-115.
Fisher, C.R., Urcuyo, I.A., Simpkins, M.A. & Nix, E. (1997). Life in the slow lane: growth and longevity of cold-seep vestimentiferans. Marine Ecology 18(1): 83-94.Frazier, M. R., Woods, H. A. & Harrison, J. F. (2001). Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster. Physiological and Biochemical Zoology 74: 641-650.
Kaariainen, J. & Bett, B. (2010). Evidence for benthic body size miniaturization in the deep sea. Journal of the Marine Biological Association of the UK. 86(6): 1339-1345.
Lomolino, M.V. (2005). Body size evolution in insular vertebrates: generality of the island rule. Journal of Biogeography 32(10): 1683-1699.
McClain, C.R & Rex, M.A. (2001). The relationship between dissolved oxygen concentration and maximum size in deep-sea turrid gastropods: an application of quantile regression. Marine Biology 139: 681-685.
McClain, C.R., Rex, M.A. & Jabbour, R. (2005). Deconstructing bathymetric body size patterns in deep-sea gastropods. Marine Ecology Progress Series 297: 181-187.
Peck, L.S. & Chapelle, G. (2003). Reduced oxygen at high altitude limits maximum size. Proceedings of the Royal Society of London B (Suppl.) 270: S166-167.
Pörtner, H.O., Peck, L.S. & Hirse, T. (2006). Hyperoxia alleviates thermal stress in the Antarctic bivalve, Laternula elliptica: evidence for oxygen limited thermal tolerance. Polar Biology 29: 688-693.

Timofeev, S.F. (2001). Bergmann's Principle and deep-water gigantism in marine crustaceans. Biology Bulletin 28(6): 646-650.

Van Voorhies, W.A. (1996). Bergmann size clines: a simple explanation for their occurrence in ectotherms. Evolution 50: 1259-1264.

Woods, H. A., Moran, A. L., Arango, C. P., Mullen, L. & Shields, C. (2008). Oxygen hypothesis of polar
gigantism not supported by performance of Antarctic pycnogonids in hypoxia. Proceedings of the Royal Society B 276: 1069-1075.
Wu, N. & Mastro, J. (2004). Under Antarctic Ice. University of California, Berkeley CA.