Plastron Respiration in the Non-Tracheate Arthropod <I

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Plastron Respiration in the Non-Tracheate Arthropod <I View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by DigitalCommons@University of Nebraska University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Eileen Hebets Publications Papers in the Biological Sciences January 2000 Surviving the flood: plastron respiration in the non-tracheate arthropod Phrynus marginemaculatus (Amblypygi: Arachnida) Eileen Hebets University of Nebraska - Lincoln, [email protected] Reginald F. Chapman University of Arizona, Tucson, AZ Follow this and additional works at: https://digitalcommons.unl.edu/bioscihebets Part of the Behavior and Ethology Commons Hebets, Eileen and Chapman, Reginald F., "Surviving the flood: plastron respiration in the non-tracheate arthropod Phrynus marginemaculatus (Amblypygi: Arachnida)" (2000). Eileen Hebets Publications. 20. https://digitalcommons.unl.edu/bioscihebets/20 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Eileen Hebets Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Published in Journal of Insect Physiology 46:1 (January 2000), pp. 13–19; doi 10.1016/S0022-1910(99)00096-7 Copyright © 1999 Elsevier Science Ltd. Used by permission. http://www.sciencedirect.com/science/journal/00221910 Submitted December 11, 1998; accepted February 17, 1999; published online October 7, 1999. Surviving the flood: plastron respiration in the non-tracheate arthropod Phrynus marginemaculatus (Amblypygi: Arachnida) Eileen A. Hebets, Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA (Corresponding author) Reginald F. Chapman, Division of Neurobiology, University of Arizona, Tucson, AZ 85721, USA Abstract Specimens of Phrynus marginemaculatus can remain responsive when submerged in water for more than 24 hours. Behavioral data indicate that P. marginemaculatus utilizes dissolved oxygen from the surrounding wa- ter. Scanning electron miscroscopy and light microscope sections show cuticular modifications for plastron res- piration. All previous examples of plastron respiration have involved animals with tracheal systems, but am- blypygids respire through the use of two pairs of book lungs. This study provides the first example of plastron respiration not only in the order Amblypygi, but also, in any non-tracheate arthropod. Keywords: amblypygid, arachnids, plastron respiration, book lungs, Phrynus 1. Introduction ders, are terrestrial, and are subject to the same flooding hazards as terrestrial insects. However, apart from these In climates with heavy rainfall and consequent flooding, mites and spiders, no adaptations for survival underwa- the ability of terrestrial arthropods to survive submer- ter comparable with those found in insects have yet been sion for extended periods of time is a critical element of discovered within the class Arachnida. survival. Many insects survive in habitats subject to in- Certain habitat types and geographic locations are undation through the possession of various behaviors more or less likely to experience severe flooding. The and structures that enable them to respire underwa- Florida Keys consist of a 210 Km island arc located a few ter. Among the physical structures permitting survival degrees North of the Tropic of Cancer and are consid- underwater, plastron respiration has evolved indepen- ered tropical. Key West (one of the lower keys) receives dently a number of times among the eggs, larvae, pupae, an annual precipitation of 100 cm, with approximately and adults of terrestrial insects (Hinton, 1960, 1961). 70% of that rainfall concentrated into only six months of A plastron is defined as a gas film of constant volume the year (mid May–mid November) (Ross et al., 1992). that is held on the outside of the cuticle by hydrofuge The Keys are also often subject to severe tropical storms hairs or cuticular projections that provide an extensive and Big Pine Key was one of the worst hit by Hurri- water-air interface (Crisp and Thorpe, 1948). Although cane George in the summer of 1998. Coupled with the plastrons have evolved many times in insects, the only fact that most of the land is less than 2 m above sea level other known examples of plastron respiration are in mil- and the highest point reaches only 5.5 m, these condi- lipedes (Diplopoda) and some mites (Acari: Arachnida) tions often result in severe inundation by the sea (Ross where, as in insects, gas exchange underwater involves et al., 1992). In response to the resulting periods of sub- a plastron linked to a tracheal system (Hinton, 1971; mergence, many of the plant species present on the Keys Messner et al., 1992; Messner and Adis, 1995; Adis, are adapted to survive periods of inundation (Ross et al., 1997; Adis and Messner, 1997; Adis et al., 1997). All ex- 1992) and it might be expected that this would also be tant arachnids, with the exception of a few mites and spi- true of the arthropods present on the islands. 13 14 HEBETS AND CHAPMAN IN JOURNAL OF INSECT PHYSIOLOGY 46 (2000) Amongst these island arthropods is the amblypy- In order to determine whether the animals could uti- gid Phrynus marginemaculatus C. L. Koch. Amblypy- lize oxygen from the surrounding water, we conducted gids, whip spiders, comprise the lesser known order of a series of trials examining the responses of individuals arachnids, Amblypygi. Although the order itself is small, over time in deoxygenated water. Two 600 ml beakers containing less then 150 species, amblypygids are com- containing 200 ml of distilled water at ~21°C were each monly found inhabiting tropical and subtropical habi- covered tightly with parafilm. A continuous flow of ni- tats around the world. They are morphologically distinct trogen was bubbled through the water of the test beaker animals with elongate antenniform first legs, enlarged via a Pasteur pipet passing through the parafilm; air was spined pedipalps, and dorso-ventrally flattened bod- bubbled through the other beaker which acted as the ies. Phrynus marginemaculatus is a species commonly control. After two hours, during which time the water found underneath limestone rocks on Big Pine Key, FL. in the test beaker was assumed to be completely deoxy- These rocks are in fairly open habitats with little verti- genated, an individual was placed into the water of each cal surface upon which to climb, and thus, it would not beaker. The individuals were paired for size. Every two be surprising if this amblypygid species has some adap- minutes, the response to mechanical stimulation with tation to avoid drowning. In this paper, we describe the forceps of each individual was determined. If it moved ability of P. marginemaculatus to survive underwater by location, it was scored as a positive, while if no move- means of a plastron connected with its two pairs of book ment was observed, it was scored as a negative. Trials lungs. lasted 10 minutes, during which time the gas flow was continued to ensure that oxygen was not replenished in 2. Materials and methods the test beaker. After 10 minutes, individuals were re- moved from the water and placed on their backs. If an 2.1. Specimens individual was able to right itself within two minutes, it was scored as a positive and if not it was scored as a neg- Individuals were collected during the day from under- ative with the assumption that it was oxygen deprived. neath rocks on Big Pine Key, FL on December 31, 1997 Fourteen pairs of individuals were tested. A Cochran’s Q and January 1, 1998. They were brought back to the lab- test was conducted to determine if individual response oratory at the University of Arizona where they were was independent of time submerged. housed individually in 20 oz Dixie cups. They were kept In order to verify the action of a plastron as the on a 12:12 L:D light cycle at 26±2°C and ambient humid- means by which amblypygids obtain oxygen underwater, ity. They were fed two to three crickets approximately we tested the responses of individuals underwater with every two weeks. a wetted, and thus disfunctional, plastron. The plas- tron was wetted with water of low surface tension placed 2.2. Responses underwater on the ventral side of the opisthosoma. When viewed To determine how long Phrynus marginemaculatus through a dissecting microscope, the wetting of the plas- would voluntarily remain underwater, individuals were tron can be seen as a darkening of the ventral surface. submerged and allowed to re-surface voluntarily. Five When the plastron is not wetted, the water cannot pene- plastic containers measuring 21 cm in diameter and 7.5 trate the cuticular structure and thus remains intact as a cm in height were filled with distilled water at ~21°C to water droplet on the surface of the opisthosoma. Batches approximately 4 cm deep. The water in these containers of water with different surface tensions were created by was not aerated in any way, but dissolved gases were pre- adding various amounts of the detergent NP40 to 200 sumably in equilibrium with air. A large rock was placed ml of distilled water. The surface tension of the experi- in the center of each plastic container so that only the mental water was subsequently measured through capil- very top of the rock was exposed to air, creating a moat lary action (Denny, 1993) around the rock. Individuals were then placed upon the For experimental trials, a new batch of low surface rock in each of these containers and gently pushed with tension water that was successful in wetting the plas- soft forceps into the water until completely submerged. tron was produced using one drop of NP40, dead crick- The time until each individual voluntarily re-surfaced ets, dirty paper towels, and dead cabbage looper cater- was recorded. pillars in water that was allowed to sit for one week to Two individuals were also placed in 600 ml beakers simulate a naturally produced reduction in surface ten- containing 200 ml of distilled water and allowed to re- sion.
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