Chemosensory in Sepia officinalis Predation Pike Spector & Tamsen Peeples 2010
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1 Chemosensory in Sepia officinalis Predation Pike Spector & Tamsen Peeples 2010 Abstract The common cuttlefish, Sepia officinalis, has been found to use distance chemoreception for a variety of facets, and has the ability to sense prey without visual cues. We designed and conducted an experiment to determine if S. officinalis uses distance-based chemoreception to locate prey in a confined space. Through the use of isolated, concentrated prey items, flow through water control and a tank designed to eliminate all visual stimuli we tested the ability of S. officinalis to rely solely upon chemoreception to locate prey. Our study showed cuttlefish did not show a response to the presence of prey scent meaning chemoreception did not clearly affect their foraging abilities at a close range Introduction Predator-prey interactions serve as the fundamental links in ecological systems. Primary producers are eaten by herbivores that are in turn eaten by carnivores. Herbivores need to locate their food and predators need to be able to locate their prey. Often, hunting relies on both being able to visually locate prey as well as developing a finely tuned sense of smell. The use of scent detection plays a pivotal part of predation for both marine and terrestrial hunters. For example, on land, detection-dogs use tracking techniques based solely upon olfactory reception (Dematteo et al. 2009). While terrestrial odor tracking may be difficult, in the marine environment it is far more challenging because the ocean is in constant motion. Compounds are dissolved in the water column and become distorted as the environment is stirred (Finelli et al. 1999). For any organism, the ability to distinguish between conspecifics, prey, predators and the environment requires a greater investment of energy to olfaction. Many marine organisms have developed the ability to chemosense (detecting compounds dissolved in the environment). For example, the pelagic yellow fin tuna uses chemosensing to detect prey that is far beyond its visual range (Williams et al. 1992). In their study of Senegalese sole, a nocturnal benthic fish, Barata and Hubert (2009) found that once the odor of prey was detected, the sole s swimming ability and feeding activity were greatly increased. A blinded octopus will still move towards a scent in perceives as a food source (Chase and Wells 1986). Chemoreception has been well studied in cephalopods. Chemoreceptors have been found on the suckers of octopods as well as, but in less concentration, on squid and cuttlefish suckers (Boal and Golden 1999). While octopods forage primarily by touch, most cephalopods utilize their chemoreceptors to detect chemical cues in concentrations of as little as 10-5 M (Budelmann 1996). This ability strongly suggests the use of distance chemoreception in Coleoid cephalopods (octopods, cuttlefish and squid). As most Coleoids are nocturnal or live at depths where little light is present, the ability to track prey by scent is crucial to their success as predators (Budelmann 1996). Research has shown that for Sepia officinalis, the common cuttlefish, distance chemoreception is useful for many aspects of interaction, not just forging. Distance
2 chemoreception refers to the ability to sense compounds without physical contact. Studies have shown that S. officinalis not only uses distance chemoreception to find a mate, but to also avoid danger by being able to sense ejected ink by conspecifics (Boal and Golden 1999). Moreover, S. officinalis can sense the presence of mated versus non-mated individuals and the odor of a predator. When water saturated with the odor of prey species (crabs, shrimps and fish) or ink from a conspecific is introduced to an individual, there is a noted increase in ventilation rates (i.e. perception) as well as distinct body movements in response to the cue (Boal and Golden 1999). The purpose of this study is to test the use of distance chemoreception in foraging by the common cuttlefish, S. officinalis. We investigate the ability of cuttlefish to use the sense of olfaction to sense prey at a close range while excluding the use of contact reception and visual acuity. By placing an individual cuttlefish in a controlled environment we can view changes in behavior when water saturated with live fish is introduced while eliminating visual cues. By providing a control flow coupled with preyconcentrated flow we can document the direction the cuttlefish chooses; either towards or away from the prey concentrate. Question: Can S. officinalis use distance-based chemoreception to locate prey in a confined space? Hypothesis: Cuttlefish hunting is based on using both visual cues and chemosensory reception. Visual confirmation is the basis for the final strike but cuttlefish locate, determine concentration, and stalk prey through the use of scent. Prediction: S. officinalis placed in a controlled, experimentally designed tank will be drawn toward the compartment containing the odor of prey species. Materials & Methods Study Species The common cuttlefish, Sepia officinalis, here after referred to as cuttlefish, is found in the Mediterranean, Baltic, and Northern seas. Like many cephalopods they are nocturnal but can be active during daylight hours. Embryonic cuttlefish visually imprint their primary prey species, and will prefer this prey over others (Darmaillacq et al. 2006). S. offcinalis is an active predator of a variety of fish and crustacean species. S. officinalis is thought to be primarily a solitary predator and only come together for breeding. S. officinalis tend to remain low to the substrate and were often found on or over sandy and rocky areas or Posidonia patches above 10m. Location This study took place at the STARESO Research Institute of Oceanography (Figure 1). Test subjects were caught using SCUBA within the STARESO harbor at a depth under 8m. The harbor is surrounded on three sides by granitic rock walls that drop steeply into the water, shielding the harbor from most wind and surf. The substrate of the harbor is comprised of sand and gravel bordering the granite walls with small patches of P. oceania giving way to a large Posidonia meadow that extends out of the harbor.
3 QuickTime and a decompressor are needed to see this picture. After capture cuttlefish were held in three aquaria when not in the experimental tank. Cuttlefish were labeled A-F in sequential order of when they were captured. Holding tanks were laid with sandy substrate from the harbor to provide an adequate habitat for the cuttlefish between experiments. Figure 1: STARESO Research Station and Harbor; cuttlefish were captured either within the harbor or just north of the jetty. Experiment Tank Construction Prey Tank Figure 2: Schematic of experiment tank showing internal dividers.
4 In order to test our hypothesis we used a tank with walls measuring 80x40x30cm and a volume of 786 cm 3. Two Plexiglas dividers were measured and cut to 27x40 cm in order to create three compartments (Figure 2). We cut two openings, one in each divider, 15x10cm centered on the bottom. The entire tank, except for the top, was blacked out, to eliminate all visual cues. This allowed us to record our statistical and behavior observations without disturbing the test subject. Experimental Method Prior to each trial the experimentation tank was flushed for 20 minutes with the control water. 15.4g wet weight of Atherina sp. and Atherion sp. were moved into the elevated prey tank. The water in the experiment tank was then siphoned down to 26L. A test subject was placed in the middle section of the tank and left to settle between 10 to 70 minutes, depending on level of visible agitation. The experiment began when the test subject would remain calmly resting on the bottom of the tank. The side which the prey flow-through was placed in was determined randomly. The doors between sections were sealed. The control flow was turned on and water from the prey tank was allowed to flow into the sealed compartments for one minute. After one minute the doors were removed and a timer started. Once the individual was observed moving from one compartment to another a 30 second time was started. If the subject remained in the selected compartment for the 30 seconds a result was recorded and the trial was ended. Should this compartment contain the prey flow-through, the subject would be rewarded with a prey of identical species to those in the prey tank. After 10 minutes the experiment was terminated if the subject remained in the center compartment, or did not remain in either of the side compartments for at least 30 seconds. After a trial the experiment tank would be flushed with control water for 20 minutes, and the prey tank refilled. After 20 minutes the experiment tank would be siphoned back down to 26L, and a new subject would then be introduced and left to settle. If the test subject was not rewarded with prey it would remain in the experiment tank during the 20-minute flushing of control water and during the siphoning. No more than four subsequent experiments would be run using the same subject. Results
5 Figure3- Contingency Analysis of Direction By Individual Mosaic Plot (n=5 cuttlefish) The sum of the direction the individual chose was plotted using a Y-by-X distribution and compared in a mosaic plot (Figure 3) in order to account for specific behavior. A null result means that the cuttlefish did not chose the prey-concentrate compartment or the control flow-through compartment. Note that of the 6 cuttlefish tested only 5 were used in the results. (P=0.05, likelihood ratio= 15.4 df=8) A chi-square test of goodness-of-fit-was performed to determine which direction the cuttlefish preferred. Presence for control flow and prey-concentrate flow and preyconcentrate was not equally distributed in the population, 2 (1, N=23)= , p<0.05 therefore we cannot reject the null hypothesis that cuttlefish do not use distance chemoreception to forage for food. Out of the 54 trials 23 were not null, there doesn t appear to be any directional bias towards or away from the prey-concentrate flow. Cuttlefish A(1) almost evenly chose each option. Cuttlefish B remained in the center tank the majority of the time and didn t respond to the stimulus during any of the trials. Cuttlefish C chose the control tank more times than the prey tank but both cuttlefishes D and E chose the prey tank more than they chose the control tank (Figure 3) Behavioral Observations Much of the data we collected was ordinal in nature. Test subjects displayed a wide range of behaviors during and between trials. Cuttlefish A often displayed agitated behavior during experimentation, characterized by constant swimming and aggressive posturing and pigmentation. Cuttlefish A exhibited similar behaviors when cuttlefish F was introduced into the same tank and when cuttlefishes D and E were visible. Other individuals, such as B and F, rarely displayed any reaction during experiments and remained motionless on the bottom.
6 QuickTime and a decompressor are needed to see this picture. Figure 4: Cuttlefish displaying aggressive posturing and pigmentation Aggressive and territorial behavior, posturing, and pigmentation were displayed (figure 4) by individuals sharing tanks, most commonly between individuals of similar size. Cuttlefish A was seen displaying aggressive posturing to conspecifics of a similar size in the tank opposite the lab (a distance of approximately two meters). Cuttlefish F was cannibalized by individuals D and/or E after three days in the same tank, and cuttlefish C was eaten by B after nine days of sharing the tank. Discussion In our study cuttlefish did not show a response to the presence of prey scent meaning chemoreception did not clearly affect their foraging abilities at a close range. A lack of change in behavior may have resulted in four outcomes; the test subject did not receive the stimulus (i.e. the prey species scent), the cue was present but elicited no response, the subject received the cue but was unable to locate the source, or the cuttlefish were too stressed to react to any stimuli. The first possibility seems unlikely considering the measured amount of prey-soaked water flowing into the tank. But if the stimulus did reach the individual what could account for the lack of response? It seems clear that although distance chemoreception is important for the cuttlefish, on a smaller scale its role may be negligent. Two factors that may have influenced our results were the inconsistent time of
7 day at which the trails were run and the changing of abundance and species of prey. Trails were run at all hours but not all individuals were run at the same time of day. While the tank was blacked out the lab was walled on one side by windows that allowed natural light to fill the lab during daylight hours. Four of the cuttlefish were observed to have fed in daylight hours, but all were observed eating after sunset. The range of daylight across the trials may have skewed the results if only some of the cuttlefish engaged in daylight feeding. Due to shared resources in the lab, the abundance and species of prey was changed throughout the experiment. While the exact numbers and species were recorded the variation may have influenced the cuttlefish s ability or willingness to detect the prey. As mentioned earlier, cuttlefish have a prey preference that is imprinted at an early age (Darmaillacq et al. 2006). We could not account for individual preference, although the diversity of prey species may have contributed to our results. Some individuals, such as cuttlefish A, were observed to have fed upon fish species varying greatly in size as well as crustaceans while other individuals were observed only eating fish of one size. Boal and Golden (1999) established the importance of distance chemoreception in S. officinalis for a variety of behaviors. As part of their results Boal and Golden found that the scent of prey increases the ventilation rate for S. officinalis, which indicates their response to the stimulus. While this remains true, our results (Figure 3) show that cuttlefish are unable to locate prey without a visual reference. Behavioral influences may have also contributed to our results. All cuttlefish displayed unique and individual behaviors and characteristics. Some cuttlefish remained completely motionless during the experiments; some swam rapidly around the tank, while others slowly shifted towards one end or the other during the trail s duration. If this project was to be repeated or expanded upon, the number of individuals should be increased and be kept in separate isolated holding tanks. To reduce stress to the subjects, experiments could be conducted in habitat tanks. The increase in the number of individuals would benefit the results by producing more data and variation. By separating the cuttlefish in their own individual holding tanks you would remove the threat of cannibalism. To account for prey species preference, a more varied range of prey species could be used and in different concentrations. Acknowledgments First would like to extend our deepest gratitude to Pierre Lejeune and the rest of the staff at the STARESO Research Institute of Oceanography for hosting us and providing the means to complete this experiment. We would especially like to humbly thank Pete Raimondi and Giacomo Bernardi for presenting us with this opportunity and for facilitating everything. We thank the TA s Jimmy O Donnell, Brenna Mahoney and Alexis Jackson for all of their editing help and assistance in the field. Special thanks to Andrew Kim for his support with capturing and keeping cuttlefish and to Alessio Bernardi for retrieving the prey species used in the experiment. Literature Cited
8 Boal, J. G., and D. K. Golden Distance chemoreception in the common cuttlefish, Sepia officinalis (Mollusca, Cephalopoda). Journal of Experimental Marine Biology and Ecology 235: Budelmann, B. U Active marine predators: The sensory world of cephalopods. Marine and Freshwater Behaviour and Physiology 27: Chase, R., and M. J. Wells Chemotactic behavior in Octopus. Journal of Comparative Physiology a-sensory Neural and Behavioral Physiology 158: Darmaillacq, A. S., R. Chichery, N. Shashar, and L. Dickel Early familiarization overrides innate prey preference in newly hatched Sepia officinalis cuttlefish. Animal Behaviour 71: Dematteo, K. E., M. A. Rinas, M. M. Sede, B. Davenport, C. F. Arguelles, K. Lovett, and P. G. Parker Detection Dogs: An Effective Technique for Bush Dog Surveys. Journal of Wildlife Management 73: Finelli, C. M., N. D. Pentcheff, R. K. Zimmer-Faust, and D. S. Wethey Odor transport in turbulent flows: Constraints on animal navigation. Limnology and Oceanography 44: Williams, J. D., K. N. Holland, D. M. Jameson, and R. C. Bruening Amino-acid profiles and liposomes - their role as chemosensory information carriers in the marine-environment. Journal of Chemical Ecology 18:
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