Title 3/4 It Read More Like a News Title and Was Overly Dramatic, but Otherwise Had The

Total score: 70/100

Title [[3/4 – it read more like a news title and was overly dramatic, but otherwise had the right concepts]] Inextricable links found between physical and biological habitat and their influencing influence on species abundance in a California kelp forest.

Zach Randell

Abstract [[not required but this is pretty good, you could improve by having the first sentence introduce the broad ecological questions that you introduce in your intro]]

Subtidal invertebrate and algae observations at Hopkins Marine Station investigated [the observations didn’t investigate] the presence, strength and relative importance between of physical and biological habitat upon in determining swath species abundance [what’s a swath species]. Bray-Curtis dissimilarity matrix compared swath observations with substrate, relief and percent coverage habitat characterization data previously gathered at the same study site. Physical habitat explained 76% of variance while biological associations accounted for 24%. Varying strengths of associations were found post species-habitat and species-species analysis. Biological associations are themselves a product of habitat interactions and therefore limit the ability to draw finite conclusions. Long term observation and select experimental manipulations will allow specific mechanisms supporting discovered associations to be unraveled.

Clarity [[12/14- work on connecting the dots so that multiple sentences work together to build ideas. Also work on cutting out extraneous words and tightening sentences to give your ideas more oomph. Work on clarifying the main points and bringing them to the top of each section or paragraph so that your writing has more direction; I feel like I get lost in some of these sections because you don’t clearly orient me. Outlining things might help a lot!]]

Introduction [[13/20 – you got the broader ecological context, but failed to explain each of the theories of how diversity is maintained. You don’t need to go into lots of depth, but you do need to give a little explanation. Also could be improved by a slightly more in-depth articulation of the specific questions for your study and a clearer description of why it’s a good study system as well as the novelty of the project.]]

An important goal of ecology is to try to understand mechanisms maintaining species diversity. Similar species are observed to thrive in rich communities without inter-specific competition driving competitive exclusion. Many models have been proposed and appropriate application differs between communities and the life history traits of those that inhabit them. The gradual change hypothesis aptly applies to marine larvae and freshwater lake organisms [you should explain this example more or exlude]. Continuous gradual change of physical and biological factors prevents one species from becoming competitive dominant. (Connel 1978) The intermediate disturbance hypothesis states species diversity will be maximized where physical or biological perturbations are neither too frequent nor too rare. Forest fire for example removes low diversity old growth terrestrial forest regions allowing succession and subsequent growth of previously inhibited species. Note this terrestrial example borrows components of the storage effect hypothesis because early successional species must maintain an adult population or seed bank until favorable conditions allow growth. The vast complexities of ecological dynamics limit any one model from universal application. [[good analysis, but a little bit longer than needed and not clearly setting us up for YOUR questions]] The niche diversification hypothesis limits inter-specific competition between similar species because natural selection drives a partitioning of resource use and thus a division of their realized niche. Controversy surrounds this hypothesis due to documentation of unspecialized organisms thriving in rich communities. Seed dispersal and successful growth was found to be higher for unspecialized plant species (Cancella 2002). For other organisms, such as herbivores specialized for feeding on specific plants, niche diversification appears plausible (Daugherty 2009). [[you’ve got the examples, but you haven’t really explained to me what niche diversification is!]] To better understand how specialized and non-specialized species partition resources we must investigate a highly diverse ecosystem. Kelp forests are rich marine communities supporting an impressive array of fish, algae and invertebrate species. The three dimensional biogenic habitat created by giant kelp (Macrocystis pyrifera) provides settlement for larvae completing the first stage of their bipartite life cycle who in turn attract a host of predators. Massive growth paired with seasonal turnover provides a plethora of organic material for grazer and scavenger composition (Duggins 1989). [[but make sure you’re direct about what makes kelp forests good for this kind of study, all you’ve really explained is that they’re cool]] Humans enjoy many products and services produced by the kelp forests. Aesthetic pleasure bolsters both the peace of mind and coffers of those living in coastal communities. Kelps forests also act as a supporting system for oxygen production, carbon sequestering, nutrient cycling and water cycling. Urchin, abalone, fish and kelp are all harvested and therefore require accurate habitat knowledge for effective stock preservation. To better manage and protect this ecosystem and all the services it provides to us, our study aims to better understand species associations with physical and biological habitat. We will determine the presence and strength of species associations with variable physical habitat. Next we investigate the effect of sessile and encrusting biology on swath species abundance. As before, association strength will be assessed. Finally, we determine the relative importance between physical and biological habitat for predicting community composition. [[you could elaborate on these questions a bit more]]

Methods [[12/18 look back at the directions I gave you last time about how to structure this section. You didn’t give me a general approach or describe your methods as they related to the specific hypotheses.]] SCUBA allowed us to sample a giant kelp forest (Macrocystis pyrifera) community at Hopkins Marine Station. Residing just inside the southern region of Monterey Bay, (36° 37’ 17.02” N, 121° 54’ 07.28” W) Hopkins allows investigate into habitat effect on species abundance due to the high diversity of species found upon differing benthic composition (Bodkin 1988 Braken et al. 2004). Granitic rock of varying physical structure interrupted by sporadic sand patches provides habitat for a diverse assemblage of fish, invertebrates and algae. Seasonal upwelling provides abundant nutrient delivery and thus habitat for recruitment drives interspecific competition in benthic species (Watanabe 1984). A previous study recorded habitat composition and structure while quantifying sessile invertebrate and algal percent coverage. Strong spatial associations between species and habitat structure highlighted the importance of physical substrate and structure formed for abundance and distribution of the primary substrate holder. Building upon these results we returned to the same study site to sample abundance of conspicuous algae and invertebrate species to better understand habitat associations. [[pretty good site description]]

Ten pairs of divers performed swath invertebrate surveys off of a permanent transect cable (Fig. 1). Mobile and conspicuous invertebrate and algal species were counted to determine abundance (Table 1). Survey data allowed us to look for associations between swath species abundance and specific habitat characterized by our recent survey. Previously, uniform point contact surveys (UPC) required observers to note substrate, physical relief, primary substrate holder and drift algae/laminarial presence for six 2.5 meter stretches, with 5 points within each 2.5 meter increment. A total of 240 points were gathered for a single transect with 4,800 points gathered for all 20 transects. 600 square meters of benthic habitat was classified.

Following that study we worked in teams of two along the cable and located a pre-assigned meter marker (90 m – 135m, 5m increment, 10 tie-off points total) indicating the appropriate place to initiate sampling. Each buddy pair performed two transects over two dives. Divers used a 30 meter tape to sample offshore (90°) and inshore (270°) of their respective meter mark. Each buddy sampled one side of the meter tape (1m x 30m). As with UPC surveys we split each transect into six sequential five meter segments (20 transects, 120 segments, each segment 10 square meters). This permitted a smaller scale of resolution for data analysis as we compared swath species in one segment to the habitat previously classified in that exact segment. Mirroring the protocol from the previous habitat study allowed a precise comparison between swath and UPC data. [[too much detail too early in the methods]]

Fig. 1 – Permanent transect location at Hopkins Marine Station, Monterey CA Transect data for each survey (swath, UPC) was grouped by segment with each species receiving a unique code. The Bray-Curdis similarity/dissimilarity matrix allowed species abundance to be grouped into a comparison friendly format. Euclidean analysis clumped environmental variables (UPC) into a similar matrix. Finally, the Spearman method allowed rank correlation comparisons between the two matrixes. Evidence supporting species-habitat and species-species associations would manifest as a shift in species abundance matching a similar shift in habitat or percent coverage composition. Our null hypothesis states that species abundance remains independent of physical and biological habitat variation.

Results [[10/16 - try organizing by hypothesis in a way that’s clear and tells me whether each hypothesis is supported or refuted. Also general results are helpful and you need more information in your figure captions]]

Different species-habitat associations were found between algae and invertebrate species. Both algal species sampled were significantly associated with bedrock and shallow relief (Fig. 2). Unlike algal associations, invertebrate associations varied between and among species with similar life history traits. The giant acorn barnacle (Balanus nubilus) was associated with high relief that was absent of algal presence, while the stalked tunicate (Styela monterey) shared spatial habitat with algae species on shallow bedrock. Both sessile invertebrates rely on the availability of organic matter in the water column, yet one successfully recruits alongside algae and one does not. These associations indicate habitat utilization differs among species. Different strengths of association were found between species and habitat. Pisaster giganteus had strong positive and negative associations compared to the relative weak associations displayed by Patiria miniata (Fig. 3). The echinoderms are similar yet our results indicate strength of association with habitat does indeed vary among similar species. Species-species associations were discovered post data analysis. Notably, Cystoseira osmundacea was found to have positive associations with seven categories of red, brown and coralline algal species. Macrocystis pyrifera displayed two weak algal associations (Fig. 5). These results confirm both the presence and difference of species-species associations. Different strengths of species-species associations were found, however, no discernible patterns or mechanisms supporting our findings explained the differing strengths. For example, Macrocystis pyrifera displayed a surprising correlation strength of 0.55 with solitary tunicates. This single result aside, the lack of sensible patterns preventing conclusions for the explanation of strength variations was not anticipated (Fig. 5) Species-habitat associations were found to explain 76% of swath species abundance variation opposed to the 24% explained by species-species associations. Our results therefore indicate physical habitat is roughly three times more important to understand swath species abundance in the sampled kelp forest. Discussion [[14/22 - you’ve got a lot of great stuff here in terms of proposed mechanisms for the associations you’re seeing, but the discussion is suffering from a lack of structure and coherence. You could really improve this by creating subheadings for each hypothesis and then structuring your discussion so that it directly addresses the hypothesis/question. Also link back to the big ecological questions from the intro very explicitly]]

Swath species associations with habitat were found to vary between algae and invertebrates and within similar invertebrate species. Our previous study found strong associations between algael associations onand bedrock and shallow relief while the invertebrates occupied high relief. Save for Styela montereyensis, swath algae and the remaining sessile invertebrate species were found to maintain the observed habitat partitioning. Maximization of light exposure is likely achieved through algal recruitment upon flatter surfaces. Regions of high relief are likely shaded for parts of the day as the sun traverses the sky. Algal settlement to regions of high relief, if present, may be outcompeted by invertebrates or fail to mature due to insufficient light exposure. Lack of strong invertebrate association on low and medium relief is either due to competition with algae or to specific spatial habitat utilization in response to life history requirements. Invertebrates outcompeted by algal species on flatter surfaces may be restricted to regions of high relief less desirable to the dominant algal competitors. Habitat with high relief likely experiences greater water flow due to the channeling of water around the obstruction. Stylaster californicus, while absent from Hopkins, is an example where very high water movement is required for successful recruitment. (Love et al, 2010) A pluralistic experimental design with algae removal (and controls), invertebrates, varying light exposure and varying water movement may help to determine factor(s) driving the mechanism behind the observed differences of habitat utilization. Whatever the mechanism, benthic substrate with varied relief was found to support greater diversity compared to uniform substrate. Styela montereyensis violates the observed relief partitioning and was found to associate with shallow bedrock (fig. 4). Strong positive associations within the previously exclusive algal habitat indicate S. montereyensis has a competitive edge enabling co-existence among algal populations. Specialization of feeding structures has been shown to increase feeding efficiency and expand habitat utilization (Daugherty 2009). A long stalk extends the solitary tunicates’ siphon above the thick fleshy red understory. Balanus nubilis, while impressive in girth, lacks the vertical growth needed to penetrate the understory canopy. Water flow delivering crucial organic matter to sessile filter feeders may be inhibited beneath the extensive understory canopy. The stalked tunicate’s specialized feeding structure allows utilization of habitat that is free of other similar sessile filter feeding species. This is clear evidence for specialization allowing different habitat utilization. As recruitment space is a limited resource in benthic communities, the lack of other sessile filter feeders associated with Steyla’s habitat indicates inter-specific competition is limited and thus niche diversification is supported. Furthermore, conclusions regarding spatial habitat utilization must be made on a case by case basis as sweeping generalizations are likely to overlook specific species specializations. Strengths of species associations with habitat were found to vary between two similar species. Patiria miniata displayed weak interactions compared to the several strong interactions displayed by Pisaster giganteus (Fig. 5). The difference in habitat associations may indicate a partitioning of benthic space and thus the avoidance of inter-specific competition. Life history differences may explain the observed habitat partitioning. Patiria scavenges across all substrate and most relief opportunistically and without preference. The lack of strong associations paired with substantial abundance indicates Patiria roams across the benthic indiscriminately. In contrast, Pisaster was found to exhibit strong positive and negative associations with substrate. Specific predation by Pisaster has been documented and may thus explain specific habitat preference where prey is most abundant (Paine 1966). In short, differing behavioral preferences between similar species were found to yield different strengths of habitat association. This indicates the presence of habitat partitioning and therefore serves as evidence for niche diversification between similar species within a diverse ecosystem.

We found multiple species-species interactions. Cystoseira displayed positive associations with seven categories of red, brown and encrusting algae. In contrast, Macrocystis was found to only associate with two algal groups (Fig. 5). Maximizing light exposure allows Macrocystis to grow at an unprecedented rate, often culminating with a thick shading canopy on the surface of the water. This has been shown to negatively affect successful recruitment for several species of brown algae in Stillwater Cove, CA (Reed 1984). However, the large size of kelp forests results in a tradeoff between light absorption and force of drag acting upon the forests. Physical forces acting to remove Macrocystis result in a high turnover rate and thus species inhibited by canopy shading persist. The large abundance of understory canopy associated with non-light inhibiting Cystoseira support ample light availability and therefore a higher density of understory algal species in the absence of Macrocystis. The lack of algal presence associated with Macrocystis supports current thinking that giant kelp inhibits understory algae until disturbances allow successful recruitment. Our results indicate biological associations influence habitat use, yet we must remember that physical factors determined where Macrocystis could recruit and in turn affect other species. Perhaps one key factor maintaining high species diversity in kelp forests is rapid turnover paired with natural selection driving species to maximize their recruitment in wake of the spatial and temporal instability of benthic habitat. Long term subtidal observations in fixed kelp forest regions may provide further insight into the nature of species abundance fluctuations in response to a Macrocystis canopy.

A variety of association strengths were found for species-species interactions. Regrettably, clear patterns did not support known species behaviors nor offer logical insight into new associations. Macrocystis pyrifera displayed an association strength of 0.55 with solitary tunicates (Fig. 5). In context, the next highest Macrocystis association strength was 0.15 for encrusting red algae. (Greater than 0.10 is considered significant.) Interestingly, only two solitary tunicate observations determined this result. Therefore, more data is needed to bolster our pool of observations and allow accurate patterns to manifest and logical inferences into the nature of species-species association strength variation to be drawn. We found physical habitat explained 76% of swath species variance opposed to the 24% explained by UPC species. Statistically, physical habitat is roughly three times a better predictor of swath species abundance. Clear physical habitat associations were discovered yet some of those associations were a direct response to biological pressure. If the observed sessile invertebrate association with high relief is due to competitive restrictive zonation than it must be true that biological factors instigated the physical habitat partitioning. Styela monterensis offered an exception as specialized feeding structures allowed habitat utilization free from similar species. Did inter-specific competition from like species fuel the specialization allowing new habitat utilization? Perhaps new algal competitors simply failed to restrict existing solitary tunicate populations and the observed association is simply with physical relief. In either case, the intrinsic link between physical and biological habitats of the kelp forest play off of one another, resulting in species associations whose origins are difficult to state conclusively. While relatively easy to observe and analysis, understanding the mechanisms driving observed associations requires long term observations and select experimental manipulations. Herein lays a key piece required to further understand processes acting to encourage and maintain species diversity. Patiria miniata L. crispatus/Scyra Dermasterias imbricata acutifrons Cryptic Henricia spp. Decorators Blood Star Mimulus foliatus Orthasterias koehleri Balanus nubilus Rainbow Star Cryptochiton stelleri Mediaster aequalis Gumboot Chiton Red Sea Star Crassadoma gigantea Pisaster brevispinus Rock Scallop Pisaster giganteus Haliotis - ID species Red, Flat or Pinto Pisaster ochraceus Abalone Pycnopodia helianthoides Megathura crenulata Sunflower Giant Keyhole Limpet Urticina lofotensis Lithopoma gibberosa Urticina piscivora Red Turban Snail Anthopleura sola Kelletia kelletii Strongylocentrotus Kellet's Whelk purpuratus Purple Urchin Ceratostoma foliatum Stongylocentrotus Leafy Hornmouth franciscanus Red Urchin Cypraea spadicea Cucumaria miniata Chestnut Cowry Parastichopus californicus Tethya aurantia Parastichopus parvimensis Orange Puff Ball Cancer spp Styela montereyensis Pugettia producta Stalked Tunicate Kelp Crab Stylaster californica Loxorhynchus grandis Cystoseira

Table 1 – Invertebrate and algae species counted on swath survey. [[this caption should be above the table per Mark’s instructions]] CYSTOSEIRA MACROCYSTIS_PYR- 0.3 0.3

0.2 0.2

0.1 0.1 N N O O I I T T

A 0.0 A 0.0 L L E E R R

R -0.1 R -0.1 O O C C -0.2 -0.2

-0.3 -0.3

Substrate or Releif Substrate or Releif BALANUS_NUBILUS STYELA_MONTEREY- 0.3 0.3

0.2 0.2

0.1 0.1 N N O O I I T T

A 0.0 A 0.0 L L E E R R

R -0.1 R -0.1 O O C C -0.2 -0.2

-0.3 -0.3

Substrate or Releif Substrate or Releif CRYPTOCHITON_ST- LITHOPOMA_GIBBE- 0.3 0.3

0.2 0.2

0.1 0.1 N N O O I I T T

A 0.0 A 0.0 L L E E R R

R -0.1 R -0.1 O O C C -0.2 -0.2

-0.3 -0.3

Substrate or Releif Substrate or Releif PATIRIA_MINIATA PISASTER_GIGANT- 0.3 0.3

0.2 0.2

0.1 0.1 N N O O I I T T

A 0.0 A 0.0 L L E E R R

R -0.1 R -0.1 O O C C -0.2 -0.2

-0.3 -0.3

Substrate or Releif Substrate or Releif

Fig. 2 – Swath species associations with physical relief and substrate.[[ need more details about what this shows]] SPECIES_2$ PATIRIA_MINIATA 0.3

0.1 C o r r

0.0 e l a t i -0.1 o n

-0.4 PISASTER_GIGANTEUS 0.3

0.1 C o r r

0.0 e l a t i -0.1 o n

UPC Species

Fig. 3 – Patiria miniata and Pisaster giganteus associations and relative strength with UPC species. SPECIES_2$ BALANUS_NUBILUS 0.4

0.2 C o

0.1 r r e l a

0.0 t i o n -0.1

-0.4 STYELA_MONTEREYENSIS 0.4

0.2 C o

0.1 r r e l a

0.0 t i o n -0.1

UPC Species

Fig. 4 – Balanus nubilius and Styela montereyensis associations and relative strength with UPC species. SPECIES_2$ CYSTOSEIRA 0.6

0.4 C o

0.3 r r e l a

0.2 t i o n 0.1

-0.2 MACROCYSTIS_PYRIFERA 0.6

0.4 C o

0.3 r r e l a

0.2 t i o n 0.1

UPC Species

Fig. 5 – Cystoseira osmundacea and Macrocystis pyrifera associations and relative strengths with UPC species. Citations [[6/6]]

Bodkin, J. L. 1988. Effects of kelp forest removal on associated fish assemblages in central California. J.Exp.Mar.Biol.Ecol. 117:227-238.

Bracken, M. S. Nielsen, K. J. 2004. Diversity of intertidal macroalgae increases with nitrogen loading by invertebrates. Ecology 85: 2828–2836

Cancela, M. C. 2002. Spatial patterns of seed dispersal and seedling recruitment in Corema album (Empetraceae): the importance of unspecialized dispersers for regeneration. Ecology. 90: 775-784

Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs. Science 199: 1302-1310 Daugherty, M. P. 2009. Specialized feeding modes promote coexistence of competing herbivores: Insights from a metabolic pool model. Environmental Entomology, 38:667-676. Duggins, D. O. Simenstad, C. A. Estes, J. A. 1989. Magnification of secondary production by kelp detritus in coastal marine ecosystems

Love, M. S. Lenarz, B. Snook, L. 2010. A survey of the reef fishes, purple hydrocoral (Stylaster californicus), and marine debris of Farnsworth Bank, Santa Catalina Island. Bulletin of Marine Science, 86: 35-52

Paine, R.T. 1996 Food Web Complexity and Species Diveristy. American Naturalist 100: 65-75 Reed, D. C. Foster, M. S. 1984. The effects of canopy shading on algal recruitment and growth in a giant kelp forest. Ecology, 65: 937-948 Watanabe, J. M. 1984. The influence of recruitment, competition, and benthic predation on spatial distribution of three sprecies of kelp forest gastropods (Trochidae: Tegula). Ecology 65: 920-936