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Octopus Vulgaris: Optimizing Energy Gain Through Prey Selection and Learning

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Octopus Vulgaris: Optimizing Energy Gain Through Prey Selection and Learning Octopus vulgaris: Optimizing Energy Gain Through Prey Selection and Learning Krista Rigsbee, Lora Johansen, Katie Mo, Daniel O’Shea Fall 2014 Abstract: We investigated the ability of Octopus vulgaris individuals to optimize energy gain through prey selection near Calvi in Corsica, France. Seven octopods were used in three different experiments: energetic efficiency trials, novel prey training trials, and prey preference trials. Common prey, Haliotis tuberculata (abalone) and novel prey, Mytilus galloprovincialis (mussel) were used in energetic efficiency trials to show that abalone provides more energy than mussels. M. galloprovincialis training trials were performed with octopus nine and showed a general, decreasing trend in energy gain with prolonged exposure, perhaps due to lack of motivation. However, octopus nine exhibited extreme potential to improve. Lastly, preference trials supported, although insignificantly, that octopus nine favored H. tuberculata before and after M. galloprovincialis training trials. Results from these three experiments suggest that O. vulgaris will choose the prey with the greatest energy gain. Consistent with optimal foraging theory, this information contributes to the management of this commercially valuable species. Introduction: According to optimal foraging theory, predators maximize their fitness by targeting prey that is most energetically favorable and has minimum associated costs, defined as time, energy, and risk of finding/handling the prey. Generalists minimize search costs by foraging for a variety of prey, while specialists minimize handling costs by learning to efficiently consume one prey type (McPeek, 1996). In 2012, Carrington et. al showed that octopods are capable of catching multiple types of prey but individuals have the capability to specialize through learning. The goal of our study is to investigate the specialized foraging behaviors associated with maximizing energy gain for Octopus vulgaris. Understanding the mechanisms that drive prey preference of O. vulgaris could be helpful in the management of this commercially and intrinsically valuable species (Castellanos-Martínez et al. 2013). With increasing temperature and acidity of marine environments, it is predicted that many invertebrates will face challenges in the near future. The ability to utilize multiple foraging strategies, combined with their short life span and ability to move, might allow octopods to adapt to a rapidly changing marine environment more effectively than other benthic invertebrates (Gutowska et. al, 2008). It has been demonstrated that acidification will have adverse affects on the genus Haliotis (Crim, 2011). However, Mytilus shows tolerance to changes in pH (Thomsen, 2013). Here we investigated the ability of octopus to specialize on the novel M. galloprovincialis by learning to handle them more efficiently. In the event of community perturbation and change in prey availability, this skill could be imperative to the survival of the common octopus. Wells et. al (1983) suggests that feeding state is determined by handling and digestion of prey and accounts for the majority of the octopus’ energy expenditure. If there is significant variation in energy requirements of handling different types of prey, it could explain individual specialization and provide evidence of optimal foraging in octopods. In order to test our general hypothesis that O. vulgaris handle common prey more efficiently than novel prey, we proposed the following specific hypothesis. Using metabolic data from feeding trials to approximate energy budget in the lab, Haliotis tuberculata will have a higher ratio of biomass per oxygen consumption than Mytilus galloprovincialis for O. vulgaris. From past studies H. tuberculata is shown to be the overwhelming preference in the lab and a common prey type in the field. M. galloprovincialis is known to be a novel prey type at this location (Carrington et. al, 2012). Because they are both molluscs, we assume they will have similar energy expenditure during digestion. Based on this assumption, the main difference in energy expenditure between these two prey items should result from handling time. Our second general hypothesis is that prey preference will reflect the prey type that the individual octopus can most efficiently handle and will change in the event that experience and learning makes novel prey more optimal. We will test this by performing a series of preference trials before and after training the octopus to handle M. galloprovincialis (novel prey). We predict that after the octopus has gained experience with mussels, it will show increased preference towards M. galloprovincialis than it did before the training. Our third general hypothesis is that experience with novel prey will decrease the energy required to handle it. In order to support this, we will perform training trials in which we only offer M. galloprovincialis to the octopus. We hypothesize that the ratio of prey biomass per oxygen consumption will increase as an individual octopus gains experience with M. galloprovincialis. Efficiency will be measured using the formula provided in the statistical analysis. Methods: Site Description We conducted this study in October 2014 at Station de Recherches Sous-Marines Oceanographiques (STARESO) (42° 34’ N, 08° 43’ E) near Calvi in Corsica, France. The octopods used in this study were located in the harbor, along the shore south of the harbor, and in deeper sand patches (Figure 1). STARESO harbor is mostly rocky bottom and seagrass (Posidonia oceanica). South of the harbor is characterized by rocky bottom at shallow depths. Offshore, P. oceanica dominates the substrate. Within these sea grass meadows there are crescent shaped sand patches called the Bananas. Species description Octopus vulgaris, also known as the common octopus, has a global range extending from the Atlantic through the Mediterranean Sea. O. vulgaris can grow to 25 cm in mantle length, with arms up to a meter long. They commonly hunt at dusk, specializing in prey types such as crabs, and molluscs (Nixon, 1987). Often found in shallow rocky substrates, O. vulgaris prefers water no deeper than 200 meters for hunting and construction of their dens (Wood & Day 1998). We used two prey types, Haliotis tuberculata and Mytilus galloprovincialis. H. tuberculata, an abalone known as the green ormer is found from the British Channel Islands through the Mediterranean Sea. Within STARESO harbor H. tuberculata was a common prey type of O. vulgaris. The green ormer is a single shelled gastropod that can grow to 12 cm in length, although no specimen larger than 5 cm was found within our study site (Peck, Culley, Helm 1987). M. galloprovincialis, commonly known as the Mediterranean mussel, is a novel prey species at STARESO. For this study, we purchased live M. galloprovincialis at a local market, as it was not found at our sampling locations. It is a native bivalve mollusc, in the Mytilus edulis complex (a group of three closely related species of blue mussels)(Varvio et. al, 1988). M. galloprovincialis is a smooth shelled filter feeder and can grow up to 150 mm in length (Branch & Steffani, 2004). Field Methods We located and tagged 17 octopus dens within 24 days of SCUBA and skin diving at STARESO. We tagged dens October 1-24, 2014 at three sites; in the harbor, South of the harbor, and in the bananas (Figure 1). Ten octopods were captured for lab experimentation; however, usable data was only obtained from seven individuals. Shallow dwelling octopods (<2m) were caught free diving, while deeper octopods (>2m) were caught SCUBA diving. Figure 1: Map of STARESO Institute of Oceanography (42° 34’ N, 08° 43’ E) near Calvi, Corsica where collections of octopus took place. Lab Studies In order to test our hypothesis that Haliotis tuberculata has a higher prey biomass per oxygen consumption than Mytilus galloprovincialis, we collected metabolic data and prey biomass from feeding trials and lab experiments described below. We conducted feeding trials throughout the day when there were limited disturbances to the octopods. To avoid confounding factors, we alternated the order in which prey was given to an individual octopus and between octopods. Blinders were used on each of the three tanks to reduce light, disturbance, and aggression to other octopods in captivity. To begin the trial, we placed the prey within the eyesight of the octopus. Since H. tuberculata has a large foot that allows it to quickly attach to substrate, we allowed it time to settle in the tank before beginning the trial, in order to simulate natural foraging. We defined a successful trial as one that produced reliable data for handling time and the number of breaths during handling time. Handling time is defined as the interval from which the octopus touched the prey to when the prey’s flesh was exposed. We considered the flesh exposed when H. tuberculata was displaced or when the two shells of the M. galloprovincialis were pulled apart. If no prey was eaten within ten minutes then it was removed and the trial was concluded. Each individual octopus had at least one successful M. galloprovincialis trial and one successful H. tuberculata trial. In order to determine the amount of oxygen used, we performed a series of tests to obtain basal breathing rate, average breath duration, siphon diameter, and water velocity per breath. To determine the basal breathing rate, two observers counted and averaged the number of times an octopus’ siphon closed during a period of one minute. We measured all other variables using video analysis. We measured average breath duration by using the siphon as a visual reference and the number of frames per second of the video. We measured the siphon diameter by using the video analysis software, ImageJ64, after calibrating the number of pixels with the meter tape in the video. Lastly, we were able to estimate the velocity of each octopus’ breath with a milk test. With the tank’s water flow temporarily turned off, we used a pipet to produce a cloud of milk near the octopus. By analyzing the video frame by frame, we measured the milk’s velocity as it was moved by the octopus’ exhalation.
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