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Home , Common octopus, Green ormer, Mediterranean mussel, 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, . Seven octopods were used in three different experiments: energetic efficiency trials, novel prey training trials, and prey preference trials. Common prey, tuberculata () and novel prey, galloprovincialis () were used in energetic efficiency trials to show that abalone provides more energy than . 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 .

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 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 . 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 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 (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 . O. vulgaris can grow to 25 cm in length, with arms up to a meter long. They commonly hunt at dusk, specializing in prey types such as , 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 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 , 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 breathing rate, average breath duration, 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. In order to obtain the biomass of the meat for each prey item, we used two different methods. For the H. tuberculata trials, we measured and recorded the weight of the entire abalone to the tenth of a gram before we placed the prey in the tank. After the trial was over and the meat eaten, we weighed the discarded shell. The difference in these two numbers gave us the meat weight of each H. tuberculata. Due to the proportionally large amount of water weight in each M. galloprovincialis, we estimated the meat weight of the individuals in the trials. Using data from M. galloprovincialis dissections, we created a linear regression model comparing meat and shell weight. We found a significant relationship (p<.0007), allowing us to calculate the meat weight using a trendline from the model, given by the following equation:

To test our second specific hypothesis, we performed a series of preference trials on octopus nine by placing one of each prey type (H. tuberculata and M. galloprovincialis) equidistant from the octopus. The octopus was then given ten minutes to take one. If octopus nine did not choose a prey item within that time, we took both items away and the trial ended. In this experiment, we defined choice as the prey item eaten, regardless of which was touched first. Once the octopus started eating one prey item, we removed the remaining one and recorded the preferred prey type. We repeated this procedure every few hours to establish octopus nine’s prey preference. After establishing the original preference, we preformed training trials, described below. We then conducted another set of preference trials in order to determine if increased experience affected the individual’s prey preference. After establishing its original preference, we offered octopus nine only M. galloprovincialis for five days (9 trials) to test our third specific hypothesis. We used this data to determine if experience improved octopus nine’s efficiency at handling M. galloprovincialis.

Figure 2: Because of the proportionally large amount of water weight in M. galloprovincialis, we created this model and used the linear equation: Meat weight=.8176+(.5368*Shell weight) to estimate the meat biomass of the individuals used in the trials. We used data from M. galloprovincialis dissections to create a linear regression model comparing meat and shell weight. P <.0007.

Statistical Analysis In order to calculate the use of oxygen necessary to open each prey item, we used the basal breathing rate, average breath duration, siphon diameter, and water velocity per breath in the following equation. According to Dejours et. al (1970), Octopus vulgaris ventilates 17L of water per mmol of oxygen consumed in 22℃ water (our study site ranged from 22-23℃). Using this information, we calculated the amount of oxygen used to handle each prey with the following equation.

Using the meat weight of each prey item to create a ratio of biomass per oxygen, we performed a one-way ANOVA test to graphically depict if abalone had a higher ratio of biomass per oxygen consumption than mussels (Figure 3) To test preference, trials were conducted to see if octopus nine preferred H. tuberculata over M. galloprovincialis. We used a Chi-squared analysis to test for preference (Figure 5). After we established a preference for octopus nine, we moved onto training trials where we only offered mussels to see if it resulted in increased efficiency. We performed a regression analysis with a best-fit line to see if the octopus’ efficiency of opening M. galloprovincialis increased (Figure 6). To test if the octopus’ preference changed after training on M. galloprovincialis, we again performed preference trials and ran a Chi-squared analysis.

Results: The results for our first hypothesis, regarding energetic gain of common vs. novel prey, were analyzed with a one-way ANOVA test shown in figure 3. This depicts a calculated p-value of .0490 and shows that the biomass per per oxygen consumption is significantly higher for H. tuberculata than for M. galloprovincialis. Regarding our hypothesis on the ability for O. vulgaris’ ability to exhibit changes in prey preference, our results showed that the preference for H. tuberculata over M. galloprovincialis did not significantly change after the training trials (fishers exact=0.533). In the initial preference trials, octopus nine chose to eat abalone 87.5% of the time (7 out of 8 trials). After the M. galloprovincialis training sessions, octopus nine chose to eat abalone 100% of the time (7 out of 7 trials (Figure 5)). However, octopus nine showed a consistant behavioral pattern in these trials in which it interacted with M. galloprovincialis before it ate H. tuberculata. Concerning our hypothesis on experience with novel prey, our linear regression model (Figure 6) showed a significant p-value of .0224, however it’s negative slope is the opposite of our prediction (shown in green). This provides evidence that biomass oxygen consumption decreases with increasing number of trials. However, there is one outlier (shown in red) that supports the potential for incredibly high energetic efficiency of handling M. galloprovincialis. If included, this outlier changes the slope of the line to be positive (shown in red). However, when the outlier is included, the relationship between biomass per oxygen consumption and trial number is insignificant with a p-value of 0.7057.

Figure 3: This one-way ANOVA test, shows Haliotis will have a higher biomass per oxygen consumption than Mytilus for Octopus vulgaris. Calculated p-value of .0490

Figure 4: Bar graph depicting mean biomass per oxygen consumption compared to prey type.

Figure 5:. Chi2 analysis before and after training on Mytilus. Fishers Exact was .533 probability that before is greater for Mytilus than Haliotis.

Figure 6: This linear regression shows the relationship between biomass/oxygen consumption and trial number for octopus 9. The red dot is an outlier and the corresponding red line is the fit line including the outlier. The green fit line is the one excluding the outlier and the one used in our analysis.

Figure 6: Including the outlier

Discussion: Since our critical p-value is .05 and our calculated p-value is .048, we reject the null and accept our first specific hypothesis that H. tuberculata will have a higher biomass per oxygen consumption than M. galloprovincialis for Octopus vulgaris. Given that abalone is a very common prey item at this study site and has been shown to be a frequently consumed in the field and lab, O. vulgaris is experienced with H. tuberculata and thus, very efficient (McConnell & Scott 2010). This supports our hypothesis that O. vulgaris chooses H. tuberculata because of its higher energy return. However, this may also be true because O. vulgaris must exert more energy to pry open the two halves in order to expose the flesh of the mussel, while abalone only needs to be plucked from the substrate. Our second general hypothesis states that each individual octopus will choose the most efficient prey and will change preference in the event that experience makes novel prey more optimal. We found that the preference of octopus nine did not change significantly after the M. galloprovincialis training sessions. These results are consistent with our second hypothesis, but not significant (Critical p-value=.05, calculated fishers exact=.533). Because octopus nine preferred H. tuberculata even after exposure to M. galloprovincialis, this suggests O. vulgaris will choose the prey with the highest energy gain. From our third hypothesis regarding M. galloprovincialis training experiments, we calculated a p- value of .0224. This, being lower than our critical p-value (.05), shows that the relationship between experience and biomass per oxygen consumption is significant, however the slope of the trend is negative. We had anticipated that with increased exposure to M. galloprovincialis, O. vulgaris would increase its energetic return. However, the overall trend was negative possibly due to a lack of motivation in the lab. Although our hypothesis is not supported by the general trend, octopus nine had some trials that showed a drastic increase in efficiency. This shows a potential for an increasing trend and we postulate that more motivation would result in conclusive findings that O. vulgaris increases its energetic return with novel prey feeding experience. The results from these three experiments suggest that O. vulgaris optimize energy gain through prey selection and learning. We supported that common prey (H. Tuberculata) provide more energy than novel prey M. galloprovincialis. Our preference trials supported, that an octopod’s preference reflects the most energy efficient prey type. Training trials showed a general, decreasing trend in energetic efficiency, but one trial shows extreme potential to support the argument that experience with novel prey increases energy gain. These results are consistent with optimal foraging theory and could be informative in the management of O. vulgaris, a commercially valuable species. This knowledge could also help predict O.vulgaris’ foraging adaptability to perturbations, especially in the event of rising temperatures and acidification. To further investigate the specialized foraging behaviors associated with maximizing energy gain for Octopus vulgaris, we propose a behavioral follow-up study to see if training octopus on a novel prey type can result in a trend of improvement. We believe with a larger study and motivation for the octopus, this behavioral study could be improved. Another area of interest would be to further test if O. vulgaris exhibit optimal foraging theory with respect to the abundance of prey by test for switching in a lab setting. This might be achieved by placing different relative abundances of prey items in the tank for preference trials to see if the octopus would target prey that was seemingly more abundant.

Acknowledgements: We would like to thank Pete Raimondi, Giacomo Bernardi, Kristy Kroeker, Gary Longo, Kate Melanson, Colin Gaylord, and all the staff at STARESO for helping guide us throughout our research. We would also like to thank everyone from Bio 159 2014 for their support and help on our project.

Works Cited:

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