SPIDER CRABITAT IN THE KELP FOREST: A TEMPORAL COMPARISON OF MICROHABITAT PARTITIONING OF SPIDER

Zoe Scholz, Adri Sparks, and Henry Vogt Kelp Forest Ecology, UCSC 2015

Abstract One longstanding question in community ecology is how pervasive and persistent habitat partitioning is as a mechanism of species coexistence and the maintenance of biodiversity. We studied habitat associations of five spider species of the family Majidae and how these habitat associations differed among species in a kelp forest in central California. To determine if these patterns of partitioning were persistent over time, we compared our results to a previous study of the same system conducted 32 years earlier. Our approach was to compare habitat use of each species with the relative availability of each habitat to quantify habitat associations and to compare those associations (i.e. disproportionate occurrence) among the five species to test for partitioning. Habitats were distinguished by the cover of and algal taxa and substratum type and relief. We found that there were strong associations between some species and particular habitats as well as similar species habitat associations between our study and the previously conducted study. Crabs exhibited associations with algal taxa that differed among the four species encountered. Our results indicate that spider crabs in Central California kelp forests partition their benthic habitat and this pattern of habitat partitioning might persist for decades. Our work adds to the many other studies that provide evidence for habitat partitioning as a mechanism of species coexistence.

Introduction A fundamental question in ecology is how so many seemingly similar species are able to coexist in a community (Hutchinson 1959). Two hypotheses to explain the maintenance of diversity are niche diversification and resource partitioning (Schoener 1974, Hutchinson 1959), where otherwise similar species are able to divide their habitat and resources to the point that competition with similar species is avoided (MacAurthur 1958). For habitat partitioning, the species should exhibit strong habitat associations, and those associations should differ among the species, such that they avoid competing for the same resources. In addition, for resource partitioning to promote coexistence, those habitat associations need to be persistent through time. However, rarely have studies of resource partitioning been repeated over time to evaluate the persistence of observed patterns of partitioning (Wiens 1977).

Kelp forest communities in coastal temperate waters are known for their great species diversity (Carr and Reed 2015). A conspicuous component of these communities is the diverse assemblage of the spider crabs of the family Majidae. Within a kelp bed there can be five or six species co- occurring. We looked at the spider crab family Majidae, a well diversified crab family in the temperate kelp forest. Such species diversity in such a small spatial context could cause significant interspecific overlap in habitat, creating an ideal environment for resource partitioning. We examined the habitat associations between five species of spider crab: Scyra acutifrons, Pugettia richii, Pugettia producta, Pugettia (formerly Mimulus) foliatus, and Loxorhynchus crispatus in the kelp forest and what type of substrate they associate with. By looking not only at where these species associate, but also what the overall substrate composition of the studied kelp forest is, we can get an accurate picture of what type of substrate these species prefer, and if they are disproportionately associating with a particular substrate, showing that they have a defined substrate niche. In addition, we compare the observed patterns of habitat partitioning with those described with a previous study 32 years prior.

Our questions therefore are two-fold. First, do the five species of spider crabs exhibit habitat associations and are they distinct among each other. Our second question is if these associations persist over time. Hines (1982) provides data regarding the habitat associations of our target species, however no study has been repeated to determine how consistent his observed patterns are, making our study a useful link in the long term observations on the Majidae species’ habitat associations.

We found the comprehensive study of Majidae at Hopkins Marine Station by Hines (1982) a good conceptual framework for our own study, helping guide what kind of questions would be valuable to ask as well as how we might conduct our study. Our findings were compared solely to this study as there was a lack of literature pertaining to spider crab habitat patterns in temperate kelp forests. He examined the differences in microhabitat use, population cycles, carapace size, diet, and predators between the same Majidae species we looked at. Due to restrictions in both time and resources we augmented our study to more accurately fit our question. Replicating Hines (1982), focusing on habitat associations, provides us with valuable insight into whether observed habitat associations of these species have persisted over time.

Methods General Approach There are two components to our study: a survey of spider crab species and their associated habitats, and comparing this data to a previous study by Hines, 1982. To accomplish this, we conducted observational field studies at Hopkins Marine Station in Pacific Grove, CA (36"36'N, 12 1°54'W). We conducted swath surveys at intervals throughout the middle of the kelp forest to collect both crab and habitat data. During our first surveys we identified spider crab species and took habitat data surrounding each crab. During our second round of surveys, we collected general habitat data, uncoupled from the crabs, in order to determine available substrate. This allowed us to see if crabs were disproportionately associating with certain habitat types. To compare our study to Hines’ we used similar habitat categories, which included algae, invertebrates, and physical substrate characteristics.

System Description Kelp forests are highly productive and species-rich ecosystems. Like other terrestrial and marine systems, it is important to understand what factors allow species to coexist in a given environment. This is especially pertinent to kelp forests because they are home to a staggering diversity of species. One factor that may contribute to the maintenance of diversity is resource partitioning by species habitat associations.

The kelp forest at Hopkins Marine Station is a Giant Kelp, Macrocystis pyrifera, forest. The substrate is characterized by high relief granitic reef outcroppings intermixed with beds of sand and shell hash. The inshore side of the reef has areas dominated by leafy red and articulated coralline algae, and slopes up to a zone of Phyllospadix surfgrass in the shallows. In the middle of the reef, Macrocystis, some understory algae, and many benthic invertebrate species cover the rocks, while the sandy areas are home to Diopatra beds and some other invertebrate species. The outer edge of the forest abuts a sand channel at a depth of about 40 ft. The number of habitats formed by the varied topography and different algae and sessile invertebrate species, makes Hopkins an ideal site for studying microhabitat associations of mobile invertebrates.

Study Design Our study aims to address the following two hypotheses:

1) Spider crab species at Hopkins Marine Station exhibit habitat associations and these associations differ among species. To determine if the spider crab species included in our study have disproportionate associations with certain microhabitat types, we used swath and UPC surveys. Habitat use was measured by encountering individuals of each species on random transects and recording their surrounding habitat in 0.25m2 quadrats. Habitat availability was measured by recording habitat attributes in randomly distributed 0.25m2 quadrats. The swath survey allowed us to find the crabs and identify the surrounding habitat, while the UPC habitat survey gave us available habitat types and how often they occurred. Assuming there is no habitat association, the crabs should be found on habitats proportionate to what is available. Using PERMANOVA analyses on this data, we were able to see if all the spider crab species, as one group, were found disproportionately on certain habitat types. A P-value of <0.05 rejects our null hypothesis and confirms that there are significant habitat associations. Using Non-metric MDS plots and Pair-Wise analyses, we are able to compare habitat usage between each species, and determine if certain species associate more strongly with certain habitats. Again, P-values of <0.05 mean there is significant evidence to reject the null hypothesis that there are no differences in habitat associations between species. All statistical analyses were conducted with PRIMER-E version 7.

2) These patterns persist over time, in that our findings will be similar to the previous study by Hines, 1982.To compare our data to what Hines presented in 1982, we used the same swath data as the previous hypothesis. Hines’ microhabitat data was presented in bar graphs of how often he found each species in each habitat category. Because we used similar habitat categories, we were able to quantitatively compare our data with his. We were not able to run statistical analyses on how significant our comparisons are because of differences in sampling methods, but we were able to visually compare the data and consider how Hines’ observations contrast or match the results of our study.

Data Collection Swath and UPC surveys were conducted on SCUBA at Hopkins Marine Station during the month of November, 2015. All transects were perpendicular to the permanent cable, which runs approximately North-South through the middle of the kelp forest (Figure 1). We spaced transects at intervals between the 100 and 150 meter mark. Inshore transects ran East, and offshore ran West. Swath surveys were 2m by 10m, and UPC surveys were run along 10m segments as well. The majority of the transects sampled directly off the cable, from 0-10m, while some were conducted at 10-20 meters off the cable, allowing us to reach depth zones of 6-12m. During the swath surveys, we looked for the five target spider crab species. When one was identified, we randomly placed a .25m2 gridded quadrat over the crab. Under each of the 16 intersections on the grid we noted the habitat category. This gave us a bigger picture of what surrounded the crab, as compared to just taking habitat data directly under the crab. For the UPC surveys, we used the same gridded quadrat technique along the same eight transects, so we would be able to accurately compare our data. The quadrats were placed at predetermined intervals along the transects and four quadrats were done per 10 meter transect.

Results General Results We identified a total of 64 spider crabs during our survey. Only four of the five target species were found—no Pugettia producta were seen on our transects. Loxorhynchus crispatus and Pugettia richii were the two most prevalent species in our study area.

1) Spider crab species at Hopkins Marine Station exhibit habitat associations and these associations differ among species. Results from the UPC surveys, denoted as “available habitat” show sand/shell hash, coralline algae, and low red algae as the most common habitat categories in our study area (Figure 2). Habitat data collected around the crabs show that P. richii and P. foliatus were both found a majority of the time in coralline algae. Scyra acutifrons and Loxorhynchus crispatus were found around both coralline and low red algae. A PERMANOVA analysis shows that the species, as a group, disproportionately associate with certain habitats, as compared to how often the habitats are available in the study area [p-value 0.001]. Looking at differences in habitat associations between species, the data shows P. richii is the only species regularly found near Cystoseira, a brown macroalgae (Figure 2) Also, S. acutifrons were most often found in the presence of other invertebrates. A Non-metric MDS plot confirms that all species are different from the expected background data, and shows that S. acutifrons and L. crispatus have some overlap in habitat associations (Figure 3). Pair-wise tests show that each species is significantly different than the expected background data [p-values less than 0.05] (Table 1). They also show a significant difference in habitat use between L. crispatus and P. richii [p-value 0.001] and S. acutifrons and P. richii [p-value 0.008].

2)These patterns persist over time, in that our findings will be similar to the previous study by Hines, 1982. Comparing our results to those presented by Hines in 1982, we can see that there are differences in the overall number of species found as well as which species were most numerous. Hines found primarily P. richii and P. foliatus, at 36% and 34% of individuals found respectively, while we saw mainly L. crispatus at 33% and then P. richii and S. acutifrons at 28% and 25% respectively (Figure 4). Comparing observed habitat associations, our results for P. richii are similar to Hines when looking at the three main habitats they were found on: Cystoseira, coralline, and low red algae (Figure 5). Results for P. (Mimulus) foliatus differ in that Hines primarily found this species on kelp holdfasts, while we saw them in coralline algae. Hines’ data on S. acutifrons shows them primarily in crevices, though this matches our personal observations, it is not shown in our data, the reasons for this we will discuss later. As for L. crispatus, Hines found most of them in crevices, on invertebrates, and in low red algae, while the largest categories we saw them in were coralline and low red algae.

Discussion Habitat partitioning by the spider crab assemblage at Hopkins supports previous theories of niche partitioning between similar species (Schoener, 1974). The non-random distribution of the species studied was established in an earlier study (Hines, 1982) and our results indicate similar patterns of habitat partitioning 32 years later. Spider crabs exhibited distinct and strong habitat selection with respect to algae cover, invertebrate presence, and rugosity of the substratum. These results lead us to conclude that the spider crabs partition their habitat and this partitioning persists over time.

Some species demonstrated greater divergence from the expected cover than others (i.e. stronger habitat associations). One example of this difference was between P. richii and C. osmundacea. Our data indicated that P. richii had one of its strongest habitat association with C. osmundacea. Prior studies have yielded similar results (Aris et al. 1982, Hines 1982), reinforcing the validity of the data we collected. In contrast, L. crispatus exhibited the least divergence from the available habitat but still showed significant variation overall (Table 1).

We also found some species to have greater overlap in habitat utilization, namely L. crispatus and S. acutifrons, but even M. foliatus and P. richii were undeniably similar. Hines (1982) suggested that similarities between L. crispatus and S. acutifrons are likely an artifact of not differentiating between individuals found exposed on the surface of substrata vs in it (ie in cracks and crevices). We made similar personal observations of these two species whereby L. crispatus occurred more often exposed on the surface, whereas S. acutifrons was more often observed in cracks and crevices. This is likely because L. crispatus grows far larger in body size and as defense against predators decorates its carapace with unpalatable organisms to appear less appetizing to potential predators (Hultgren and Stachowicz 2011). Meanwhile S. acutifrons relies on cracks, crevices, and even the inside of some invertebrates as refuge, and a more detailed survey methods might have accounted for the discrepancies (Abele 1974).

Hines noted P. foliatus had the greatest microhabitat niche breadth, but associated most frequently with Macrocystis pyrifera holdfasts. In contrast, we found P. foliatus most often near coralline algae and never around M. pyrifera holdfasts. The reason behind the stark difference is unclear. The majority of differences between our results and Hines’ can be explained by the differences in sampling methods: Hines recorded solely below each crab while we took 16 data points around each crab, as we sought to account for individuals moving around within their niche. We also had less time to survey (four weeks as opposed to three years) in addition to less bottom time (maximum of 60 minutes as opposed to 90), so it is likely our surveys missed the smallest Majidae hiding in M. pyrifera holdfasts. We also saw a decrease in M. pyrifera this season (personal observation), so it is possible other species have begun to occupy a disproportionate amount of this biohabitat meanwhile pushing P. foliatus out.

In contrast to the previous study, in 2015 we found no P. producta on our transects. We believe this is due to some discrepancies in survey locations. Our methods entailed surveys within the kelp forest and 2 meters off the floor up a M. pyrifera plant, while Hines reported most P. producta findings in the Phyllospadix zones and kelp canopy. Coincidentally, most days we surveyed had large swells, but this did not seem to bring P. producta into deeper water or off the kelp canopy.

Some variation in our results compared to the prior study could have been eliminated if we had chosen to match the prior methods. If this study is to be replicated in the future to further strengthen our understanding of spider crab ecology, some aspects of the techniques should be adjusted. We propose differentiating between occupying space on top of a habitat versus inside. In addition, we may have identified stronger associations with greater resolution of the taxa and greater characterization as well. We also suggest using the original dimensions and breadth from the 1982 survey, looking in shallower zones as well as the entirety of kelp plants within the study areas. It should also be noted that both studies were conducted during El Niño years (1982-83 and 2015), and it would be useful to conduct a similar study during non El Niño years.

The results of this study demonstrate the temporal and spatial complexity of Majidae habitat distribution. These observational studies have reinforced theories of niche partitioning but suggest refinement of survey methods. Given the extremely high biodiversity of Macrocystis pyrifera kelp forests (Carr and Reed 2015), understanding the links between species and how they interact with phylogenetically close species is important for preservation of relevant habitat as well as further deciphering the complex interactions that make up the diverse kelp forest ecosystem.

Acknowledgements We thank our professors Dr. Mark Carr and Dr. Pete Raimondi for their advice and support through the project. We also thank the teaching assistants Rachel Zuercher and Kat Beheshti for all their aid throughout the term. We are grateful to staff at Hopkins Marine Station for use of their space and marine reserve.

References

Abele, L.G. 1974. Species diversity of decapod in marine habitats. Ecology 55:156- 161. Aris, J.P., A.D. Eisemann, and L. Moulton. 1982. The occurrence of Pugettia richii (Crustacea: ) on Cystoseira osmundacea follows a diel pattern. 32:243–249. Carr, M.H., and Reed, D.C. 2015. Shallow Rocky Reefs and Kelp Forests. Pages 311-336 in: H. Mooney and E. Zavaleta (eds) Ecosystems of California. University of California Press, Oakland, California Carr, M.H. 1989. Effects of macroalgal assemblages on the recruitment of temperate zone reef fishes. Journal of Experimental Marine Biology and Ecology 126:59–76. Carr, M.H. 1991. Habitat selection and recruitment of an assemblage of temperate zone reef fishes. Journal of Experimental Marine Biology and Ecology 146:113–137. Hultgren, K.M., and J. Stachowicz. 2011. Camouflage in decorator crabs: integrating ecological, behavioural and evolutionary approaches. Pages 214-238 in: M. Stevens and S. Merilaita (eds) Animal Camouflage. Cambridge University Press, Cambridge, United Kingdom. Hutchinson, G. E. 1959. Homage to Santa Rosalia or why are there so many kinds of ? American Naturalist 93:145–159. Hines, A.H. 2015. Coexistence in a kelp forest: size, population dynamics, and resource partitioning in a guild of spider crabs (Brachyura, Majidae). Ecological Monographs. 52:179– 198. MacArthur, R.H. 1958. Population ecology of some warblers of northeastern coniferous forests. Ecology. 39:599–619. Schoener, T.W. 1974. Resource partitioning in ecological communities. Science. 185:27–39. Wiens, J.A. 1977. On competition and variable environments. American Scientist. 65:590–597.

Table and Figures

Table 1: Pair-wise tests run using PERMANOV between each species and the expected background data. P-values of <0.05 mean habitat associations between that pair are significantly different.

Figure 1: Map of Hopkins study site with permanent cable and meter marks. Red arrows indicate transect sites.

Figure 2: The percentage of each species found with each type of habitat. The bottom bar graph shows the expected habitat categories, assuming no association. This is based on background UPC data, which shows the percentage of available habitat types in the study area. Non-metric MDS Resemblance: S17 Bray-Curtis similarity 2D Stress: 0 Species Loxorhynchus crispatus Scyra acutifrons Mimulus foliatus Scyra acutifrons Pugettia richii ExpectedAvailable

Loxorhynchus crispatus

Pugettia richii

ExpectedAvailable Mimulus foliatus

Figure 3: A Non-metric MDS plot, which acts as a visual representation of how similar habitat usage is between species. Points that are closer together have more overlapping habitat use, while points that are farther apart use different habitat types. For the significance of these distances see pair-wise tests in Table 1.

P. Scholz, Sparks, and Vogt 2015 Hines 1982 producta L. 4% crispatus 6%

L. P. richii S. P. richii crispatus 28% acutifrons 36% 33% 20%

P. S. foliatus P. acutifrons 14% foliatus 25% 34%

Figure 4: Pie graphs comparing percentage of each species found in Hines 1982 (left) and our study (right). Number of each species found can be seen in Figure 4. P. richii N=18

P. (Mimulus) foliatus N= 9

S. acutifrons N=16

L. crispatus N=21

Figure 5: Comparing Hines 1982 data (left) to our study (right). Graphs show the percent each species was found on each habitat category. Note that some habitats have been omitted from our study and that no P. product was found in our study.