Surviving the flood: plastron respiration in the non-tracheate arthropod Phrynus marginemaculatus (Amblypygi: Arachnida)
Introduction
In climates with heavy rainfall and consequent flooding, the ability of terrestrial arthropods to survive submersion for extended periods of time is a critical element of survival. Many insects survive in habitats subject to inundation through the possession of various behaviors and structures that enable them to respire underwater. Among the physical structures permitting survival underwater, plastron respiration has evolved independently a number of times among the eggs, larvae, pupae, and adults of terrestrial insects (Hinton, 1960, Hinton, 1961, Hinton, 1969).
A plastron is defined as a gas film of constant volume that is held on the outside of the cuticle by hydrofuge hairs or cuticular projections that provide an extensive water-air interface (Crisp and Thorpe, 1948). Although plastrons have evolved many times in insects, the only other known examples of plastron respiration are in millipedes (Diplopoda) and some mites (Acari: Arachnida) where, as in insects, gas exchange underwater involves a plastron linked to a tracheal system (Hinton, 1971, Messner et al., 1992, Messner and Adis, 1995, Adis, 1997, Adis and Messner, 1997, Adis et al., 1997). All extant arachnids, with the exception of a few mites and spiders, are terrestrial, and are subject to the same flooding hazards as terrestrial insects. However, apart from these mites and spiders, no adaptations for survival underwater comparable with those found in insects have yet been discovered within the class Arachnida.
Certain habitat types and geographic locations are more or less likely to experience severe flooding. The Florida Keys consist of a 210 Km island arc located a few degrees North of the Tropic of Cancer and are considered tropical. Key West (one of the lower keys) receives an annual precipitation of 100 cm, with approximately 70% of that rainfall concentrated into only six months of the year (mid May–mid November) (Ross et al., 1992). The Keys are also often subject to severe tropical storms and Big Pine Key was one of the worst hit by Hurricane George in the summer of 1998. Coupled with the fact that most of the land is less than 2 m above sea level and the highest point reaches only 5.5 m, these conditions often result in severe inundation by the sea (Ross et al., 1992). In response to the resulting periods of submergence, many of the plant species present on the Keys are adapted to survive periods of inundation (Ross et al., 1992) and it might be expected that this would also be true of the arthropods present on the islands.
Amongst these island arthropods is the amblypygid Phrynus marginemaculatus C. L. Koch. Amblypygids, whip spiders, comprise the lesser known order of arachnids, Amblypygi. Although the order itself is small, containing less then 150 species, amblypygids are commonly found inhabiting tropical and subtropical habitats around the world. They are morphologically distinct animals with elongate antenniform first legs, enlarged spined pedipalps, and dorso-ventrally flattened bodies. Phrynus marginemaculatus is a species commonly found underneath limestone rocks on Big Pine Key, FL. These rocks are in fairly open habitats with little vertical surface upon which to climb, and thus, it would not be surprising if this amblypygid species has some adaptation to avoid drowning. In this paper, we describe the ability of P. marginemaculatus to survive underwater by means of a plastron connected with its two pairs of book lungs.
Section snippets
Specimens
Individuals were collected during the day from underneath rocks on Big Pine Key, FL on 31 December, 1997 and 1 January, 1998. They were brought back to the laboratory at the University of Arizona where they were housed individually in 20 oz Dixie cups. They were kept on a 12:12 L:D light cycle at 26±2°C and ambient humidity. They were fed two to three crickets approximately every two weeks.
Responses underwater
To determine how long Phrynus marginemaculatus would voluntarily remain underwater, individuals were
Response underwater
When submerged in normally aerated water, individuals of Phrynus marginemaculatus remained submerged voluntarily for periods of 30 minutes to more than eight hours without coming to the surface (Fig. 1). They remained active underwater even though they did not carry a visible air bubble and periodically walked along the underside of the rock. Immediately following emergence, their activity levels appeared normal. The two individuals that were placed in aerated water for more than 24 hours
Discussion
Our results show that individuals of Phrynus marginemaculatus can remain underwater for periods of more than 24 hours. Since arachnid cuticle is not usually very permeable (Hadley, 1994), we explored the possibility of plastron respiration. We determined that animals were not able to remain responsive in deoxygenated water and thus, to remain active while submerged, they must be obtaining oxygen from the surrounding water. Structural observations indicate cuticular buttressing on the ventral
Acknowledgments
We would like to thank W. Hebets and N. Hebets for aiding in the collection of specimens. We also thank H. Alonso–Pimentel, E. Jockusch, K. Ober, W. Maddison, G. Binford, G. Bodner, S. Masta, M. Hedin, P. Gerba, E. Dyreson, J. O'Brien, M. Conklin, D. Bentley, B. Daley and S. Redella for their help in experimental procedures/design and their constant encouragement. E. Bernays and C. Martinez del Rio kindly commented on the manuscript. We would also like to acknowledge the United States
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