Tuesday, June 14, 2016

The Sinuous Salamanderfish, by Derek Wheaton

-->A bit of an enigma in the fish world, the Salamanderfish (Lepidogalaxias salamandroides Mees 1961) is a small fish (up to about 70mm in length) endemic to the coastal scrub and peat flats of southwestern Australia(Pusey 1990). What may initially appear to most as a small, brown, boring little fish is actually incredibly remarkable for a variety of reasons, once a bit more is understood. The most obviously strange thing about this fish, which happens to be the driver for all its other unusual traits, is the fish’s habitat. This fish is found exclusively in small temporary pools that dry up in the middle of summer(Berra and Allen 1989). Indeed, for those of us familiar with the ecology of “vernal pools” here in the US, these water bodies are unique and valuable for having a lack of fish that allows various other creatures to utilize them. This is not so in Australia, where the Salamanderfish thrives in a seemingly impossible habitat through the benefits of its very strange adaptations. The ability to burrow to survive dry spells, breathe through its skin, perform internal fertilization, and several bone modifications are a bit like fishy superpowers, allowing this strange fish to thrive in a hostile world. 
Salamanderfish Lepidogalaxias salamandroides (Mees 1961) Photo by Gerry Allen
-Burrowing & Aestivation
In order to utilize a habitat that dries out, a fish must have a way of getting through this hostile period until wetter times arrive. This ability is not unheard of in the fish world: some killifish, for instance, lay eggs that can survive (and may even require) a period of dormancy in dry conditions. Others, like the large familiar lungfishes, burrow into the ground and aestivate. The Salamanderfish falls into this second category. These remarkable little fish move below the surface of the sand and leaf litter in search of substrate hydrated by ground water, and, remarkable for a fish of this size, they have been recovered up to 60cm (about 2 feet) below the surface! Interestingly they are incredibly quick to re-emerge, and when their habitat was experimentally rehydrated with water from a fire truck, fish were captured as little as 8 minutes later (Berra and Allen 1989). The ability to survive dry periods and rapidly resume normal activity is of huge benefit to a fish that inhabits such a seasonally hostile environment.  
Salamanderfish in process of burrowing.   Photo by Auscape.
 -Cutaneous respiration
Another incredible adaptation, related to aestivation but significant enough to mention separately, is the ability of this species to perform cutaneous respiration. In what must have been a delicate task, researchers separated the head and gill structures from the rest of the body by putting a “collar” around the fish and measured oxygen and CO2 levels while the fish was out of water. They were able to determine that L. salamandroides is capable of considerable gas exchange through the skin. Surprisingly, however, they also determined that when out of water, this fish does not produce extra mucous or have any other apparent mechanism to prevent dessication, so while they can breathe out of water, they must stay moist in order to survive any prolonged period on land or in the substrate (Martin et al. 1993). Another interesting aspect of this is that, unlike many other aestivating fish species, the Salamanderfish does not have the ability to survive hypoxic water conditions (Berra & Allen, 1995) and has no accessory breathing apparatus in the swim bladder or gills (Berra et al. 1989). The reason for this may be because the typical habitat of this fish is physically predisposed to gas exchange, being relatively shallow pools of water with relatively large surface area. Except under the influence of extreme amounts of microbial oxygen usage, water in this situation would likely contain plenty of dissolved oxygen by default. One possible benefit of cutaneous respiration when the fish is not able to maintain water balance, may be forays above the waterline to forage on insects. This has not yet been studied in this species, but it is within the realm of possibility, as the Mangrove Killifish (Kryptolebias marmoratus Poey 1880), a small estuarine species of similar habitat and ability, has been shown to actively feed above the waterline (Pronko et al. 2013).
-Internal fertilization
Back in the water, in good conditions at the appropriate time of year, it’s time for the Salamanderfish to breed. In yet another plot twist, this fish defies the odds yet again by practicing internal fertilization. Lepidogalaxias salamandroides males possess a modified anal fin with a scaly sheath that serves as an intromittent organ, while females have ciliated ducts connecting to the ovaries and are capable of storing sperm. Strangely, there has not been observed to be any courtship display, but instead the male approaches a female and rolls her so he can position his anal fin and scaly sheath adjacent to her vent. The scaly sheath structure apparently secretes a kind of adhesive mucous that connects the mating pair (with a researcher even noting that when lifted from the water they remained attached!)(Pusey and Stewart 1989). The function or history of internal fertilization can only be theorized at this point. This species has undergone dramatic changes in taxonomic placement, most recently being placed in the basal position of euteleosts (Li et al. 2010), and therefore it is difficult to make connections to where this may have arose in the evolution of this species. Its mode of fertilization is quite unlike any other teleost (Pusey and Stewart 1989), making it difficult to ascertain the origin. It has been theorized that internal fertilization evolved as a response to the often highly acidic conditions in which this species lives, which is a hostile environment for sperm, or that this (and the mucous adhesion which subsequently serves to form a “plug”) arose as a result of sperm competition (Pusey and Stewart 1989). This subject requires additional study to elucidate the evolutionary details of this process.
-Bone and skull adaptations – neck bending
 When one first observes the Salamanderfish, most of these interesting facets are not readily apparent. One thing that does, however, immediately grasp the attention is this fish’s amazing (in the fish world) ability to turn its head. This fish is capable of moving its skull directionally both side-to-side and up-and-down as much as 90 degrees (Berra and Allen 1989). This is possible because the distance between the back of the skull and the cervical vertebrae is relatively large, allowing an enhanced degree of flexibility. Besides this increased flexibility potentially aiding in the ability to burrow, this fish lacks typical musculature surrounding the eye, preventing the Salamanderfish from moving the eye within its socket (Mcdowall and Pusey 1983). Thus, the ability to bend the neck may be of crucial importance during foraging and feeding, allowing the fish to lie nearly motionless on the bottom while scanning the environment for prey. Despite being such a small fish, L. salamandroides has a formidable array of teeth, which may assure the consumption of any prey captured by the fish. The reinforced, wedge-shaped skull and largely reduced ribs may be adaptations that additionally enhance burrowing by decreasing drag and increasing flexibility, aiding in travel through the substrate (Berra and Allen 1989)For a demonstration of the neck-bending ability of this fish, see video.
Neck bending Salamanderfish.  Photo by Tim Berra
With a huge variety of specialized adaptations, the Salamanderfish (Lepidogalaxias salamandroides Mees 1961) is a truly fascinating example of a fish living where a fish shouldn’t really be. A curious suite of characters have led this species to drive taxonomists crazy, with its placement on the evolutionary tree changing often since its discovery as ichthyologists struggle to determine where it belongs. This animal has proven intensely fascinating some researchers who continue to unravel the mysteries of its uniqueness. In the meantime, while we are struggling to understand it, the Salamanderfish will continue to eke out a living in one of the most hostile environments known to fish-kind.
Berra, T., and G. Allen. 1989. Burrowing, emergence, behavior, and functional morphology of the Australian salamanderfish, Lepidogalaxias salamandroides. Fisheries 2415(May 2014):37–41.
Berra, T. M., D. M. Sever, and G. R. Allen. 1989. Gross and Histological Morphology of the Swimbladder and Lack of Accessory Respiratory Structures in Lepidogalaxias salamandroides , an Aestivating Fish from Western Australia.  Copeia  1989(4):850–856.
Li, J., R. Xia, R. M. McDowall, J. A. Lopez, G. Lei, and C. Fu. 2010. Phylogenetic position of the enigmatic Lepidogalaxias salamandroides with comment on the orders of lower euteleostean fishes. Molecular Phylogenetics and Evolution 57(2):932–936.
Martin, A. K. L. M., T. M. Berra, and G. R. Allen. 1993. Cutaneous Aerial Respiration during Forced Emergence in the Australian Salamanderfish, Lepidogalaxias salamandroides. Copeia 1993(3):875–879.
Mcdowall, R. M., and B. J. Pusey. 1983. Lepidogalaxias Salamandroides Mees – a Redescription, With Natural History Notes. Records of the Western Australian Museum 11(1):11.
Pronko, A. J., B. M. Perlman, and M. a Ashley-Ross. 2013. Launches, squiggles and pounces, oh my! The water-land transition in mangrove rivulus (Kryptolebias marmoratus). The Journal of Experimental Biology 216(Pt 21):3988–95.
Pusey, B. J. 1990. Seasonality, aestivation and the life history of the salamanderfish Lepidogalaxias salamandroides (Pisces: Lepidogalaxiidae). Environmental Biology of Fishes 29(1):15–26.
Pusey, B. J., and T. Stewart. 1989. Internal fertilization in Lepidogalaxias salamandroides mees (Pisces: Lepidogalaxiidae). Zoological Journal of the Linnean Society 97(1):69–79.

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