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Behavior of Remipedia in the Laboratory, with Supporting Field Observations JOURNAL OF CRUSTACEAN BIOLOGY, 27(4): 534–542, 2007 BEHAVIOR OF REMIPEDIA IN THE LABORATORY, WITH SUPPORTING FIELD OBSERVATIONS Stefan Koenemann, Frederick R. Schram, Thomas M. Iliffe, Lara M. Hinderstein, and Armin Bloechl (SK, correspondence; AB) Institute for Animal Ecology and Cell Biology, University of Veterinary Medicine Hannover Foundation, Bu¨nteweg 17d, 30559 Hannover, Germany; (FRS) Burke Museum, University of Washington, Seattle, Washington 98195, U.S.A; (TMI, LMH) Department of Marine Biology, Texas A&M University at Galveston, Galveston, Texas 77553-1675, U.S.A. (SK: [email protected]) ABSTRACT We observed in the laboratory the behavior of six individuals of an as yet undescribed species of Speleonectes (Remipedia) over a period of 76 days. The live specimens were collected from an anchialine cave on the Yucatan Peninsula and maintained in separate aquaria at the Zoological Museum Amsterdam. In addition, field observations were conducted in the same cave to compare the laboratory results with naturally occurring behaviors. We found a variety of complex behavioral traits that include several new and unexpected findings. For example, our observations suggest that remipedes are not obligatory, but rather facultative carnivores, and that filtering particles might be the predominant mode of feeding. A digital video with examples of various behavioral traits can be downloaded at http://www. tiho-hannover.de/einricht/botanik/research.htm. INTRODUCTION reveal that the behavior of Remipedia comprises a variety Among the most intriguing arthropods that have emerged in of complex traits, including some new and unexpected recent years are crustaceans of the class Remipedia (Yager, findings. 1981). To date, we recognize 18 species (Koenemann et al., For example, it is widely accepted that remipedes are 2003, 2004; Wollermann et al., 2007; Koenemann et al., carnivores based on the three pairs of raptorial, prehensile 2007a), while new species are constantly emerging from the cephalic limbs, a distinct apomorphic feature shared by all caves in the Caribbean islands, the Yucatan Peninsula, species. This assumption is partially corroborated by our Mexico, and other tropical locations. Remarkably, some 25 observations, made both in the laboratory and in the field by years after their discovery, essential aspects of the biology two of us (TMI and LMH). However, our laboratory of Remipedia are either still not known, or poorly under- observations suggest that remipedes might not be obligatory stood. Unresolved issues include, for example, their phylo- carnivores but that filtering particles out of the water column genetic relationships and evolutionary history (Koenemann is another important mode of feeding. et al., 2007b), reproductive and developmental modes (Koenemann et al., 2007c), and reconstructions of their MATERIAL AND METHODS life cycle. In the laboratory, we studied six living individuals of a species of There are two relatively detailed investigations that focus Speleonectes that is morphologically closely related to S. tulumensis Yager, 1987. The animals were collected from Cenote Crustacea, a cave on the on the behavior and ecology of Remipedia. Kohlhage and Yucatan Peninsula located several kilometers south of Puerto Morelos, Yager (1994) provided an analysis of swimming and the Quintana Roo, Mexico, where this species occurs in comparatively high metachronal movement of trunk limbs. Another study of abundance. Five individuals were adults with body sizes ranging from 33.9 living remipedes in the laboratory by Carpenter (1999) to 40.8 mm (40 to 42 trunk segments), and one smaller individual, probably confirmed several instances of predatory behavior, with a sub-adult, measured 20.6 mm (35 trunk segments). The animals were maintained in two separate tanks in a completely dark detailed comments on the function of individual cephalic climate room at ZMA. The larger aquarium (150 liters) was connected to an appendages. However, aside from these studies and a few Eheim bio-filter pump system; fine sediment and small carbonate rocks brief published notes, we still know little else about the taken from the original collection site (anchialine cave) were used as bottom behavior of Remipedia. Therefore, we wish to take this material. The commercial bacterial culture ‘Bactomarine’ was added to the bio-filter of the large tank. A smaller tank, not connected to a pump or opportunity to record some new observations based on filtering system, contained small-sized aquarium gravel as bottom material. living remipedes both in the laboratory and in their natural After three weeks, small quantities of ‘Bactomarine’ were also added to the habitat. water of the small tank. A coral sea salt mix was used to maintain salinity During a recent diving expedition investigating anchialine between 32 to 35 ppt (49 to 53 mS/cm), which fell within the salinity range caves on the Yucatan Peninsula, we were able to collect live measured in several caves. Water temperature was kept constant around 24 degrees C, and the pH ranged from 6.8 to 7.7. specimens of Remipedia. Six individuals of an as yet Laboratory observations were conducted in three daily sessions, each undescribed species of the genus Speleonectes Yager, 1981 lasting between 30 and 60 min. In addition, we made videos between direct were brought back to the Zoological Museum Amsterdam observation intervals and overnight. Total observation time (direct (ZMA) and kept in aquaria. These were observed over observation and video-taping) constituted approximately 147 hours over a period of 76 days. We conducted several light reaction tests including a period of more than two months. We also conducted field abrupt and punctual illuminations of the tanks and/or individuals in the observations in the same cave to compare the laboratory tanks. In all instances, the observed individuals did not exhibit any results with naturally occurring behaviors. Our observations noticeable reaction to light. This is corroborated by field observations when 534 KOENEMANN ET AL.: REMIPEDE BEHAVIOR 535 whether the individual was swimming on its dorsal or ventral surface. When feeding behavior was observed, the remipede was followed, but not interfered with. In addition, food in the form of freshly killed cave shrimp (Typhlatya sp.) was offered to remipedes by hand and by placing shrimp on the cave sediment. RESULTS AND DISCUSSION Behavioral Observations in the Laboratory Swimming and Locomotion.—Apart from several different swimming modes described below, we made the following general observations: 1. The beating movement of the biramous trunk limbs is ceaseless, even during so-called resting periods, as described by Parzefall (1986). On each side of the trunk, five to seven limb pairs perform metachronal, synchro- nous strokes that appear as continuous, upward (anteriad) rolling waves (Fig. 1; for a detailed analysis of leg movement see Kohlhage and Yager, 1994). 2. The second antennae are also constantly moving; performing very fast, flap-like strokes from anteriad to posteriad (Fig. 2). Carpenter (1999) proposed that the antennae in Speleonectes epilimnius are used to comb detritus and plankton from the peduncular aesthetascs of the first antennae (antennules) and move them towards the atrium oris. The fact that the strokes of the second antennae are performed ceaselessly suggests that filtering particles out of the water column is a critical mode of feeding in Remipedia. 3. When feeding on large prey, the prehensile cephalic appendages are used to continuously manipulate the prey object (as described by Carpenter, 1999). 4. At least two pairs of the three prehensile cephalic limbs, the maxillae and maxillipeds, seem to beat irregularly laterad to mediad when individuals were not feeding on prey. These movements are not performed constantly, but most of the time and asynchronously, with left and Fig. 1. Individual of the remipede Speleonectes sp. from Cenote Crustacea right limbs moving differently (Fig. 3). Movement of the showing ‘vertical swimming’ behavior, with metachronal, synchronous maxillules was not distinguishable with the naked eye. strokes of trunk appendages. Left: ventral view; right: lateral view. 5. The first antennae (antennules) perform irregular, asynchronous sweeping strokes. individuals were illuminated with dive lights and showed no response. Several distinctive phases were noted while the animals Nevertheless, during direct observation periods and most video recordings, we used dim, indirect light sources, and occasionally an additional were in swimming mode. flashlight for short inspections. Some video tapes were recorded using the 1. Horizontal ‘backstroke’ swimming. This type of swim- infrared mode, i.e., without additional light sources. A digital video that summarizes various behavioral traits can be downloaded at http:// ming, with the ventral side up, was the predominant www.tiho-hannover.de/einricht/botanik/research.htm. mode of movement (approximately 65% of total During the initial phase of the observations, four individuals were kept observation time in the laboratory). This mode of in the large tank (including the sub-adult specimen) and two individuals in swimming was performed in the water column, at the the smaller tank. Whenever an individual died, individuals in both tanks were relocated, so that each tank contained at least two individuals. The first surface, and along the bottom (Fig. 4). individual (20.6 mm sub-adult) died after two days; the remaining five 2. Horizontal
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