Habitat Association of Arbacia Lixula in the Ligurian Sea

Transcription

1 Habitat Association of Arbacia Lixula in the Ligurian Sea Audra Barrios, Kimberly Powell, Melissa Nehmens Abstract The sea urchin Arbacia lixula is a common intertidal species found in the Mediterranean in association with crustose coralline algae. Previous studies on habitat association between A. lixula and crustose coralline algae reported that A. lixula creates mosaics of crustose coralline algae interwoven between erect foliose algae. Through surveys of urchin distribution and algal distribution, we were able to determine that the urchin distribution was not due to random chance, but based on preference with a p-value of > Because A. lixula is a mobile species driving the habitat association, a field study was done to determine whether the habitat association was due to the food preference of the urchin or because the coralline algae acts as a refuge from harm for the urchin. We tested the force required to remove the urchins from different substrates and found that a force of 2000g was required to dislodge the urchin from crustose coralline algae, while only 350 g were needed to dislodge the urchin from erect foliose algae. This showed that the urchin does benefit from living on crustose coralline for hydrodynamic purposes. Urchins dissected from the field and lab tests helped determine that the food preference of A. lixula was erect foliose algae which averaged 92.62% of their diet. Introduction Examining habitat associations allows for a better understanding of how a species interacts with its environment. The general theory of such relationships often results in a net benefit for the species driving the association where the habitat provides food resources, protection, and/or enhanced ability for reproduction. Habitat associations are seen in many systems such as parrot fish and corals, where the parrot fish uses the coral as an algal food source. In the case of Arbacia lixula, a sea urchin found

2 in the Mediterranean sea, there is an association with crustose coralline algae. Coralline algae is a habitat that provides both food and protection, thus allowing them to successfully occupy the inter and subtidal regions in the Ligurian Sea. The black sea urchin, more commonly known as the male urchin, has a coastal distribution ranging in depths from 0-50 m, is herbivorous and grazes on a variety of substrates (Bulleri et al, 2002). A. lixula is more commonly found on vertical walls covered with coralline encrusting substrates, rather than walls covered in erect foliose algae (Bulleri et al 1999) and bare rock. A. lixula is also commonly found on regions of mosaics dominated by crustose coralline algae and erect foliose algae (Bulleri et al, 2002), which in this study we refer to as patch. A. lixula is located in shallower regions near and within the intertidal, and thus, must be able to tolerate harsh wave action (Bulleri et al, 2002). A study performed by Bulleri, Bertocci, and Micheli (2002) suggested that urchins are mainly found on coralline alga due to wave exposure which allows for easier attachment on coralline substrate. Through preliminary urchin counts and observations of distribution, we noticed a pattern in which urchins congregated on areas composed of coralline algae, and even more commonly on the mosaic coralline regions. From this observed pattern, our goal for this study is to determine the mechanisms which cause the observed habitat association between A. lixula and its environment, particularly coralline algae. To that end, we tested two hypotheses: (1): A. lixula is found on coralline algae because it has eaten the erect foliose algae allowing coralline algae to proliferate. (2) A lixula is found more often on crustose coralline patches because they can withstand wave action better on coralline as opposed to erect foliose algae. Materials and Methods Study Site Our experiment was conducted in Revellata bay at STARESO marine field station in Calvi,

3 Corsica, France ( 42º34'48.85 N, 8º43'26.89 E). (Figures 1 and 2). The rocky walls of the intertidal are composed of granite, which is where the urchins in this study were found. We observed five sites to the North and four sites to the South of the harbor at STARESO for the duration of October, Our surveys took place within two meters in depth from the surface. Study Systems Arbacia lixula is a key component of the system in which it is found. It plays a large role in algal distribution through its active grazing. Its a mobile species that uses tube feet, or podia, for locomotion, feeding and attaching to substrate. The podia have suction pads at the extremities, which are a component of their water vascular system (Smith, 1989). They occur most abundantly on vertical surfaces of rock walls. For our experiments, A. lixula was easy to manipulate since they do not move quickly. However, removing them from rocks without damaging their podia was difficult due to the suction pads. They do not migrate over long distances however, generally staying in the same area throughout their life. (Guidetti, 2004) They reproduce via broadcast spawning, which is when the organism releases sperm and eggs into the water column. The habitat association with coralline algae begins once the larva settles, usually on encrusting coralline algae. (Pedrotti, 1993) Sea urchins graze at night to avoid predation (Guidetti, 2004) moving from their coralline covered areas to patches of erect foliose that surrounded the encrusting coralline algae. General methods Patterns of habitat association for A. lixula In order to determine if A. lixula has associations with particular habitat forming species, we did urchin surveys at five random study sites to the North of STARESO and four study sites to the South. Within each survey site we counted every urchin we found within two meters of the surface. The sites were picked randomly and varied in size. The size was also picked at random. For each urchin we

4 notated its size, its depth and whether it was found on rock, crustose coralline algae, erect foliose algae or a patch of crustose coralline algae. All of these surveys were taken during the day. Once we established a general pattern of urchin distribution, we looked at survey data taken on the algal cover from the same area (Fields and Hubach 2010).With the algal survey we developed an expected distribution of urchins for various algal groups: erect foliose algae, crustose coralline algae and Posidonia. The algal data was compared to the urchin data using a chi square test to determine if the pattern of habitat use by urchins differed from that expected, based on the overall frequency of the algal groups. In order to test our hypothesis of whether A. lixula is found on coralline due to food preference, we first had to determine if we could discriminate algal species following consumption by urchins. We collected four urchins right before sunrise from the North and within the STARESO harbor, took them to the lab where they were promptly dissected so the digested material would not be expelled or processed further. The four urchins were collected from four different substrates; bare rock, crustose coralline algae, a patch of crustose coralline algae surrounded by macrophytic algae and erect foliose algae. This was to discern if their stomach contents differed depending on their location. From the urchin dissection we assessed the percent composition of the stomach contents by looking at three different 0.4 g samples from each urchin under a dissecting microscope. We placed each sample in a petri dish and broke up the urchin pellets from the gut so as to see the algae more clearly. In order to identify the different types of algae, we created a key based on visual categorization. To help the categorization we used control samples of Posidonia oceanica, various erect foliose algal species and crustose coralline algae that were taken from the bay. Each sample was cut and placed on a slide. We categorized the algal contents based on observation and separated them into different groups labeled A through I. We also categorized the portion of the stomach contents that is digested beyond recognition as fluff. For the purpose of this study, this categorization was more specific than necessary, so for

5 data analysis and comparison they were lumped into three groups of Posidonia, erect foliose algae and crustose coralline algae. As a means for further comparison and categorization of stomach contents, we performed a series of feeding experiments on 16 urchins removed from various locations around STARESO. We separated the urchins equally into four tanks without substrate or food. For two days we did not allow the urchins eat as to empty their gastrointestinal tract so the previous stomach contents would not contaminate the experiment. After two days, we added Posidonia oceanica in the first tank, erect foliose algae to the second tank, Padina pavonica, an erect foliose algae in the third tank, and rocks covered with crustose coralline algae to the fourth tank. We allowed them to feed for one week, then dissected them to compare these known stomach contents to the stomach contents from the nonexperimental urchins that were previously dissected. This was to give us a better understanding of what the stomach contents in the field look like digested. We did a brief survey of the stomach contents of urchins collected after a few days of heavy storms to see if stomach contents differed from urchins collected during calm days. These urchins were found on coralline algae during the night because of the high wave action. According to Bulleri's study, urchins can switch from active foraging to passive feeding on drift algae in barren areas (Bulleri et al, 2002). Although this study was done in areas that were not barren, we did look at urchins during abnormally high wave action from the storm. We dissected two urchins collected from the field and compared their stomach contents to urchins collected when the sea was tranquil. In order to test our second hypothesis; A. lixula is found on coralline as a refuge from harm, we tested urchins ability to grip different substrates by measuring the amount of force required to dislodge them by means of spring dynamometrics. We collected ten urchins from the field, removing them carefully with knifes as not to damage their podia, so that their ability to attach was not impaired for our experiments in the lab. One at a time, we allowed the urchins to settle onto one of three substrates in

6 indoor tanks; rock covered with crustose coralline algae, rock covered with erect foliose algae and bare rock. We made a small net with fishing line that we placed the urchin into before allowing it to settle onto the substrate. Each urchin was given six minutes for attachment (more than six minutes and the urchin would begin to move around, moving the net with it), then attached to net to a spring dynamometer and pulled up until the urchin was dislodged. The force in grams was recorded for each urchin. Each urchin was tested on each substrate, always starting with the macrophyte rock. Experimental trials showed that the least (usually none) podia were damaged when attached to macrophytes, which is why each urchin was tested on macrophytes first. Results The pattern of algal species associations we observed for A. lixula was different from what we expected based on our random surveys of the community (See Figure 1. Chi square = , degrees of freedom = 3, p-value = >.00001). This indicates that the observed distribution of urchins was significantly different from the expected value if they showed no habitat preferences. The available substrates were rock, erect foliose algae and encrusting coralline algae. The expected value however, shows that when compared with percent cover of the rocks, most urchins should be found on foliose algae. We found that the habitat preference was encrusting coralline algae (Figure 3). The majority of the stomach contents we observed consisted mostly of foliose algae. We thus determined that a foliose alga is A. lixula s preferred food source. When compared to community composition, we found that the trends were similar. Foliose algae is the most abundant substrate, and urchins are mainly consuming foliose algae (Figure 4). When stomach contents were compared to urchin location, we found the trends to be opposite. Foliose algae is most abundant, yet urchins are mostly located on encrusting coralline algae (Figure 5) during daylight. Finally, we found that the algal composition of the community was opposing the substrate preference of A. lixula. Foliose algae was

7 most prevalent, yet urchins were mostly found on encrusting coralline algae ( Figure 6). To further confirm that erect foliose algae is the primary food source for urchins, we performed a survey comparing location during the night and day. We observed ten urchins over four days. We found that 92.5% of the time the urchins moved onto erect foliose at night, which is when we expect them to feed, and 97.5% went back to encrusting coralline during the day. This showed that urchins move onto erect foliose algae, their main food source, during the night which is a safer period with a significantly smaller number of predators. They move back to encrusting coralline algae in the morning in order to be on a substrate to which they can attach to more strongly. To test the assocaiton of A. lixula with encrusting coralline algae as a refuge from harm, we tested the stregth to which the urchin can hold onto different substrates. We found that there was a significant difference between the force required to remove the urchins on coralline substrate versus foliose substrate. Our results showed that a force of 2000g was required to dislodge the sea urchin from coralline algae and 350 g for erect foliose algae. This result was significant at p >.0001 (t value=18.45, df=8). Discussion In this study the pattern of association of urchins with their habitat is driven by the sea urchins due to their mobility. The results from the surveys and experiments conducted in this study are to provide reasoning for this association which is hypothesized to be food resources and protection. The algal community composition when compared to substrate associated with urchin locations made clear that urchin location was not by chance, but was selected by preference. The majority of the urchins when surveyed during the day were located on encrusting coralline algae rather than on erect foliose algae, even though the erect foliose algae had the highest percentage of overall cover at 62.40%. This lead to believe that the positioning on encrusting coralline was due to the ability for a stronger hold and

8 therefore protection from predators and environmental factors (Gianguzza et al 2010). When urchins were surveyed at night, they were found on erect foliose algae, which lead to believe that they were found on this substrate at night for feeding purposes( Guidetti 2004). The results from our surveys and experiments helped us conclude that our hypotheses about urchin distribution due to food resources and protection was true. Experimental feeding tests in the lab and the dissections of the urchins helped to identify erect foliose algae as the overwhelmingly dominant food source for urchins averaging 92.62%. As the urchins graze on the erect foliose algae, encrusting coralline algae can take over and dominate the area which is maintained as barren or encrusting coralline due to constant feeding of urchins on the surrounding erect foliose algae. Therefore, the mosaic of pattern patches is due to urchin grazing, leaving areas which Privitera et al describes as barren grounds...with low density and patchy algal cover, dominated by encrusting coralline (2008). In studies that Ruitton et al (1999) and Bulleri et al (2002) conducted they both came to the conclusion that sea urchin grazing on erect foliose algae is what maintains the patched regions and that erect foliose algae is the preferred food source. As a quick comparison to regular conditions, two urchins were dissected that were collected during a large storm that caused an increase in wave action. When the storm urchins were dissected, a new composition of stomach contents were found with a huge increase of mean coralline algae content. The normal percentage of coralline is 6.33%, however, during the storm these urchins had a mean of 41.67% while erect foliose algae had a mean of 23.33%, compared to the normal 92.62%. In a study done by Privitera et al (2008), they studied urchin stomach composition in areas with low abundance and low diversity of foliose algal species and higher wave action. Their results yielded larger amounts of coralline in urchin gastrointestinal tracts, showing that urchins will eat coralline if necessary, but it is not the preferred food source if erect foliose algae is available for consumption. This is important to our study because it shows that erect foliose algae is the preferred food source, but when it is not obtainable

9 either because of abundance or inability to move due to a storm, coralline algae will be consumed. The fact that the two urchins that were dissected had a much higher abundance of coralline algae in their stomach contents during a storm, when the wave action increased dramatically, helps to support the hypothesis that urchins are on encrusting coralline for hydrodynamic purposes. In a study done by Gianguzza et al (2010) they found that urchins were able to hold on stronger and longer to encrusting coralline algae compared to erect foliose algae. This was consistent with what was seen in our experiments where the mean force with which it took to remove the urchins from the encrusting coralline algae was 2000g and to remove them from erect foliose algae was 350g. Knowing that sea urchins feed at night (Guidetti 2004) so they do not have to be concerned about feeding during the day and that they are exposed predators and wave action during the day, it is important that they can hold on to their substrate as well as possible. At night when predators are not as active and they must feed, they can afford to go onto substrates on which it is harder to hold to be able to feed on their preferred food sources. The survey and experiments done in our study, lead to a better understanding of the habitat association that Arbacia lixula has with its environment. The black sea urchins use the habitat in which they live effectively for their needs of food resources and protection. Arbacia lixula uses the surrounding erect foliose algae to feed and the encrusting coralline patches they have helped to create (Ruitton 2000) to protect themselves from predators and wave action. Arbacia lixula perfectly matches the general theory of habitat association where they receive a net benefit from their habitat, provided that Arbacia lixula are the driving force due to their mobility. Habitat associations are important in many biological systems and are pivotal in understanding species interactions and the benefits and costs that the those species receive from their interactions.

10 Works Cited Benedetti-Cecchi, L., F. Bulleri, and F. Cinelli. "Density Dependent Foraging of Sea Urchins in Shallow Subtidal Reefs on the West Coast of Italy (Western Mediterranean)." Marine Ecology- Progress Series 163 (1998): Bulleri, F., L. Benedetti-Cecchi, and F. Cinelli. "Grazing by the Sea Urchins Arbacia Lixula L. And Paracentrotus Lividus Lam. In the Northwest Mediterranean." Journal of Experimental Marine Biology and Ecology (1999): Bulleri, F., I. Bertocci, and F. Micheli. "Interplay of Encrusting Coralline Algae and Sea Urchins in Maintaining Alternative Habitats." Marine Ecology-Progress Series 243 (2002): Fields, S., Hubach, E., The relationship between wave action and algal communities Unpublished Gianguzza, P., Bonaviri, C., Milisenda, G., Barcellona, A., Agnetta, D., Fernandez, T.V., Badalamenti, F. "Macroalgal Assemblage Type Affects Predation Pressure on Sea Urchins by Altering Adhesion Strength." Marine Environmental Research 70.1 (2010): Guidetti, P. Consumers of sea urchins, Paracentrotus lividus and Arbacia lixula in shallow Mediterranean rocky reefs. Journal of Biomedical and Life Science 58.2 (2004): Pedrotti, M.L. Spatial and temporal distribution and recruitment of echinoderm larvae in the Ligurian Sea. Journal of the Marine Biological Association of the United Kingdom 73. (1993): Privitera, D., Chiantore, M., Mangialajo, L., Glavic, N., Kozul, W., Cattaneo-Vietti, R. "Inter- and Intra- Specific Competition between Paracentrotus Lividus and Arbacia Lixula in Resource-Limited Barren Areas." Journal of Sea Research 60.3 (2008): Ruitton, S., P. Francour, and C. F. Boudouresque. "Relationships between Algae, Benthic Herbivorous Invertebrates and Fishes in Rocky Sublittoral Communities of a Temperate Sea (Mediterranean)." Estuarine Coastal and Shelf Science 50.2 (2000): Smith, A.B. "Peristomial tube feet and plates of regualr echinoids." Zoomorphology 94.1 (1989)

11 STARESO Marine Research Station, study site in Calvi, Corsica, France. Figure 1:

12 Figure 2: Algal study sites

13 Figure 3: Shows the comparison between the percent algal cover and the substrate on which A. lixula is found. Figure 4: A comparison between the stomach contents and substrate associated with urchin locations of A. lixula.

14 Figure 5: A comparison between algal composition of the community and the stomach contents of urchins. Figure 6: A comparison between substrate associated with urchin locations and the algal composition of the community.