Biphasic burrowing in Atlantic hagfish (Myxine limosa).

Myxine limosa is a burrowing species of hagfish that occurs in the western North Atlantic in areas with muddy substrate and at depths generally greater than 100 meters. Burrowing of M. limosa has been observed from submersibles, but little is known about the behavior of these animals within the substrate or the biomechanical mechanisms involved. Here, we investigated burrowing in M. limosa by observing individuals as they burrowed through transparent gelatin. A photoelastic setup using crossed polarizers allowed us to visualize stress development in the gelatin as the hagfish moved through it. We found that M. limosa created U-shaped burrows in gelatin using a stereotyped, two-phase burrowing behavior. In the first ('thrash') phase, hagfish drove their head and their anterior body into the substrate using vigorous sinusoidal swimming movements, with their head moving side-to-side. In the second ('wriggle') phase, swimming movements ceased, with propulsion coming exclusively from the anterior, submerged portion of body. The wriggle phase involved side-to-side head movements and movements of the submerged part of the body that resembled the internal concertina strategy used by caecilians and uropeltid snakes. The entire burrowing process took on average 7.6 min to complete and ended with the hagfish's head protruding from the substrate and the rest of its body generally concealed. Understanding the burrowing activities of hagfishes could lead to improved understanding of sediment turnover in marine benthic habitats, new insights into the reproductive behavior of hagfishes, or even inspiration for the design of burrowing robots.

Terrestrial capabilities of invasive fishes and their management implications.

Amphibious fishes have many adaptations that make them successful in a wide variety of conditions, including air-breathing, terrestrial locomotor capabilities, and extreme tolerance of poor water quality. However, the traits that make them highly adaptable may allow these fishes to successfully establish themselves outside of their native regions. In particular, the terrestrial capabilities of invasive amphibious fishes allow them to disperse overland, unlike fully aquatic invasive fishes, making their management more complicated. Despite numerous amphibious fish introductions around the world, ecological risk assessments and management plans often fail to adequately account for their terrestrial behaviors. In this review, I discuss the diversity of invasive amphibious fishes and what we currently know about why they emerge onto land, how they move around terrestrial environments, and how they orient while on land. In doing so, I use case studies of the performance and motivations of nonnative amphibious fishes in terrestrial environments to propose management solutions that factor in their complete natural history. Because of their terrestrial capabilities, we may need to manage amphibious fishes more like amphibians than fully aquatic fishes, but to do so, we need to learn more about how these species perform in a wide range of terrestrial environments and conditions.

From reductionism to synthesis: The case of hagfish slime.

Reductionist strategies aim to understand the mechanisms of complex systems by studying individual parts and their interactions. In this review, we discuss how reductionist approaches have shed light on the structure, function, and production of a complex biomaterial - hagfish defensive slime. Hagfish slime is an extremely dilute hydrogel-like material composed of seawater, mucus, and silk-like proteins that can deploy rapidly. Despite being composed almost entirely of water, hagfish slime has remarkable physical properties, including high strength and toughness. While hagfish slime has a promising future in biomimetics, including the development of eco-friendly high-performance fibers, recreating hagfish slime in the lab has been a difficult challenge. Over the past two decades, reductionist experiments have provided a wealth of information about the individual components of hagfish slime. However, a reductionist approach provides a limited understanding because hagfish defensive slime, like most biological phenomena, is more than just the sum of its parts. We end by providing some thoughts about how the knowledge generated in the last few decades might be synthesized into a working model that can explain hagfish slime structure and function.

Why did the invasive walking catfish cross the road? Terrestrial chemoreception described for the first time in a fish.

Clarias batrachus (walking catfish) is an invasive species in Florida, renowned for its air-breathing and terrestrial locomotor capabilities. However, it is unknown how this species orients in terrestrial environments. Furthermore, while anecdotal life history information is widespread for this species in its nonnative range, little of this information exists in the literature. The goals of this study were to identify sensory modalities that C. batrachus use to orient on land, and to describe the natural history of this species in its nonnative range. Fish (n = 150) were collected from around Ruskin, FL, and housed in a greenhouse, where experiments took place. Individual catfish were placed in the center of a terrestrial arena and were exposed to nine treatments: two controls, L-alanine, quinine, allyl isothiocynate, sucrose, volatile hydrogen sulphide, pond water and aluminium foil. These fish exhibited significantly positive chemotaxis toward alanine and pond water, and negative chemotaxis away from volatile hydrogen sulphide, suggesting chemoreception - both through direct contact and through the air - is important to their terrestrial orientation. Additionally, 88 people from Florida wildlife-related Facebook groups who have personal observations of C. batrachus on land were interviewed for information regarding their terrestrial natural history. These data were combined with observations from 38 YouTube videos. C. batrachus appear to emerge most frequently during or just after heavy summer rains, particularly from stormwater drains in urban areas, where they may feed on terrestrial invertebrates. By better understanding the full life history of C. batrachus, we can improve management of this species.

Evolutionary optimization of an anatomical suction cup: Lip collagen content and its correlation with flow and substrate in Neotropical suckermouth catfishes (Loricarioidei).

In riverine ecosystems, downstream drag caused by fast-flowing water poses a significant challenge to rheophilic organisms. In neotropical rivers, many members of a diverse radiation of suckermouth catfishes (Loricarioidei) resist drag in part by using modified lips that form an oral suction cup composed of thick flesh. Histological composition and morphology of this cup are interspecifically highly variable. Through an examination of 23 loricarioid species, we determined that the tissue most responsible for lip fleshiness is collagen. We hypothesized that lip collagen content is interspecifically correlated with substrate and flow so that fishes living on rocky substrates in high-flow environments have the largest, most collagenous lips. By mapping the amount and distribution of lip collagen onto a phylogeny and conducting ANOVA tests, we found support for this hypothesis. Moreover, these traits evolved multiple times in correlation with substrate and flow, suggesting they are an effective means for improving suction-based attachment. We hypothesize that collagen functions to reinforce oral suction cups, reducing the likelihood of slipping, buckling, and failure under high-flow, high-drag conditions. Macroevolutionary patterns among loricarioid catfishes suggest that for maximum performance, biomimetic suction cups should vary in material density according to drag and substrate requirements.

Where do fish go when stranded on land? Terrestrial orientation of the mangrove rivulus Kryptolebias marmoratus.

The goal of the present study was to determine which sensory cues the mangrove rivulus Kryptolebias marmoratus, a quasi-amphibious, hermaphroditic fish, uses to orient in an unfamiliar terrestrial environment. In a laboratory setting, K. marmoratus were placed on a terrestrial test arena and were provided the opportunity to move toward reflective surfaces, water, dark colours v. light colours, and orange colouration. Compared with hermaphrodites, males moved more often toward an orange section of the test arena, suggesting that the response may be associated with camouflage or male-male competition, since only males display orange colouration. Younger individuals also moved more often toward the orange quadrant than older individuals, suggesting age-dependent orientation performance or behaviour. Sloped terrain also had a significant effect on orientation, with more movement downhill, suggesting the importance of the otolith-vestibular system in terrestrial orientation of K. marmoratus. By understanding the orientation of extant amphibious fishes, we may be able to infer how sensory biology and behaviour might have evolved to facilitate invasion of land by amphibious vertebrates millions of years ago.

A walking behavior generates functional overland movements in the tidepool sculpin, Oligocottus maculosus.

Tidepool sculpins (Oligocottus maculosus) have been observed moving overland in the rocky intertidal, and we documented the terrestrial walking behavior that they use to accomplish this. We quantified the terrestrial movements of O. maculosus and compared them to (1) their aquatic locomotion, (2) terrestrial locomotion of closely-related subtidal species (Leptocottus armatus and Icelinus borealis), and (3) terrestrial movements of walking catfishes (Clarias spp.). We recorded sculpin movements (210 fps) on a terrestrial platform and in a water tank and tracked body landmarks for kinematic analysis. The axial-appendage-based terrestrial locomotion of O. maculosus is driven by cyclic lateral oscillations of the tail, synchronized with alternating rotations about the base of the pectoral fins, a behavior that appears similar to a military "army crawl." The pectoral fins do not provide propulsion, but act as stable points for the body to rotate around. In contrast, individuals of O. maculosus use primarily axial undulation during slow-speed swimming. The army crawl is a more effective terrestrial behavior (greater distance ratio) than the movements produced by L. armatus and I. borealis, which use rapid, cyclic oscillations of the tail, without coordinated pectoral fin movements. Relative to Clarias spp., O. maculosus rotated the body about the base of the pectoral fin, rather than the tip of the fin, which may cause O. maculosus to have a lower distance ratio. Since O. maculosus lack major morphological adaptations for terrestrial locomotion, instead relying on behavioral adaptations, we propose behavioral adaptations may evolutionarily predate morphological adaptations for terrestrial locomotion in vertebrates.

Look before you leap: Visual navigation and terrestrial locomotion of the intertidal killifish Fundulus heteroclitus.

Mummichogs (Fundulus heteroclitus; Cyprinodontiformes) are intertidal killifish that can breathe air and locomote on land. Our goals were to characterize the terrestrial locomotion of mummichogs and determine their method of navigation towards water in a terrestrial environment. We used high-speed video to record behavior during stranding experiments and found that mummichogs use a tail-flip jump to move overland, similarly to other Cyprinodontiformes. However, mummichogs also prop themselves upright into a prone position between each jump, a previously undescribed behavior. After becoming prone, mummichogs rotate about their vertical axis, directing the caudal fin towards the water. Then, they roll back onto their lateral aspect and use a tail-flip behavior to leap into a caudally-directed, ballistic flight path. We conducted experiments to determine the sensory stimulus used to locate a body of water by placing mummichogs on a square platform with one side adjacent to a sea table. Under artificial light, mummichogs moved towards the sea table with a higher frequency than towards the other sides. Under dark conditions, mummichogs did not show a preference for moving towards the sea table. When the surface of the water was covered with reflective foil, mummichogs moved towards it as if it were a body of water. These results suggest that mummichogs primarily use visual cues, specifically reflected light, to orient towards the water. The uprighting behavior that mummichogs perform between terrestrial jumps may provide an opportunity for these fish to receive visual information that allows them to safely return to the water. J. Exp. Zool. 325A:57-64, 2016. © 2015 Wiley Periodicals, Inc.