COMMUNITY STRUCTURE AND ENERGY FLOW WITHIN RHODOLITH HABITATS AT SANTA CATALINA ISLAND, CA

A Thesis

Presented to

The Faculty of the Department of Marine Science

San José State University

In Partial Fulfillment

Of the Requirements for the Degree

Master of Science

In

Marine Science

by

Scott Stanley Gabara

December 2014

© 2014

Scott S. Gabara

ALL RIGHTS RESERVED

The Designated Thesis Committee Approves the Thesis Titled

COMMUNITY STRUCTURE AND ENERGY FLOW WITHIN RHODOLITH HABITATS AT SANTA CATALINA ISLAND, CA

By

Scott Stanley Gabara

APPROVED FOR THE DEPARTMENT OF MARINE SCIENCE

SAN JOSÉ STATE UNIVERSITY

December 2014

Dr. Diana L. Steller Moss Landing Marine Laboratories

Dr. Michael H. Graham Moss Landing Marine Laboratories

Dr. Scott L. Hamilton Moss Landing Marine Laboratories

ABSTRACT

COMMUNITY STRUCTURE AND ENERGY FLOW WITHIN RHODOLITH HABITATS AT SANTA CATALINA ISLAND, CA

by Scott Stanley Gabara

The purpose of this study was to describe the floral and faunal community associated with rhodolith beds, which are aggregations of free-living coralline algal nodules, off of Santa Catalina Island. Surveys of macroalgal cover, infaunal and epifaunal invertebrates, and fishes suggest rhodolith beds off Santa Catalina Island support greater floral and faunal abundances than adjacent sand habitat. Community separation between rhodolith and sand habitats was due to increased presence of fleshy macroalgae, herbivorous gastropods, and greater abundance of infaunal invertebrates dominated by amphipods, mainly tanaids and gammarids. Stable isotopes were used to determine important sources of primary production supporting rhodolith beds and to identify the major pathways of energy. Stable isotopes suggest the rhodolith bed food web is detrital based with contributions from water column particulate organic matter, drift kelp tissue, and kelp particulates from adjacent kelp beds.

ACKNOWLEDGEMENTS

I am indebted to many people who have helped me over this journey. First I would like to thank Diana Steller, a great teacher, advisor, and friend, thank you for giving me your guidance, your love of the underwater environment and diving, and your ability to enjoy life and always look at the bright side. I would like to thank my committee member, Scott Hamilton, for inspiring me and providing a great role model. I would like to thank my committee member, Michael Graham, for helping me grow a thick skin, encouraging me to be an objective scientist, and for the time he put into helping me understand and appreciate science and its ability to expand our sphere of knowledge. I would like to thank many people that have had large impacts on me and helped me get this beast of a thesis done including: Paul “PT” Tompkins, Bruce Finney,

Rita Mehta, Jack Redwine, Michelle Marraffini, Mike Fox, Arley Muth, Will Fennie,

Sarah Jeffries, Kristin Meagher Robinson, Everett Robinson, Ben Higgins, Dan van Hees,

Kelley van Hees, Ian Moffit, Kai Kopecky, Sarah Sampson, Cheryl Barnes, Stephen

Loiacono, Christian Denney, Angela Szesciorka, Clint “DS” Collins, Erin Loury, Sara

Tanner, Craig Hunter, Alex Macleod, Alex Olson, Rob Franks, Jocelyn Douglas, Jim

Harvey, John Douglas, James Cochran, William “Billy” Cochran, Michelle Keefe, Ivano

Aiello, Rhett Frantz, Jason Adelaars, Gary Adams, Joan Parker, Brynn and Zach

Kaufman, Matt Edwards, Jane Schuytema, the Benthic Ecology and Experimental

Research, Phycology in General (BEERPIGs) group, realistically the entire MLML lab population for both physical and emotional support, the USC Wrigley Institute with special thanks to Trevor Oudin, Lauren Czarnecki Oudin, and Kellie Spafford, Becky

“Smalls” Locker for her endless support, and my family for their encouragement.

vii This would not be possible without the aid from my funding sources:

The American Academy of Underwater Sciences (AAUS) Kevin Gurr Scholarship

Award, Moss Landing Marine Laboratories (MLML) Signe Lundstrom Memorial

Scholarship, Moss Landing Marine Laboratories (MLML) 2013 Wave Award, Council on Ocean Affairs, Science & Technology (COAST) Student Award for Marine Science

Research, David and Lucile Packard Foundation Award, and the Dr. Earl H. Myers and

Ethel M. Myers Oceanographic and Marine Biology Trust.

vii

TABLE OF CONTENTS

List of Figures…………………………………………………………………………….ix

List of Tables……………………………………………………………………………...x

Introduction………………………………………………………………………………..1

Chapter I:

Abstract……………………………………………………………………….…...3 Introduction………………………………………………………………..………4 Methods…………………………………………………………………..………..8 Results………………………………………………………………………..…..12 Discussion…………………………………………………………………….….21 Literature Cited………………………………………………………………..…28

Chapter II:

Abstract……………………………………………………………………….….35 Introduction………………………………………………………………..……..36 Methods…………………………………………………………………..………39 Results………………………………………………………………………..…..46 Discussion…………………………………………………………………….….55 Literature Cited………………………………………………………………..…61

Conclusions………………………………………………………………………………69 Literature Cited…………………………………………………………………………..70 Appendices……………………………………………………………………………….76 Appendix A: Biodiversity of California rhodolith beds……………...….76 13 15 Appendix B: Stable isotope ratios, δ C and δ N, for primary producers and consumers from Isthmus Cove by season…………….78

viii LIST OF FIGURES

Chapter I:

Figure 1. Map of survey locations off Santa Catalina Island……………………………...9

Figure 2. Percent cover of primary substrate within (A) rhodolith and (B) sand habitats at Catalina Island, for all sites combined……………...……...... 12

Figure 3. Species accumulation curves for rhodolith (red lines) and sand habitat (black lines) by the (A) Macroalgae, (B) Infauna, (C) Epifauna, and (D) Fish functional groups………………….………………..……………14

Figure 4. Non-metric multidimensional scaling (nMDS) plot based on a square root transformed Euclidean distance matrix of the combined community...…………………………………………………………...……...16

Figure 5. Non-metric multidimensional scaling (nMDS) plots based on square root transformed Euclidean distance matrices of (A) Macroalgae, (B) Infauna, (C) Epifauna, and (D) Fishes. ……..…………………………...18

Figure 6. Abundance of (A) Macroalgae, (B) Infaunal invertebrates, (C) Epibenthic invertebrates, and (D) Fishes, within rhodolith and sand habitats.…………...20

Chapter II:

Figure 1. Map of Santa Catalina Island with inset of Isthmus cove and the rhodolith bed where collections of primary producers and consumers were made……………………………...……………………………………..40

Figure 2. δ13C versus δ15N biplot of rhodolith bed invertebrate consumers values (mean±SD) pooled across sampling times from Isthmus Cove………..49

Figure 3. Diet contribution of pooled SPOM, SOM, and drift kelp to planktivore, detritivore, herbivore, and predator trophic groups from a SIAR mixing model…………………………………………………………………………..51

Figure 4. δ13C versus δ15N biplot of rhodolith bed primary producers and potential herbivore consumers by season……………………………………..53

Figure 5. Percent diet contribution to the gastropods (A) Lirularia spp. and (B) Megastraea undosa………………………………………………………...54

Figure 6. Generalized rhodolith bed food web model based on δ13C and δ15N biplot, incorporating pooled primary producers and consumers from Isthmus Cove………………………………………………………………….55

ix

LIST OF TABLES

Chapter I:

Table 1. Mean ± SE values for sediment size classes from cores in rhodolith and sand habitats during spring and winter…………………………….………13

Table 2. Tests for differences in assemblage by habitat and season based on two-way permutational multivariate analysis of variance (PERMANOVA)……………………………………………………………….16

Table 3. Relative contribution of taxa to the observed differences in the overall community assemblage by (A) habitat and (B) season. Similarity percentage (SIMPER) analysis listed for taxa contributing over 50% to dissimilarity. …………………………………………………...…...………16

Table 4. Tests for differences in assemblage by habitat and season based on two-way permutational multivariate analysis of variance (PERMANOVA) for (A) macroalgae, (B) infauna, (C) epifauna, and (D) fishes.………………………………………………………...……..…18

Table 5. Relative contribution of (A) macroalgal, (B) infaunal, and (C) epifaunal taxa, to the observed differences in assemblage by habitat. Relative contribution of (D) epifaunal taxa to the observed differences in assemblage by season. Similarity percentages (SIMPER) analysis listed for taxa contributing to over 90% dissimilarity. Abundance values are averages between habitats or seasons..……….…………...……..…19

x INTRODUCTION

High biodiversity has been correlated with structural complexity in both terrestrial

(Simpson 1964) and marine systems (Ormond et al. 1997, Kamenos et al. 2004).

Foundation species are critical to the establishment and persistence of populations and increase the structural complexity of the benthos (Bruno & Bertness 2001). The structure and dynamics of foundation species have broad consequences for associated biota, community dynamics, ecosystem function, and stability (Ellison et al. 2005). In marine systems, conspicuous foundation species include kelps (Estes & Palmisano 1974, Graham

2004), salt marsh grasses (Bertness & Hacker 1994, Bertness et al. 1999), mangroves

(Nagelkerken et al. 2008, Nagelkerken & Faunce 2008, Nagelkerken et al. 2010), sea grasses (Ellison & Farnsworth 2001, Ellison et al. 2005, Nagelkerken & Faunce 2008), and corals (Luckhurst & Luckhurst 1978, Alvarez-Filip et al. 2009). Marine foundation species provide a variety of benefits to community inhabitants such as generating habitat, reducing environmental and predation stresses, enhancing retention of propagules and particulates, and increasing the supply of resources (Bruno & Bertness 2001).

Rhodoliths are species of free-living coralline algal nodules with a world-wide distribution (Foster 2001). It has been posited that rhodoliths increase diversity by creating hard substratum supporting epifauna, by creating interstitial spaces among branches harboring cryptofauna, and supporting infauna in the underlying sediment

(Foster 2001, Steller et al. 2003). Species diversity associated with rhodolith beds can be relatively high with around 300 invertebrate and algal species found associated with a bed in the Gulf of California (Steller et al. 2003) and 450 algal and invertebrate species associated with a bed in the Iberian Peninsula (Bordehore et al. 2003). With high density

1 and diversity of associated marine flora and fauna (Steller et al. 2003, Foster et al. 2007), rhodoliths serve as foundation species in some areas (Foster et al. 2007). Recent descriptions of rhodolith beds at Santa Catalina Island, CA lack basic biological information about the floral and faunal community (Tompkins 2011).

The overarching goals of this study were to describe the community of rhodolith beds at Santa Catalina Island and to determine potential sources of primary production.

The objectives of Chapter I were to compare habitat and seasonal differences of (1) species richness and abundance of macroalgae, infauna, epifauna, and fishes within rhodolith beds and adjacent sand, and (2) determine which taxa may drive differences.

The objectives of Chapter II were to (1) determine the main trophic groups structuring the rhodolith community food web and the primary trophic pathways connecting them, and

(2) determine the influence of giant kelp drift through time to herbivorous epibenthic invertebrates within a Catalina rhodolith bed.

2 CHAPTER I ENHANCED ABUNDANCE AND RICHNESS OF ORGANISMS IN RHODOLITH BEDS RELATIVE TO SAND AT SANTA CATALINA ISLAND, CA

ABSTRACT

Reduction and homogenization of structurally complex habitats is occurring throughout the world. Species that increase structural complexity often have a disproportionate influence on the structure and function of an ecosystem. Rhodoliths are carbonate-forming species that increase structural complexity of the benthos over an otherwise soft bottom habitat. The goal of this study was to characterize the associated community inhabiting rhodolith beds and to make a comparison to adjacent sandy habitat to elucidate the ecological role of rhodoliths and allude to the impact of rhodolith loss.

To create a community composition within rhodolith beds and sand habitats, surveys of four functional groups were conducted including macroalgae, infaunal and epifaunal invertebrates, and fishes. Observed differences in overall community composition were due to both habitat and season. Community differences by habitat were driven by greater abundance of fleshy attached algae, infauna, and epifauna within rhodolith beds. These surveys suggest the loss of rhodolith structure results in reduced abundance of macroalgal, infaunal, and epifaunal taxa. Rhodolith size and complexity appears relatively low compared to other rhodolith beds worldwide, suggesting a potential cause of reduced faunal abundance. Factors reducing rhodolith structural complexity, such as mooring chains, are predicted to diminish community biodiversity and abundance.

3 INTRODUCTION

High biodiversity is often associated with structural complexity in terrestrial

(Simpson 1964) and marine systems (Ormond et al. 1997, Kamenos et al. 2004a). An increase in diversity likely occurs because complex biogenic habitats alter environmental parameters (Bruno & Bertness 2001) and stabilize predator-prey relationships (Kamenos et al. 2004c). As the primary habitat-forming structure, foundation species increase structural complexity by transforming two-dimensional homogeneous landscapes into more complex three-dimensional areas with increased biodiversity (Simpson 1964, Bruno

& Bertness 2001). Foundation species are of fundamental importance to ecologists as they are critical to the establishment and persistence of populations (Bruno & Bertness

2001). As defined here, foundation species are those species that have a disproportionate influence on the structure and function of a community through their presence and not by their actions (Dayton, 1972, Bruno & Bertness 2001, Shelton 2010). For example the structure provided by Eastern hemlock (Tsuga canadensis) has dramatic consequences on the underlying community as they have higher leaf area index than deciduous trees which blocks light and snow mediating soil moisture, stabilizing stream base-flows, and decreasing diel temperature variation (Ellison et al. 2005). The structure and dynamics of foundation species have broad consequences for associated biota, community dynamics, ecosystem function, and stability (Ellison et al. 2005).

In marine systems, conspicuous foundation species include kelps (Estes &

Palmisano 1974, Graham 2004), salt marsh grasses (Bertness & Hacker 1994, Bertness et al. 1999), mangroves (Nagelkerken et al. 2008, Nagelkerken & Faunce 2008,

Nagelkerken et al. 2010), sea grasses (Ellison & Farnsworth 2001, Ellison et al. 2005,

4 Nagelkerken & Faunce 2008), and corals (Luckhurst & Luckhurst 1978, Alvarez-Filip et al. 2009). Marine foundation species provide a variety of benefits to community inhabitants by increasing structural complexity, as they generate habitat that reduces environmental stress and predation pressure, enhance retention of propagules and particulates, increase the supply of resources, and potentially by serving as a food resource themselves (Bruno & Bertness 2001, Graham 2004). For example, in the subtropics, mangrove prop-roots and pneumatophores increase structural complexity by creating hard structure in a soft sediment environment, forming habitat for marine plants, algae, invertebrates, and vertebrates (Nagelkerken et al. 2008). The high productivity of mangroves and nutrient cycling in these systems is also important as it enhances bacteria, microalgae, and detritus production, potentially providing food resources for sponges, prawns, crabs and gastropods (Nagelkerken et al. 2008). The importance of foundation species is demonstrated by the impact of their loss, which affects local and adjacent populations and environments, rates of decomposition, nutrient flux, carbon sequestration, and energy flow (Ellison et al. 2005).

The impact of foundation species removal is most conspicuous when the foundation species provides the primary habitat and is also the dominant food resource.

For example, kelp forest deforestation can have dramatic effects on community composition by causing a shift from a diverse kelp and macroalgal assemblage to one dominated primarily by coralline algae. The result of this phase shift is a reduction in feeding of primary consumers on attached macroalgae and phytodetritus to solely phytoplankton detritus (Graham 2004). In southern California the effect of deforestation on the kelp forest-associated community has been shown to result in an almost complete

5 loss of canopy fishes and two large predators (Graham 2004). The influence of a foundation species on a community is related to the strength with which species associate with it, the degree of persistence of that foundation species in the system, and the potential for functional redundancy, i.e. can another species perform a similar functional role or roles of the foundation species? (Witman 1985, Bertness & Hacker 1994, Shelton

2010). Understanding the functional role of a foundation species requires knowledge of the species it supports, the population dynamics of the foundation species itself, and its impact on the community (Shelton 2010).

Rhodoliths are bed forming species of free-living coralline algal nodules which have a world-wide distribution (Foster 2001). Rhodoliths support a high diversity of organisms, likely due to the provision of hard substrate over what would otherwise be a soft sedimentary benthos (Foster 2001, Steller et al. 2003, Foster et al. 2007). Rhodoliths propagate above mud or fine sand substrate with dead material sloughing to the perimeter of the living portion of the bed (Tompkins 2011). Studies have compared rhodolith to adjacent sand habitats, revealing increases in species abundance, richness, and diversity in high density rhodolith beds relative to adjacent non-rhodolith sedimentary substrate

(Cabioch 1968, Bosence 1979, Steller et al. 2003). These studies have revealed benefits of rhodolith structure which include providing refuge from predation (Kamenos et al.

2004a, c), aggregation of food resources for filter feeders (Grall et al. 2006), retention of water born and algal detritus for deposit feeders (Grall et al. 2006), and alteration of water flow increasing larval retention (Steller et al. 2003), and/or creation of substrate enhancing larval settlement and metamorphosis (Morse & Morse 1984, Johnson et al.

6 1991, Steller & Cáceres-Martinez 2009, Tung & Alfaro 2011). These rhodolith-derived benefits create distinct communities from adjacent non-rhodolith sedimentary habitats.

Rhodolith bed community composition has been described in the North Pacific

(Konar et al. 2006), Baja California in Mexico (Steller et al. 2003, Foster et al. 2007),

Brazil (Villas-Boas 2014), the central Mediterranean (Sciberras et al. 2009), the North

Eastern Atlantic (Grall et al. 2006), and the South Eastern Atlantic (Figueiredo et al.

2012, Amado-Filho et al. 2012). While these studies describe the community dominants, most are snapshots and do not establish descriptions of the entire community assemblage.

Although some studies have described temporal changes in secondary cover (Piazzi et al.

2002, Steller et al. 2003, Amado-Filho & Maneveldt 2010, Pascelli et al. 2013) few studies have described changes in community composition through time with emphasis on higher trophic level predators such as fishes (Foster 2001, Foster et al. 2007).

The extent of live and dead rhodolith substrate at seven rhodolith beds around

Santa Catalina Island has recently been described (Tompkins 2011). However, little is known about the attached macroalgae, infaunal and epifaunal invertebrates, and fishes, creating a community within these beds. Disturbance from mooring chains has been suggested to reduce live rhodolith cover and the structural complexity of the rhodoliths.

The objective of this study was to determine community changes between two extremes, live rhodolith habitats to that of adjacent sand habitat with reduced structural complexity.

Specifically I asked the following questions (1) Are there detectable differences in the community composition between rhodolith and sand habitats and does this relationship vary by season?, (2) does abundance and species richness vary between rhodolith and adjacent sand habitats?, and (3) which taxa drive observed community composition

7 differences by habitat and season? This study is the first step in describing the contribution rhodoliths make to macroflora and fauna relative to sand substrate in southern California. The results of this study will help to understand the impact of rhodolith loss and decreasing structural complexity on community composition.

METHODS

Study Site

Santa Catalina Island is part of the Channel Islands archipelago in the Eastern

Pacific off of southern California. The island sits in a Northwest-Southeast orientation and is exposed to warm water from the Southern California Countercurrent. The near shore subtidal is dominated by diverse and productive kelp beds that propagate over rocky reefs. Recently, the locations and percent carbonate cover of seven rhodolith beds were described by Tompkins (2011). The rhodolith beds range from 4 - 21 meters water depth, are located in bays and coves, and each bed is composed of patchy aggregations of live rhodolith surrounded by dead rhodolith (non-pigmented) carbonate sand, with a gradient into sand with greater contributions of silicate sediment. Mooring chain disturbance creates channels of live material straddled by disturbed un-pigmented dead rhodolith in all Catalina beds (Tompkins 2011).

Sampling Design

To establish community composition relative to habitat, benthic community surveys were performed in rhodolith beds and adjacent sedimentary habitats devoid of rhodoliths, hereafter called sand. Rhodolith beds were defined as locations with >50 % cover of live rhodolith while adjacent sand areas contained no detectable live rhodolith

8 cover, however contained dead rhodolith sand. To encompass the range of known Santa

Catalina Island rhodolith beds, locations were chosen randomly and treated as rhodolith bed replicates. Locations included Cherry Cove (33.451°N, 118.502°W), Isthmus Cove

(33.444°N, 118.497 °W) and Avalon Harbor (33.348°N, 118.325°W, Figure 1). Surveys at each bed consisted of four transects. Transect locations within rhodolith beds and adjacent sand habitats were stratified within each bed to minimize environmental differences between habitats such as depth, swell exposure, hydrodynamics, mooring chain proximity, and kelp bed proximity. To estimate seasonal variability in community composition surveys were conducted during April 2013 (Spring) and December 2013

(Winter).

Figure 1. Map of survey locations off Santa Catalina Island in Cherry Cove (CC), Isthmus Cove (IC), and Avalon Harbor (AH). Surveys were conducted in rhodolith (R) and adjacent sand (S) habitats (Adapted from Tompkins 2011).

Surveys of primary substrate, attached flora, infaunal invertebrates, epifaunal invertebrates, and fishes, were conducted along 20-meter transects in rhodolith beds and

9 adjacent sand habitats. Transect length was selected so replicates would fit within existing live rhodolith patches. Percent cover of primary and secondary substrates was estimated using Uniform Point Contact (UPC) method with substrate and cover recorded every meter along the 20-meter tape. Primary or basal substrate was recorded as live rhodolith, dead rhodolith sand, or sand, and used to estimate differences in cover between habitats (n=4 transects per habitat, during both seasons). Secondary substrate was recorded to test for differences in attached or epiphytic macroalgae between habitats (n=4 transects per habitat, during both seasons). The density of epifaunal invertebrates

(individuals >2cm) was recorded in a 20 x 2 meter area (n=4 transects per habitat, during both seasons). Fish density was estimated within 20 x 2 x 2 meter volume (n=4 transects per habitat, during both seasons).

Invertebrates within individual rhodoliths or between rhodolith thalli, referred to as cryptofauna (Steller et al. 2003), and invertebrates within the underlying sediment, infauna, were grouped and collectively referred to as infauna as they could not be distinguished post collection. Infaunal invertebrate density was estimated in rhodolith and sand habitats using sediment cores (6.5 cm diameter x 10 cm deep, 1327.32 cm3).

Two cores were taken at random distances along survey transects. These 2 cores were averaged, yielding 4 replicates within each habitat during both seasons. Core contents were placed into plastic zip bags, transported to Wrigley Institute of Environmental

Studies (WIES), placed into a -80°C freezer (to preserve invertebrates for future isotopic analysis). Frozen material was thawed, sediment was wet sieved using Fisher U.S. standard brass sieves (4.75mm, 2mm, 0.05 mm), organisms were identified to lowest taxonomic resolution, class or order for most infauna, using a dissecting microscope

10 (Leica S6D), and stored in ethanol or dried for later isotopic analysis. To assess sediment for size class comparison between habitats, the sediments within the four size classes

(x>4.75mm, 4.75

Scientific drying oven at 60°C for 48 hours, and dry mass was recorded for each size class using a Sartorius balance.

Statistical analyses

Species (taxa) accumulation curves were used to compare species richness between rhodolith and sand habitats for each of the four functional groups. Species accumulation or rarefaction curves were created by plotting the cumulative number of species (taxa) resulting from an increase in sampling effort, using 1000 permutations, and were generated using the ‘vegan’ package in R (Oksanen et al. 2010).

To test for habitat or seasonal differences in the overall community, assemblages of macroalgae, infauna, epifauna, and fishes, were combined. Taxa that were found in

5% or less of surveys were excluded from analysis. Estimates of abundance for flora and fauna were square root transformed to reduce the impact of taxa with relatively large abundance values (Clarke & Green 1988). Resemblance matrices based on Euclidian distance were created for each of the four functional groups, these matrices were then normalized and combined to create an overall community assemblage. The community of each functional group was also examined individually to determine if the community composition varied by habitat or season without the influence of other functional groups.

Non-metric multi-dimensional scaling ordinations (nMDS) based on Euclidian distance similarity matrices were created to visually represent differences in community assemblages. To test for differences of community composition by habitat and season a

11 two-factor crossed permutation-based analysis of variance (PERMANOVA) was conducted on Euclidian distance similarity matrices (Anderson et al. 2008). Similarity percentage (SIMPER) analysis was used to identify which taxa contributed greatest to the observed differences in assemblage by habitat and/or season if significant effects were detected. Analyses (nMDS, PERMANOVA, and SIMPER) were conducted using

PRIMER-E (Plymouth Routines in Multivariate Ecological Research), 6.0 (Clarke1993,

Clarke & Warwick 2001).

RESULTS

Habitat differences

Surveys in rhodolith beds were conducted in areas with approximately 50% or greater live rhodolith cover, averaging (±SE) 59.58% ± 9.67 in spring and 50.83% ± 3.54 in winter. Surveys in adjacent sand habitat lacked live rhodolith with primary substrate dominated by silicate sand averaging (±SE) 90.21% ± 5.44 in spring and 97.50% ± 1.45 in winter (Figure 2). Sediment size class distribution suggests sand habitats have much greater contributions of fine sediment (<0.05mm) while rhodolith bed habitats are characterized by greater contributions of sediments size classes greater than 0.05mm and particularly sediment over 2mm in size (Table 1).

12

Figure 2. Percent cover of primary substrate within (A) rhodolith and (B) sand habitats at Catalina Island, for all sites combined. Error bars are standard error.

Table 1. Mean ± SE size class percentage (dry weight) from sediment cores in rhodolith and sand habitats during spring and winter.

Richness

Estimates of species (taxon) richness were generated from species rarefaction curves. Taxa were greater within rhodolith beds across all four functional groups, although the magnitude of difference varied between habitats (Figure 3). Estimates of taxon richness of macroalgae revealed rhodolith beds supported one more taxa than sand, with 12.9 and 11.8 taxa estimated within rhodolith beds and sand respectively. Estimates of taxon richness for infauna revealed rhodolith beds supported 6 more taxa than sand, with 20.9 and 14.9 taxa estimated within rhodolith beds and sand respectively. Estimates of taxon richness of epifauna revealed rhodolith beds supported 4 more taxa than sand, with 14.9 and 10.8 taxa estimated within rhodolith beds and sand respectively. Estimates

13 of taxon richness for fish revealed rhodolith beds supported 1 more taxa than sand, with

8.9 and 7.9 taxa estimated within rhodolith beds and sand respectively.

Figure 3. Species accumulation curves for rhodolith (red lines) and sand habitat (black lines) by the (A) Macroalgae, (B) Infauna, (C) Epifauna, and (D) Fish functional groups. Lines are average number of taxa by transect with 95% confidence intervals (shaded portion), based on 1000 permutations.

14 Community Composition

Non-metric multidimensional scaling analysis of community composition indicated differences in community structure by habitat and season (Figure 4).

PERMANOVA results confirmed significant community differences by habitat (pseudo- f1,11 = 5.05, P = 0.005) and season (pseudo-f1,11 = 2.39, P = 0.016) with habitat explaining about three times more of the variance (33.5%) relative to season (11.5%) (Table 2). The taxa responsible for the observed differences in community composition by habitat spanned many functional groups and taxa including epifaunal Megastraea undosa

(>2cm) and Lirularia spp., epiphytic fleshy red algae, and many infauna including gammarids, tanaids, isopods, ophiuroids, gastropods, decapods, Megastraea undosa

(<2cm), polychaetes, caprellids (Table 3A). With the exception of polychaete worms, these taxa were all more abundant within rhodolith beds (Table 3A). Taxa exclusively found within rhodolith habitat included the gastropod Lirularia spp. and geniculate corallines, mostly comprised of Lithothrix aspergillum. Taxa responsible for the observed differences in community composition by season spanned all functional groups and included Pachycerianthus fimbriatus, polychaetes, Lytechinus pictus (<2cm),

Halichoeres semicinctus, Lytechinus pictus (>2cm), bivalves, turf algae, ostracods, dictyotales, Citharichthys spp., and Rhinogobiops nicholsii (Table 3B). Densities of

Pachycerianthus fimbriatus and both infaunal and epifaunal Lytechinus pictus showed decreases from spring to winter, and other taxa showed mixed directionality (Table 3B).

15

Figure 4. Non-metric multidimensional scaling (nMDS) plot based on a square root transformed Euclidean distance matrix of the combined community. Distances between points represent relative dissimilarities in community assemblage. Symbols represent rhodolith (*, red asterisk), sand (Ÿ, black circle), Spring (s), and Winter (w).

Table 2. Tests for differences in assemblage by habitat and season based on two-way permutational multivariate analysis of variance (PERMANOVA) for the community assemblage created from incorporating macroalgae, infauna, epifauna, and fish functional groups.

Community Source df SS MS Pseudo-F P (perm) % variance Habitat (A) 1 102.73 102.73 5.05 0.005 33.52 Season (B) 1 48.60 48.60 2.39 0.016 11.49 Habitat x Season 1 26.85 26.85 1.32 0.198 5.29 Residual 8 162.82 20.35 49.70 Total 11 341.00

Table 3. Relative contribution of taxa to the observed differences in the overall community assemblage by (A) habitat and (B) season. Similarity percentage (SIMPER) analysis listed for taxa contributing over 50% to dissimilarity. Directionality shown for general trend in abundance between (A) habitats, Rhodolith = R and S = Sand, and between (B) seasons, S = Spring and W = Winter.

A Community (habitat) B Community (season) Contribution to Directionality Contribution to Directionality Taxa Dissimilarity (%) in Abundance Taxa Dissimilarity (%) in Abundance Megastraea (epifauna) 4.91 R > S Pachycerianthus fimbriatus 6.57 S > W Gammarid 4.42 R > S Polychaeta 5.64 S = W Tanaid 4.41 R > S Lytechinus pictus (infauna) 4.83 S > W Isopod 4.32 R > S Halichoeres semicinctus 4.79 S < W Ophiuroid 4.28 R > S Lytechinus pictus (epifauna) 4.62 S > W Gastropod 4.27 R > S Bivalves 4.57 S < W Decapod 4.23 R > S Turf Algae 4.42 S < W Megastraea (infauna) 4.19 R > S Ostracods 4.39 S < W Polychaete 4.17 R = S Dictyotales 4.21 S < W Caprellid 4.12 R > S Citharichthys spp. 4.08 S > W Fleshy Red Algae 4.00 R > S Rhinogobiops nicholsii 3.98 S > W Lirularia spp. 3.95 R > S

16 Non-metric multidimensional scaling analysis of the four community functional groups indicated differences in community composition by habitat for macroalgae, infauna, and epifauna, and differences by habitat and season for epifauna (Figure 5A-D).

PERMANOVA results detected community differences by habitat for macroalgae

(pseudo-f1,11 = 3.30, P = 0.028), infauna (pseudo-f1,11 = 16.73, P = 0.002), epifauna

(pseudo-f1,11 = 7.05, P = 0.004), and differences by season for epifauna (pseudo-f1,11 =

4.43, P = 0.003) (Table 2). The fish assemblage did not vary by habitat (pseudo-f1,11 =

0.675, P = 0.531) or season (pseudo-f1,11 = 1.080, P = 0.364) (Figure 5D, Table 4D). The taxa responsible for over 50% of the observed differences in macroalgal assemblage by habitat were from the brown algal Dictyotales group, comprised of Dictyopteris undulata and Dictyota binghamiae, and fleshy red algae, comprised of Polysiphonia spp.,

Chondracanthus canaliculatus, and Rhodymenia spp. (Table 5A). Percent cover of

Dictyotales and fleshy red algae were 2.9 and 7.6 times greater in rhodolith beds than sand habitats respectively (Fig. 6). The taxa responsible for the observed differences in infaunal assemblage by habitat were mainly tanaids and gammarids (Table 5B) and density was 5.2 and 3.3 times more abundant within rhodolith beds than sand habitats respectively (Fig. 6). The taxa responsible for the observed differences in epifaunal assemblage by habitat were Megastraea undosa and Lirularia spp., and these taxa were more abundant within rhodolith beds (Table 5C, Fig. 6). The taxa responsible for the observed differences in epifaunal assemblage by season were Pachycerianthus fimbriatus and Lytechinus pictus, and densities were characterized by reductions from Spring to

Winter (Table 5D).

17

Figure 5. Non-metric multidimensional scaling (nMDS) plots based on square root transformed Euclidean distance matrices of (A) Macroalgae, (B) Infauna, (C) Epifauna, and (D) Fishes. Distances between points represent relative dissimilarities in community assemblage. Symbols represent rhodolith (*, red asterisk), sand (Ÿ, black circle), Spring (s), and Winter (w).

Table 4. Tests for differences in assemblage by habitat and season based on two-way permutational multivariate analysis of variance (PERMANOVA) for (A) Macroalgae, (B) Infauna, (C) Epifauna, and (D) Fishes.

18 Table 5. Relative contribution of (A) Macroalgal, (B) Infaunal, and (C) Epifaunal taxa, to the observed differences in assemblage by habitat. Relative contribution of (D) Epifaunal taxa to the observed differences in assemblage by season. Similarity percentages (SIMPER) analysis listed for taxa contributing to over 90% dissimilarity. Abundance values are averages between habitats or seasons.

19 Figure 6. Abundance of (A) Macroalgae, (B) Infaunal invertebrates, (C) Epibenthic invertebrates, and (D) Fishes, within rhodolith and sand habitats. Error bars are standard error. NF = not found.

20 DISCUSSION

Loss of Structural Complexity

This study supports the hypothesis that homogenizing structurally complex habitats leads to a loss of marine biodiversity and abundance (Airoldi et al. 2008).

Community surveys between rhodolith and adjacent sand suggests the abundance of many taxa will decrease following a reduction of rhodolith structure. Two taxa were found exclusively in live rhodolith habitat and these were the gastropod Lirularia spp. and epiphytic geniculate corallines that appeared to grow on rhodolith thalli. As only two taxa were exclusive to rhodolith habitat, differences in community composition by habitat are mainly due to differences in abundance of shared taxa rather than the presence or absence of taxa creating distinct communities. This suggests for rhodolith communities, loss of structural complexity may lead to dramatic losses of floral and faunal abundance with moderate reductions of species richness.

It is well known that features of the physical habitat can greatly influence the abundance and diversity of taxa influencing community structure (MacArthur R. &

MacArthur J. 1961). This study suggests that even on a scale of centimeters, loss of structural complexity can cause reductions in richness and dramatic reductions in associated faunal abundance. A reduction in the size, density, and morphological complexity of rhodolith habitat (Bruno & Bertness 2001, Bruno et al. 2003) occurs from live rhodolith to adjacent sand habitat (Tompkins 2011). A loss of these features lead to declines in the diversity of microhabitats creating niches available for associated organisms (Grall et al. 2006), declines of the structure creating refuge from predation

(Rogers et al. 2014), and declines in retention of food resources (Steller & Cáceres-

21 Martínez 2009), such as sedimenting detritus or potentially benthic diatoms (Grall et al.

2006). The relative importance of rhodoliths as refuge or for food provision should be investigated in future rhodolith work to predict the impact of disturbance. Future studies should consider investigating the impact of structural complexity on smaller habitat forming species such as rhodoliths.

Abundance

Rhodolith beds are capable of supporting high abundance of associated organisms, however overall abundance appears to vary globally across rhodolith bed locations (Steller et al. 2003, Foster et al. 2007, Sciberras et al. 2009). Compared to other rhodolith beds worldwide, Santa Catalina beds supported much lower invertebrate abundance. Infaunal densities in a rhodolith bed in the Gulf of California (1,402,000 individuals / m2) were 54 times greater than the abundance estimated within Catalina

Island rhodolith beds (25,915 individuals / m2) (Steller et al. 2003). Gulf of California rhodolith beds also supported much greater infaunal abundance than adjacent sand habitats (956 times), a much greater magnitude of difference relative to the estimated 3.5 times increase estimated within Catalina Island beds (Steller et al. 2003). As more descriptions of rhodolith bed diversity and abundance are made, potential factors driving global differences can be identified and studied in future work.

California rhodolith beds may have reduced diversity and abundance relative to other beds worldwide due to reduced size, density, or morphological complexity of rhodoliths (Steller et al. 2003, Tompkins 2011). Catalina Island rhodoliths are much smaller (0.3-2.5 cm, Tompkins 2011) relative to rhodoliths of Bahía Concepción (2.1-4.8 cm, Steller et al. 2003), supporting the hypothesis that larger rhodoliths support greater

22 abundances of infauna (Steller et al. 2003). Potential factors affecting rhodolith morphology are vast and include abiotic factors such as light, water clarity, water temperature, nutrients, exposure, and hydrodynamics (review in Foster 2001). Potential biotic factors affecting rhodolith morphology and size include species, nutrients from fauna, fouling, and bioturbation (review in Foster 2001). Other causes of reduced rhodolith size, density, and morphology are from anthropogenic disturbance such as moorings and boat anchors (Steller et al. 2003, Tompkins 2011), dredging (De Grave &

Whitaker 1999, Hall-Spencer & Moore 2000), and trawling (Bordehore et al. 2003).

The effects of mooring disturbance, dredging, or trawling can homogenize the benthos having a dramatic and wide effect on associated species (Kamenos et al. 2003,

Levin et al. 2010). The rhodolith beds at Santa Catalina Island appear highly disturbed by mooring chains, resulting in a reduction in rhodolith size distribution and quality of the beds, likely leading to community shifts to sand associated taxa (Tompkins 2011).

Mooring chain disturbance is likely similar to the effects of grab or pump dredging that reduces fauna and shifts community dominants to taxa such as bivalves (De Grave &

Whitaker 1999) and otter trawling that changes community composition by reducing epiphytic invertebrates with a community shift toward polychaetes (Bordehore et al.

2003). These community shifts following disturbance are likely long lasting as rhodolith beds have shown little recovery on the scale of years post-dredging (Hall-Spencer &

Moore 2000). Low recovery potential is tied to slow growth rates on the scale of millimeters per year (Potin et al. 1990, Hall-Spencer & Moore 2000). With low recovery potential, disturbance causes long lasting effects and worldwide degradation (Steller &

Cáceres-Martínez 2009). Disturbance and its impact to rhodolith morphology and bed

23 structure is a necessary factor for future investigation on rhodolith bed ecology at Santa

Catalina Island.

Rhodolith Infaunal Composition

Dominant infaunal taxon appears to vary widely across rhodolith beds worldwide.

In this study, crustaceans dominated infaunal abundance with contributions of 71.7% and

75.1%, during spring and winter respectively. Similarly a study conducted in an Irish rhodolith bed also found crustaceans contributed greatly (75%) to infaunal composition

(Grave & Whitaker 1999). Dominant taxa appears to vary widely across rhodolith beds with gastropods contributing most to abundance in the Maltese Islands (Sciberras et al.

2009), echinoderms and annelid worms in a Gulf of California bed (Foster et al. 2007), polychaetes worms in a south Australian bed (Harvey & Bird 2008), echinoderms and chiton in a Newfoundland bed (Gagnon, Matheson & Stapleton 2012), and chiton in a

North Pacific bed (Konar et al. 2006). Rhodolith beds do not appear to have a consistent community dominant, this may be due to many factors such as varying environmental conditions, rhodolith morphology, different available food resources, rhodolith bed depth differences, rhodolith size structure, and variation in sampling (Steller et al. 2003).

Consistencies of rhodolith community structure are that most rhodolith beds have few if any herbivore taxa, and detritivores or predators are dominant feeding guilds, suggesting the dominant pathway of primary production is detritus based, either directly to dominant detritivores or indirectly to dominant predators (Grall et al. 2006, Sciberras et al. 2009).

Little is known about the food resources available within rhodolith beds, however food resources of the dominant infaunal taxa may suggest important trophic pathways.

The infauna of Catalina rhodolith beds were dominated by tanaids, which are likely

24 selective deposit feeding omnivores (Blazewicz-Paszkowycz & Ligowski 2002) that consume detritus (Bracken et al. 2007), macroalgae, or epiphytes (Blazewicz-

Paszkowycz & Ligowski 2002). Contrasting studies describing tanaids as carnivores

(Gutu 1986), more recent studies have demonstrated tanaids may consume detritus

(Blazewicz-Paszkowycz & Ligowski 2002, Gillies et al. 2011) however identification and more diet analysis is needed. The second dominant infaunal taxa were gammarids, and similar to tanaids, they likely consume epiphytic macroalgae or detrital giant kelp particulates, as they prefer decaying brown algae (Martin 1966). Greater abundance within rhodolith beds may be due to greater availability of food resources as rhodoliths may collect particulate and detrital food within their interstitial spaces, similar to kelp holdfasts supporting deposit feeders (Schaal et al. 2012). Tanaids and gammarids may rely on detritus that collects within rhodolith thalli, supporting greater abundances of these taxa relative to sand, however experimentation, gut content analysis, and/or stable isotope analysis is needed.

Seasonality

Rhodolith beds are characterized by seasonal changes of flora and fauna likely related to environmental changes such as water temperatures, nutrients, and invertebrate recruitment pulses (Steller et al. 2003, Foster et al. 2007). Temporal fluctuations of epifaunal invertebrates in Catalina rhodolith beds are consistent with other studies that detected large changes in invertebrate composition over time (Kamenos et al. 2004a,b,

Foster et al. 2007, Steller et al. 2003). I detected seasonal changes of the infaunal and epifaunal Lytechinus pictus, Megastraea undosa, Parastichopus parvimensis, and Aplysia californica within rhodolith beds. Juveniles of both Lytechinus pictus and Megastraea

25 undosa were observed within rhodolith sediment core samples (>2cm), suggesting these taxa may either preferentially settle on corallines (Kamenos et al. 2004c, Steller &

Cáceres-Martínez 2009) or have greater growth and survivorship within rhodolith relative to sand habitat (Kamenos et al. 2004a). The seasonal fluctuations of Lytechinus pictus densities appears similar to fluctuations of echinoderms in a Mexican rhodolith bed with greater densities observed in spring and seasonal declines becoming almost undetectable during fall (Foster et al. 2007). These observations suggest annual episodic settlement and/or recruitment events may be common. Explanations for the observed decrease of infaunal and epifaunal Lytechinus pictus densities in fall include: (1) seasonal changes in foraging of fish predators or sheltering behavior by urchins (Bernstein et al. 1981), (2) seasonal emigration of urchins to other habitats or locations, such as deeper water

(Schroeter et al. 1983), and (3) seasonal fluctuations in resource availability likely tied to temperature changes (Steller et al. 2003, Foster et al. 2007). Seasonal changes of grazers such as Megastraea undosa and Lytechinus pictus may alter macroalgal cover and community dynamics, however this requires further study. Future work should consider seasonal changes and investigate community interactions within rhodolith beds.

Conclusion

As the first study conducted within Santa Catalina Island rhodolith beds these surveys establish important baseline information on species composition and abundance, imperative to making comparisons of Catalina Island rhodolith beds through time, to other Channel Island rhodolith beds, and to rhodolith beds worldwide. As the last review on rhodoliths was conducted over a decade ago in Foster (2001), an updated review on the description of rhodolith bed locations and recent work progressing our knowledge on

26 the effects of ocean acidification and global warming on corallines could be beneficial.

Rhodolith beds are an excellent system to study the impact of structural complexity on smaller scales. Future studies within rhodolith beds should consider trophic interactions

(Kamenos et al. 2004c), creation of food web depictions (Grall et al. 2006), succession following disturbance (Hall-Spencer & Moore 2000), and the impact of habitat fragmentation (Hovel & Lipcius 2001).

27

LITERATURE CITED

Airoldi, L., Balata, D. & Beck, M. (2008) The Gray Zone: Relationships between habitat loss and marine diversity and their applications in conservation. Journal of Experimental Marine Biology and Ecology, 366, 8–15.

Alvarez-Filip, L. & Dulvy, N. (2009) Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proceedings of the National Academy of Sciences of the United States of America, 276, 3019–25.

Amado-Filho, G. & Maneveldt, G. (2010) Seaweed diversity associated with a Brazilian tropical rhodolith bed. Ciencias Marinas, 36, 371–391.

Amado-Filho, G.M., Moura, R.L., Bastos, A.C., Salgado, L.T., Sumida, P.Y., Guth, A.Z., Francini-Filho, R.B., Pereira-Filho, G.H., Abrantes, D.P., Brasileiro, P.S., Bahia, R.G., Leal, R.N., Kaufman, L., Kleypas, J.A., Farina, M. & Thompson, F.L. (2012) Rhodolith Beds Are Major CaCO3 Bio-Factories in the Tropical South West Atlantic (ed S Thrush). PLoS ONE, 7, e35171.

Bernstein, B., Williams, B. & Mann, K. (1981) The Role of Behavioral Responses to Predators in Modifying Urchins (Strongylocentrotus droebachiensis) Destructive Grazing and Seasonal Foraging Patterns. Marine Biology, 49, 39–49.

Bertness, M. & Hacker, S. (1994) Physical stress and positive associations among marsh plants. American Naturalist, 144, 363–372.

Bertness, M., Leonard, G. & Levine, J. (1999) Testing the relative contribution of positive and negative interactions in rocky intertidal communities. Ecology, 80, 2711–2726.

Blazewicz-Paszkowycz, M. & Ligowski, R. (2002) Diatoms as food source indicator for some Antarctic Cumacea and Tanaidacea (Crustacea). Antarctic Science, 14, 11–15.

Bordehore, C., Ramos-Espla, A. & Riosmena-Rodriguez, R. (2003) Comparative study of two maerl beds with different otter trawling history, southeast Iberian Peninsula. Aquatic Conservation: Marine and Freshwater Ecosystems, 13, S43–S54.

Bosence, D. (1979) Live and dead faunas from coralline algal gravels, Co. Galway. Palaeontology, 22, 449–478.

Bracken, M., Gonzalez-Dorantes, C. & Stachowicz, J. (2007) Whole-community mutualism: associated invertebrates facilitate a dominant habitat-forming seaweed. Ecology, 88, 2211–9.

28 Bruno, J.F. & Bertness, M.D. (2001) Habitat modification and facilitation in benthic marine communities. In Marine Community Ecology (Bertness, M.D. et al., eds), pp. 201–218, Sinauer.

Bruno, J.F., Stachowicz, J.J. & Bertness, M.D. (2003) Inclusion of facilitation into ecological theory. Trends in Ecology and Evolution, 18(3), 119–125.

Carr, M.H. (1994) Effects of Macroalgal Dynamics on Recruitment of a Temperate Reef Fish. Ecology, 75, 1320–1333.

Clarke, K. (1993) Non‐parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18(1), 117-143.

Clarke, K. & Green, R. (1988) Statistical design and analysis for a“ biological effects” study. Marine Ecology Progress Series, 46, 213–227.

Clarke, K. & Warwick, R. (2001) A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Marine Ecology Progress Series, 216, 265–278

Davenport, A.C. & Anderson, T.W. (2007) Positive indirect effects of reef fishes on kelp performance: the importance of mesograzers. Ecology, 88, 1548–61.

Dayton, P. (1972) Toward an understanding of community resilience and the potential effects of enrichments to the benthos at McMurdo Sound, Antarctica. Proceedings on the colloquium on conservation problems in Antarctica, 81–95.

Ebeling, A., Larson, R. & Alevizon, W. (1980) Habitat Groups and Island-Mainland Distribution of Kelp-bed Fishes off Santa Barbara, CA.

Ellison, A., Bank, M., Clinton, B. & Colburn, E. (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment, 3, 479–486.

Ellison, A.M. & Farnsworth, E.J. (2001) Mangrove Communities. Marine community ecology (eds M.D. Bertness, S.D. Gaines & M.D.E. Haywood), Sinauer Associates, Sunderland, MA.

Estes, J. & Palmisano, J. (1974) Sea otters: their role in structuring nearshore communities. Science, 185, 1058–1060.

Figueiredo, M.A.O., Coutinho, R., Villas-Boas, A.B., Tâmega, F.T.S. & Mariath, R. (2012) Deep-water rhodolith productivity and growth in the southwestern Atlantic. Journal of Applied Phycology, 24, 487–493.

Foster, M.S. (2001) Rhodoliths: between rocks and soft places. Journal of Phycology, 37, 659–667.

29 Foster, M.S., McConnico, L., Lundsten, L., Wadsworth, T., Kimball, T., Brooks, L., Medina-Lopez, M., Riosmena-Rodriguez, R., Hernandez-Carmona, G. & Vasquez- Elizondo, R. (2007) Diversity and natural history of a Lithothamnion muelleri- Sargassum horridum community in the Gulf of California. Ciencias Marinas, 33, 367.

Gagnon, P., Matheson, K. & Stapleton, M. (2012) Variation in rhodolith morphology and biogenic potential of newly discovered rhodolith beds in Newfoundland and Labrador (Canada). Botanica Marina, 55, 85–99.

Gillies, C., Stark, J., Johnstone, G. & Smith, S. (2011) Carbon flow and trophic structure of an Antarctic coastal benthic community as determined by δ13C and δ15N. Estuarine, Coastal and Shelf Science, 97, 44–57.

Graham, M.H. (2002) Prolonged reproductive consequences of short-term biomass loss in seaweeds. Marine Biology, 140, 901–911.

Graham, M.H. (2004) Effects of Local Deforestation on the Diversity and Structure of Southern California Giant Kelp Forest Food Webs. Ecosystems, 7, 341–357.

Grall, J., Leloch, F., Guyonnet, B. & Riera, P. (2006) Community structure and food web based on stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. Journal of Experimental Marine Biology and Ecology, 338, 1–15.

De Grave, S. & Whitaker, A. (1999) Benthic community re-adjustment following dredging of a muddy-maerl matrix. Marine Pollution Bulletin, 38, 102–108.

Gutu, M. (1986) Description of Apseudes olimpiae n. sp. and of Tanabnormia cornicauda ng, n. sp.(Crustacea, Tanaidacea). Travaux du Muséum National d’Histoire naturelle “Grigore Antipa”, 30, 129–133.

Hall-spencer, J.M. & Moore, P.G. (2000) Scallop dredging has profound, long-term impacts on maerl habitats. ICES Journal of Marine Science, 57, 1407–1415.

Hamilton, S., Caselle, J., Lantz, C., Egloff, T., Kondo, E., Newsome, S., Loke-Smith, K., Pondella DJ, I., Young, K. & Lowe, C. (2011) Extensive geographic and ontogenetic variation characterizes the trophic ecology of a temperate reef fish on southern California (USA) rocky reefs. Marine Ecology Progress Series, 429, 227– 244.

Harvey, A.S. & Bird, F.L. (2008) Community structure of a rhodolith bed from cold- temperate waters (southern Australia). Australian Journal of Botany, 56, 437.

Hixon, M. & Beets, J. (1993) Predation, prey refuges, and the structure of coral-reef fish assemblages. Ecological Monographs, 63, 77–101.

30 Hobson, E. S., & Chess, J. R. (1986). Relationships among fishes and their prey in a nearshore sand community off southern California. Environmental Biology of Fishes, 17(3), 201-226.

Hovel, K. A., and R. N. Lipcius. 2001. Habitat Fragmentation in a Seagrass Landscape : Patch Size and Complexity Control Blue Crab Survival. Ecology, 82, 1814–1829.

Johnson, C., Muir, D. & Reysenbach, A. (1991) Characteristic bacteria associated with surfaces of coralline algae: a hypothesis for bacterial induction of marine invertebrate larvae. Marine Ecology Progress Series, 74, 281–294.

Kamenos, N.A., Moore, P. & Hall-spencer, J.M. (2004a) Nursery-area function of maerl grounds for juvenile queen scallops Aequipecten opercularis and other invertebrates. Marine Ecology Progress Series, 274, 183–189.

Kamenos, N.A., Moore, P.. & Hall-Spencer, J.M. (2004b) Attachment of the juvenile queen scallop (Aequipecten opercularis (L.)) to maerl in mesocosm conditions, juvenile habitat selection. Journal of Experimental Marine Biology and Ecology, 306, 139–155.

Kamenos, N.A., Moore, P. & Hallspencer, J. (2004c) Maerl grounds provide both refuge and high growth potential for juvenile queen scallops. Journal of Experimental Marine Biology and Ecology, 313, 241–254.

Konar, B., Riosmena-Rodriguez, R. & Iken, K. (2006) Rhodolith bed: a newly discovered habitat in the North Pacific Ocean. Botanica Marina, 49, 355–359.

Levin, L., Sibuet, M. & Gooday, A. (2010) The roles of habitat heterogeneity in generating and maintaining biodiversity on continental margins: an introduction. Marine Ecology, 31, 1–5.

Lewis, L. & Anderson, T. (2012) Top-down control of epifauna by fishes enhances seagrass production. Ecology, 93, 2746–2757.

Lowe, C. & Topping, D. (2003) Movement patterns, home range, and habitat utilization of adult kelp bass Paralabrax clathratus in a temperate no-take marine reserve. Marine Ecology Progress Series, 256, 205–216.

Luckhurst, B.E. & Luckhurst, K. (1978) Analysis of the influence of substrate variables on coral reef fish communities. Marine Biology, 49, 317–323.

MacArthur, R. & MacArthur, J. (1961) On Bird Species Diversity. Ecology, 42, 594–598.

Martin, A. (1966) Feeding and digestion in two intertidal gammarids: Marinogammarus obtusatus and M. pirloti. Journal of Zoology, 515–525.

31 Morse, A.N.C. & Morse, D.E. (1984) GABA-mimetic molecules from Porphyra (Rhodophyta) induce metamorphosis of Hafotis (Gastropods) larvae. Hydrobiologia, 116-117, 155–158.

Nagelkerken, I., Blaber, S.J.M., Bouillon, S., Green, P., Haywood, M., Kirton, L.G., Meynecke, J.-O., Pawlik, J., Penrose, H.M., Sasekumar, A. & Somerfield, P.J. (2008) The habitat function of mangroves for terrestrial and marine fauna: A review. Aquatic Botany, 89, 155–185.

Nagelkerken, I. & Faunce, C.H. (2008) What makes mangroves attractive to fish? Use of artificial units to test the influence of water depth, cross-shelf location, and presence of root structure. Estuarine, Coastal and Shelf Science, 79, 559–565.

Nagelkerken, I., De Schryver, A.M., Verweij, M.C., Dahdouh-Guebas, F., Van der Velde, G. & Koedam, N. (2010) Differences in root architecture influence attraction of fishes to mangroves: A field experiment mimicking roots of different length, orientation, and complexity. Journal of Experimental Marine Biology and Ecology, 396, 27–34.

Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, et al. (2010) vegan: Community Ecology Package. R package version 1.17–4. http://CRAN.R- project.org/package=vegan.

Pascelli, C., Riul, P., Riosmena-Rodríguez, R., Scherner, F., Nunes, M., Hall-Spencer, J.M., Oliveira, E.C. De & Horta, P. (2013) Seasonal and depth-driven changes in rhodolith bed structure and associated macroalgae off Arvoredo island (southeastern Brazil). Aquatic Botany, 111, 62-65.

PiazzI, L., Pardi, G. & Cinelli, F. (2002) Structure and temporal dynamics of a macroalgal assemblage associated with a rhodolith bed of the Tuscan Archipelago (Tyrrheniam Sea). Atti della Società Toscana di Scienze Naturali, Memorie, 5–10.

Polidoro, B.A, Carpenter, K.E., Collins, L., Duke, N.C., Ellison, A.M., Ellison, J.C., Farnsworth, E.J., Fernando, E.S., Kathiresan, K., Koedam, N.E., Livingstone, S.R., Miyagi, T., Moore, G.E., Ngoc Nam, V., Ong, J.E., Primavera, J.H., Salmo, S.G., Sanciangco, J.C., Sukardjo, S., Wang, Y. & Yong, J.W.H. (2010) The loss of species: mangrove extinction risk and geographic areas of global concern. PLoS ONE, 5, e10095.

Potin, P., Floc'h, J. Y., Augris, C., & Cabioch, J. (1990). Annual growth rate of the calcareous red alga Lithothamnion corallioides (Corallinales, Rhodophyta) in the Bay of Brest, France. Hydrobiologia, 204(1), 263-267.

Prado, P., Romero, J. & Alcoverro, T. (2009) Welcome mats? The role of seagrass meadow structure in controlling post-settlement survival in a keystone sea-urchin species. Estuarine, Coastal and Shelf Science, 85, 472–478.

32 Rogers, A., Blanchard, J.L. & Mumby, P.J. (2014) Vulnerability of coral reef fisheries to a loss of structural complexity. Current biology, 24, 1000–1005.

Sabeel, R.A.O., Ingels, J., Pape, E. & Vanreusel, A. (2014) Macrofauna along the Sudanese Red Sea coast: potential effect of mangrove clearance on community and trophic structure. Marine Ecology, 1-16.

Schaal, G., Riera, P. & Leroux, C. (2012) Food web structure within kelp holdfasts (Laminaria): a stable isotope study. Marine Ecology, 370–376.

Schroeter, S., Dixon, J. & Kastendiek, J. (1983) Effects of the starfish Patiria miniata on the distribution of the sea urchin Lytechinus anamesus in a southern Californian kelp forest. Oecologia, 141–147.

Sciberras, M., Rizzo, M., Mifsud, J.R., Camilleri, K., Borg, J. a., Lanfranco, E. & Schembri, P.J. (2009) Habitat structure and biological characteristics of a maerl bed off the northeastern coast of the Maltese Islands (central Mediterranean). Marine Biodiversity, 39, 251–264.

Shelton, A.O. (2010) Temperature and community consequences of the loss of foundation species: Surfgrass (Phyllospadix spp., Hooker) in tidepools. Journal of Experimental Marine Biology and Ecology, 391, 35–42.

Simpson, G. (1964) Species density of North American recent mammals. Systematic Zoology, 13, 57–73.

Singh GG, Markel RW, Martone RG, Salomon AK, Harley CDG, et al. (2013) Sea Otters Homogenize Mussel Beds and Reduce Habitat Provisioning in a Rocky Intertidal Ecosystem. PLoS ONE, 8(5), e65435.

Steller, D.L. & Cáceres-Martínez, C. (2009) Coralline algal rhodoliths enhance larval settlement and early growth of the Pacific calico scallop Argopecten ventricosus. Marine Ecology Progress Series, 396, 49–60.

Steller, D.L., Riosmena-Rodriguez, R., Foster, M.S. & Roberts, C.A. (2003) Rhodolith bed diversity in the Gulf of California: the importance of rhodolith structure and consequences of disturbance. Aquatic Conservation: Marine and Freshwater Ecosystems, 13, S5–S20.

Tompkins, P.A. (2011) Distribution, Growth, and Disturbance of Catalina Island Rhodoliths. Masters Thesis. Moss Landing Marine Laboratories, San Jose State University.

Topping, D.T., Lowe, C.G. & Caselle, J.E. (2005) Home range and habitat utilization of adult California sheephead, Semicossyphus pulcher (Labridae), in a temperate no- take marine reserve. Marine Biology, 147, 301–311.

33 Tung, C.H. & Alfaro, A. (2011) Effects of Dual Microalgal Species Biofilms on New Zealand Black-Footed Abalone (Hailotis iris) Larval/Post-Larval Processes. Journal of Applied Aquaculture, 23, 14–31.

Pereira-Filho, G. H., Amado-Filho, G. M., de Moura, R. L., Bastos, A. C., Guimarães, S. M., Salgado, L. T., et al. (2011). Extensive Rhodolith beds cover the summits of southwestern atlantic ocean seamounts. Journal of Coastal Research, 28(1), 261- 269.

Villas-Boas, A. (2014) Community structure of rhodolith-forming beds on the central Brazilian continental shelf. Helgoland Marine Research, 68, 27-35.

Witman, J. (1985) Refuges, Biological Disturbance, and Rocky Subtidal Community Structure in New England. Ecological Monographs, 55, 421–445.

Young, P. (1963) The kelp bass (Paralabrax clathratus) and its fishery, 1947-1958. Fish Bulletin, 1947–1958.

34 CHAPTER II TROPHIC STRUCTURE AND ENERGY FLOW WITHIN A RHODOLITH BED AT SANTA CATALINA ISLAND

ABSTRACT

In many coastal marine systems with low productivity, cross-habitat exchange of macroalgal material has been shown to have significant bottom-up effects. California rhodolith beds are slow-growing carbonate red algae that support diverse communities and are often adjacent to highly productive kelp beds. As the trophic structure and sources of productivity supporting this system were unknown, I examined energy flow, trophic structure, and temporal patterns using stable isotopes in a rhodolith bed off

Catalina Island. Using cluster analysis on isotopic signals of 12 invertebrate consumer taxa, I identified four trophic groups: planktivore, detritivore, herbivore, and predator.

The isotopic signature of organic matter within rhodoliths overlapped isotopically with the signature of both fresh and drift Macrocystis pyrifera, suggesting kelp contributed to the organic matter within sediments. Detritivores appeared to consume a mixture of sources suggesting sediment detritus was an amalgam of giant kelp M. pyrifera particulates derived from adjacent kelp beds and suspended particulate organic matter from the water column. Dominant food resources produced within the rhodolith bed appeared to be epiphytic red macroalgae that propagated on rhodoliths and contributed little to the food web relative to suspended particulate organic matter and M. pyrifera subsidies. As detritivores and predators were greatly influenced by kelp, temporal fluctuations of drift subsidies from adjacent kelp beds likely has dramatic effects on secondary production and community structure of the rhodolith community.

35 INTRODUCTION

Movement of nutrients among habitats involves material fluxes from a donor system to recipient systems and is increasingly recognized as an important factor influencing populations, communities, and food web structure (Polis et al. 1997). The relative importance of drift subsidies to aquatic food webs has long been debated (Mann

1988). In polar and temperate marine systems, kelps are a major source of primary production (Krumhansl & Scheibling 2012) and drift material is consumed locally or exported to adjacent low-productivity habitats such as beaches (Ince et al. 2007), the intertidal (Rodríguez 2003), offshore areas (Kelly et al. 2012), and submarine canyons

(Vetter 1985, Vetter and Dayton 1998, 1999) where it can be utilized by infaunal and epifaunal macroinvertebrates (Duggins et al. 1989, Ince et al. 2007, Kelly et al. 2012).

The role of these spatial subsidies can be particularly important to low productivity environments where community members are more reliant on this input (Britton-

Simmons et al. 2012).

Multiple factors can influence the flux of material from donor systems. These factors include productivity, temporal patterns in storm frequency and intensity, local geomorphology and current patterns, proximity of recipient systems to donor systems, and the perimeter to area ratio of recipient systems leading to differences in productivity in recipient systems (Gerard 1976, Gerard & North 1984, Polis & Holt 1996, Polis et al.

1997, Kelly et al. 2012). Kelp subsidies have been widely studied and the availability of kelp drift subsidy to internal and external systems change through time and space as individuals differentially senesce, and environmental factors such as local geomorphology, currents, wind, and wave motion vary (Gerard 1976, Harrold & Reed

36 1985). For example, the degree of exposure of a site affects kelp availability as greater diet contributions of kelp to invertebrates is observed at sheltered locations with reduced hydrodynamics, and likely reduced kelp export (Leclerc et al. 2013). Studies on the influence of seasonal variability in nutrient flux from kelp systems to low productivity foundation species are limited.

Rhodolith beds are poorly studied foundation species composed of free-living coralline algal nodules. These rhodolith beds are globally distributed (Foster 2001) and can support highly diverse communities (Foster 2001, Steller et al. 2003, Foster et al.

2007). Prior research has enumerated species within rhodolith communities, however little work has examined energy flow and trophic structure in this habitat or determined whether communities are supported by internally or externally generated productivity.

Rhodoliths provide increased habitat complexity to the benthos, through branching that creates interstitial spaces among and within rhodoliths, which may affect food availability and food retention, similar to kelp holdfasts that increase small scale heterogeneity influencing particulate food retention (Schaal et al. 2012). Rhodolith branching may trap algal particulates which may subsequently become enriched by microbial activity resulting in increased nutritive value via increased nitrogen content (Tenore & Hanson

1984, Duggins & Eckman 1997), and palatability through decreases in herbivore deterrent compounds (Duggins & Eckman 1997, Norderhaug et al. 2003, Schaal et al.

2011). Invertebrates resident to rhodolith beds are likely reliant on suspended particulate organic matter from the water column and sediment organic matter composed of many sources (Grall et al. 2006). If rhodoliths increase retention of drift algal subsidies, this

37 will likely benefit detritivore/deposit feeders in the beds, leading to increased abundance, size, and reproductive output of these invertebrates (Kelly et al. 2012).

Energy flow through natural systems has traditionally been examined by studying consumer gut contents. This approach alone, however, can be inadequate as gut contents give a short-term measure of ingested food, potentially over-representing indigestible food items, and identification of prey items can be difficult or require expert taxonomic knowledge (Jaschinski et al. 2011). In contrast, stable isotope analysis can be a powerful tool for the study of trophic relationships as it can integrate diet over longer time scales and, if prey sources are isotopically distinct, identify the relative contribution of prey

(Michener & Schell 1994, Fry 2006). Ratios of heavier to lighter carbon (C13/C12) and nitrogen (N15/N14), denoted by δ13C and δ15N respectively, are often used to explore food web relationships. Generally, carbon isotope ratios are used as an indicator of the source of primary production and nitrogen is used as an indicator of food web trophic level.

Differences in primary producer size and photosynthetic pathways cause differences in the isotopic ratios of algae (Raven et al. 2002), with carbon isotopic signatures of phytoplankton having low δ13C values relative to nearshore macroalgae (Raven et al.

2002). Due to this isotopic separation, the relative importance of pelagic

(phytoplankton), benthic (macroalgae), and mixtures of these food resources to a consumer can be evaluated if these isotopic values are known.

Rhodolith beds have recently been described around Santa Catalina Island off southern California, USA (Tompkins 2011) adjacent to productive kelp beds which seasonally produce and export kelp material (Gerard & North 1984, Harrold & Reed

1985). Kelp beds have been shown to be an important source of subsidies to herbivorous

38 invertebrates in adjacent habitats (Kelly et al. 2012). This study provides a model for how rhodolith bed communities may be supported. As rhodoliths have low organic content (6%) relative to calcium carbonate (94%), the contribution of rhodoliths to the food web was hypothesized to be low relative to other organic sources (Grall et al. 2006).

In this study, I examined the dynamics of food subsidies from macroalgal kelp beds to adjacent rhodolith beds off Santa Catalina Island. I hypothesized that rhodoliths act as substrate for macroalgae and trap drift kelp particulates, and that these were important food sources for herbivorous and detritivorous consumers. Specifically, I sought to (1) determine the main trophic groups structuring the rhodolith community food web and the primary trophic pathways connecting them, and (2) determine the influence of giant kelp drift through time to herbivorous epibenthic invertebrates within a Catalina rhodolith bed.

This is the first trophic study of this ecosystem in the Pacific and coastal California, and the first to examine temporal changes of herbivore diet in a rhodolith bed food web.

METHODS

Study Site

Santa Catalina Island is part of the Channel Islands archipelago in the Eastern

Pacific off the coast of southern California. The island sits in a Northwest-Southeast orientation and is exposed to warm water from the Southern California Countercurrent.

Diverse and productive kelp beds surround the island, propagating over rocky reefs, dominating the subtidal. Rhodolith beds cover sedimentary bottoms in protected coves on the Northeast-facing leeward side of the island (Fig. 1). The locations and percent carbonate cover of seven rhodolith beds were described by Tompkins (2011). Rhodolith beds range from 4 - 21 meters water depth, are located in bays and coves, and each bed is

39 composed of patchy aggregations of live rhodolith surrounded by dead rhodolith (non- pigmented) carbonate sand, with a gradient into more silicate sediment (Tompkins 2011).

Mooring chain orientation and disturbance creates channels of un-pigmented dead rhodolith straddeled by live material. Rhodolith bed food web structure was examined at the Isthmus Cove rhodolith bed (area = 1148 m2). This site was reported to have high average live rhodolith cover (~50 percent, Tompkins 2011).

To construct a rhodolith bed food web and to quantify energy flow through the system, samples of suspended particulate organic matter from offshore and nearshore water, sediment organic matter (SOM), epiphytic macroalgae on rhodoliths, fresh and drift kelp tissue, and invertebrate consumers were collected from the rhodolith bed at

Isthmus Cove and transported to the Wrigley Institute for Environmental Studies (WIES) using SCUBA. Samples were collected haphazardly across the entire bed area from patches of greatest live rhodolith cover. To compare temporal variation in isotopic signatures, sample collection for primary producers and consumers were made during summer (August 2012), spring (April 2013), and winter (December 2013). Details are listed in each section and in Table 1.

Figure 1. Map of Santa Catalina Island with inset of Isthmus cove and the rhodolith bed where collections of primary producers and consumers were made. (Adapted from Tompkins 2011).

40 To construct a rhodolith bed food web and to quantify energy flow through the system, samples of suspended particulate organic matter from offshore and nearshore water, sediment organic matter (SOM), epiphytic macroalgae on rhodoliths, fresh and drift kelp tissue, and invertebrate consumers were collected on SCUBA from the rhodolith bed at Isthmus Cove and transported to the Wrigley Institute for Environmental

Studies (WIES). Samples were collected haphazardly across the entire bed area but collected from patches of greatest live rhodolith cover. To compare temporal variation in isotopic signatures, sample collection for primary producers and consumers were made during summer (August 2012), spring (April 2013), and winter (December 2013).

Details are listed in each section and in Appendix B.

Water and sediment samples

To estimate the isotopic signature of water born nutrients or Suspended

Particulate Organic Matter hereafter (SPOM), seawater samples were collected from 4 km offshore and within Isthmus Cove, at 3m and 7m water depths using SCUBA in 1- gallon plastic zip bags (n = 10) pre-rinsed with DI water. These samples were divided into three 5-liter replicates. Sediment Organic Matter (SOM) may be an isotopically distinct food source available for consumers (Grall et al. 2006). To estimate an isotopic signature of the sediment organic matter, four rhodoliths were haphazardly collected from the Isthmus rhodolith bed, individually stored in plastic zipbags and transported to WIES, agitated in 50 ml of deionized water for 30 sec using a VWR multi-tube vortexer. Both

SPOM and SOM samples were filtered through precombusted (500°C for 4 hrs) 47mm glass microfiber filters (grade GF/F, Whatman) under low pressure (~5-7 mmHg) using a

41 GAST vacuum pump. Samples for SPOM and SOM were collected during summer

(August 2012), spring (April 2013), and winter (December 2013).

Macroalgal primary producers

Samples of macroalgae were collected to estimate the importance of local attached and adjacent drift production to the system. The dominant macroalgae (> 10% cover) included the red alga Polysiphonia spp. and giant kelp Macrocystis pyrifera drift tissue. To compare kelp drift tissue to fresh tissue, collections from attached M. pyrifera thalli (1 meter above the holdfast) were haphazardly made in the adjacent kelp bed, about

30 meters away from the Isthmus rhodolith bed. Samples of red algae and giant kelp were collected during summer (August 2012), spring (April 2013), and winter (December

2013).

Consumers

Samples of 12 conspicuous invertebrate consumers were collected during community surveys from the rhodolith bed surface (epifauna) by hand, and from within the sediment (infauna) using cores (6.5 cm diameter x 10 cm high). Consumers were the most abundant fauna available and were used to examine the importance of different primary producer inputs to the community. Epifaunal consumers included Conus californicus, Lirularia spp., Lytechinus pictus, Megastraea undosa, Parastichopus parvimensus, Podochela hemphilli, and infaunal consumers were Americardia biangulata, Limaria hemphilli, Dendraster excentricus, gammarid amphipods, polychaetes, and tanaids. These organisms were transported to WIES and held for 24

42 hours in flowing seawater to clear gut contents, and were sacrificed via freezing.

Replicates were of individuals with the exception of smaller infauna including gammarids (n = 16-44 per sample) and tanaids (n = 37-96 per sample) that were composed of pooled individuals from the same core to meet minimum mass spectrometry requirements for stable isotope analysis.

Filters for SPOM and SOM, and samples of macroalgae and consumers were all stored at -80°C at Catalina post-collection, transported to Moss Landing Marine

Laboratories, stored at -80°C, and thawed for isotope preparation. Filters were acidified with dilute HCl fumes to remove carbonates. Samples of fleshy algae were rinsed with deionized water and gently scrubbed to remove epiphytes, and consumers were extracted from their shell, test, cuticle, or tube. Both macroalgae and consumers were briefly acidified using 10% HCl only if rhodolith carbonate was present. All samples were dried at 60°C for 48 hours and ground to a fine powder using an agate mortar and pestle, then placed in tin capsules (Costech Analytical Technologies, Inc. Valencia, CA). Samples were weighed using a Sartorius CP2P microbalance, and sent to Idaho Stable Isotopes

Laboratory for isotopic analysis.

Sample preparation and stable isotope analysis

Stable isotope ratios were determined using an ECS 4010 (Elemental Combustion

System 4010) interfaced to a Delta V advantage mass spectrometer through the ConFlo

IV system at the Interdisciplinary Laboratory for Elemental and Isotopic Analysis

(ILEIA) lab, Idaho State University. The ratios of heavier to lighter stable isotopes for

43 carbon and nitrogen were determined. Data were expressed in the standard δ unit, where

3 δX = [(Rsample/Rstandard) - 1] x 10 . These values were reported as parts per thousand (‰).

⎛ 13C / 12C ⎞ 13C sample δ = ⎜ 13 12 ⎟ ⎝ C / CVPDB ⎠

Carbon ratios (δ13C/ δ12C) were relative to the global standard Vienna PeeDee Belemnite

(VPDB).

⎛ 15N / 14 N ⎞ 15N sample δ = ⎜ 15 14 ⎟ ⎝ N / Nair ⎠

15 14 Nitrogen ratios (δ N/ δ N) were reported relative to atmospheric N2. In house standards

(ISU Peptone, Costech Acetanilide, and DORM-3) were calibrated against international standards. Based on standards, the isotope measurement error (SD) was estimated to be

±0.07‰ δ15N and ±0.08‰ δ13C for ISU Peptone, 0.07‰ δ15N and 0.10‰ δ13C for

Costech Acetanilide, and 0.11‰ δ15N and 0.13‰ δ13C for DORM-3.

Data Analysis

A hierarchical cluster analysis using Ward’s minimum variance method separated carbon and nitrogen stable isotope ratios of consumers into trophic groups (Davenport &

Bax 2002, Grall et al. 2006, Carlisle et al. 2012). Stable Isotope Analysis in R (SIAR), a

Bayesian mixing model package used in conjunction with R, was used to determine the relative importance of different primary producers to consumers. This package took stable isotope signatures and fit a Bayesian model to this dietary information based upon a Gaussian likelihood with a continuous multivariate probability distribution prior on the mean (Semmens et al. 2009, Parnell et al. 2010). Use of this model was considered more

44 robust to other mixing models as it incorporated variability of sources, consumers, and trophic enrichment (Parnell et al. 2010).

To determine the relative contribution of sources to a consumer, consumer isotopic signatures must first be corrected for trophic enrichment. Carbon and nitrogen stable isotope values increase as energy moves through a food web and are altered by consumers that more readily lose the lighter 12C and 14N isotopes during assimilation and protein synthesis (Fry 2006). This enrichment of δ15N, called isotopic enrichment or fractionation, creates a reliable indicator of the trophic level of a consumer, while δ13C fractionates much less and is therefore a reliable indicator of a prey source (Fry 2006).

Consumer stable isotope values were corrected using a mean trophic enrichment factor for carbon (∆13C) of 1‰, and incorporated into the mixing models (DeNiro &

Epstein 1978, Ouisse et al. 2012). Consumer values were also corrected using a mean trophic enrichment for nitrogen (∆15N) of 3.4‰ applied to predator values (Vanderklift &

Ponsard 2003, Ouisse et al. 2012) and 2.5‰ applied to mixed diet consumers (Zanden &

Rasmussen 2001, Ouisse et al. 2012, Vafeiadou et al. 2013). This yields a rough estimation of fractionation for each group and is only an indication of a consumer’s trophic level and therefore an estimate of diet contributions. Species or taxa specific trophic enrichment factors (which require controlled laboratory studies) may help yield better approximations of trophic level position and source contributions (Moncreiff &

Sullivan 2001, Jaschinski et al. 2011), however these are currently unknown.

To determine the main trophic pathways and structure of the rhodolith community food web base for planktivores, detritivores, herbivores, and predatory feeding groups, a

SIAR mixing model was used to determine the relative contribution of SPOM, SOM, and

45 giant kelp Macrocystis pyrifera drift to the trophic groups identified by cluster analysis.

Predators were trophically corrected twice to determine the indirect contribution of primary producers that would be transferred (primary producer to prey, then from prey to predator). To determine if seasonal differences in stable isotope ratios existed across summer (August 2012), spring (April 2013) and winter (December 2013) for epibenthic invertebrates (Lirularia spp., Megastraea undosa and Lytechinus pictus), a one-way

ANOVA was conducted on each of the carbon and nitrogen isotope values. When a significant season effect was detected, a Tukey honest significant difference (HSD) multiple comparisons test was used to determine which season means differed. Finally, to determine the importance of food resources to epibenthic herbivorous invertebrates through time, a second SIAR mixing model was used. This model determined the temporal contribution of SPOM, SOM and drift giant kelp, to the diet of two potential herbivores (Lirularia spp. and Megastraea undosa) during summer (August 2012), spring

(April 2013), and winter (December 2013). Samples from spring of the red alga

Polysiphonia spp. did not yield enough sample material for conclusive values therefore samples collected during summer and winter seasons were combined and used to give an approximation of a signal for spring.

RESULTS

Primary Producers

The main sources considered in this study included pelagic-based offshore and nearshore particulate organic matter, rhodolith bed sediment organic matter, the epiphytic red algae Polysiphonia spp., and giant kelp M. pyrifera drift tissue present within the

46 rhodolith bed. Source carbon values spanned a wide range, ~13‰ δ13C, from -28.42 to -

13 15.33 ‰ δ C. Sources varied by carbon isotope values (ANOVA, F5,86 = 115.26,

P<0.001) with the most carbon depleted source being the epiphytic red alga Polysiphonia spp. (-28.42±0.98‰ δ13C), which was isotopically distinct relative to other sources

(Tukey HSD, P<0.001). Carbon isotope values of offshore (-23.02±0.48‰ δ13C) and nearshore (-22.49±0.85‰ δ13C) SPOM were similar (Tukey HSD, P=0.355), and were more enriched in carbon relative to Polysiphonia spp (Tukey HSD, P=<0.001). The most carbon-enriched sources were SOM (-17.88±1.65 δ13C), fresh kelp (-16.49±1.62‰ δ13C), and drift kelp tissue (-15.33±1.93‰ δ13C). Surprisingly, carbon isotopic values for sediment organic matter and fresh kelp were similar (Tukey HSD, P=0.011), and values for fresh kelp were similar to drift kelp (Tukey HSD, P<0.001), suggesting sediment organic matter may be composed of kelp derived organic matter from fresh or decaying kelp (Fig. 2A, Table 1). Nitrogen isotopic values varied by source (ANOVA, F5,86 =

115.26, P<0.001) with nearshore and offshore SPOM values appearing similar (Tukey

HSD, P=0.369), these values were more deplete (Tukey HSD, P<0.001) relative to

Polysiphonia spp, SOM, drift kelp, and fresh kelp which overlapped and were similar

(Tukey HSD, P=0.985).

Consumer trophic groups

Rhodolith bed trophic structure was built using 12 taxa that spanned three trophic levels. Cluster analysis revealed that the 12 consumer taxa were best described by 4 distinct trophic groups (Fig. 2B). Using published studies on diet, other isotope studies, and isotopic position, the groups were assigned a feeding description including

47 planktivore, detritivore, herbivore, or predator. The stable isotope ratios of planktivores were the most deplete in nitrogen, followed by the detritivore group, followed by herbivores, and then leading to the most enriched nitrogen ratios of consumers. The results from cluster analysis identified a planktivore group composed of the bivalves

Americardia biangulata and Limaria hemphilli. The detritivore group was composed of the echinoderms Dendraster excentricus and Parastichopus parvimensus, gammarid amphipods, the gastropod Megastraea undosa, and the urchin Lytechinus pictus. The herbivore group was composed of the gastropod Lirularia spp. and tanaid crustaceans.

The predatory group was composed of polychaetes, the decapod Podochela hemphilli, and the gastropod Conus californicus.

48

Figure 2. δ13C versus δ15N biplot of invertebrate consumer isotope values (mean±SD) pooled across sampling times from Isthmus Cove rhodolith bed. (A) Potential food resources displayed with corrected isotope values (3.5-2.5‰ δ15N, 1‰ δ13C) for consumers. (B) Uncorrected isotope values for trophic consumer groups enclosed by colored ellipses from cluster analysis, insert shows a dendrogram with each node representing a taxon or species. Gray circles are source values and convex hulls encompass sources: the red alga Polysiphonia spp., offshore Suspended Particulate Organic Matter - SPOM (off), nearshore Suspended Particulate Organic Matter - SPOM (on), Sediment Organic Matter (SOM), Fresh kelp, and Drift kelp. Symbol and color denote feeding guild and number denotes species or taxa: blue triangles = planktivore, 1 - Americardia biangulata, 2 - Limaria hemphilli, brown inverted triangles = detritivore, 3 - Dendraster excentricus, 4 - Parastichopus parvimensus, 5 - Megastraea undosa, 6 - Gammarid crustaceans, 7 - Lytechinus pictus, green squares = herbivore, 8 - Tanaid crustaceans, 9 - Lirularia spp., black circles = Predators, 10 - Polychaetes (scale worms), 11 - Podochela hemphilli, 12 - Conus californicus.

49 Contribution of sources to consumer trophic groups

Due to carbon isotopic separation in nearshore suspended particulate organic matter (SPOM), drift kelp tissue, and sediment organic matter (SOM), a SIAR mixing model could be used to determine the diet contributions of these sources to the planktivore, detritivore, herbivore, and predator trophic groups. The SIAR model revealed differences in source contributions to trophic groups (Fig 3). Suspended particulate organic matter dominated the diet of planktivores (85.1%) with smaller contributions from SOM (9.1%) and Macrocystis drift (5.9%). Detritivore diet was characterized by contributions from all sources including SOM (43.6%), SPOM (31.8%) and Macrocystis drift (24.6%). Herbivore diet was also composed of mixed sources including Macrocystis drift (46.1%), SOM (32.6%), and SPOM (21.3%). Predator diet appeared to be composed mostly of detritivores as suggested by the large contribution of

SOM (67.2%), with much smaller contributions from Macrocystis drift (22.2%), and

SPOM (10.6%).

50

Figure 3. Diet contribution of pooled SPOM, SOM, and drift kelp to planktivore, detritivore, herbivore, and predator trophic groups from a SIAR mixing model. Data are pooled isotope values from rhodolith bed consumers and prey across sampling times from Isthmus Cove, Catalina Island. Temporal Isotopic Variability of Epibenthic Invertebrates

The carbon and nitrogen stable isotope values of herbivores varied by season (Fig.

4 A, B, C). Stable isotope values for Lirularia spp. differed by season for both carbon

(ANOVA, F2,13 = 5.521, P = 0.018) and nitrogen (ANOVA, F2,13 = 34.938, P<0.001), with more enriched nitrogen values in winter than spring (Tukey HSD, P = 0.01) and intermediate values in summer. Stable isotope ratios for Megastraea undosa differed by season for both carbon (ANOVA, F2,13 = 20.139, P<0.001) and nitrogen (ANOVA, F2,13

= 11.485, P = 0.001), with greater nitrogen isotope values in winter and summer than spring (Tukey HSD, P = 0.01). Stable isotope signatures for the urchin Lytechinus pictus did not differ between spring and winter for carbon (t-test, t = 2.131, df = 11, P = 0.056) or nitrogen (t-test, t = 0.791, df = 11, P = 0.446) and values were distant from the predicted food sources.

51 Temporal Shifts of Epibenthic Invertebrate Diet

Temporal fluctuations in consumer diet (Lirularia spp. and Megastraea undosa) were detected using a SIAR mixing model. The SIAR model revealed that SPOM, SOM, and M. pyrifera drift tissue contributions varied for consumers through time. The contribution of drift kelp was temporally variable for Lirularia spp. with contributions varying from summer, spring, to winter with values of 79.5%, 35.6%, and 40.3% respectively (Fig. 5). The contribution of drift kelp was seasonally less variable for M. undosa with contributions from summer, spring, to winter of 34.6%, 34.5%, and 40.6%, respectively (Fig 5). The contribution of sediment organic matter was seasonally variable and similar for both epibenthic inverts, with the lowest contribution in summer, intermediate values in spring, and the greatest contributions during winter. The percent contributions of SOM from winter, to spring, to summer for Lirularia spp. were 9.0%,

31.6%, and 50.3%, and for M. undosa were 19.5%, to 29.3%, to 50.1% (Fig. 5).

52 A) Summer 14

12 Polysiphonia SOM Drift Kelp 10

8 SPOM 6 4

-30 -25 -20 -15 -10

B) Spring 14 Figure 4. δ13C versus δ15N biplot of rhodolith bed primary 12 Polysiphonia producers and potential SOM herbivorous consumers by season. A - Summer (August 10 Drift Kelp 2012), B - Spring (April 2013), and C - Winter (December

8 2013) from samples collected in SPOM Isthmus Cove. Potential herbivorous consumers: gray 6 squares: denote the gastropod Lirularia spp., black squares

4 denote Wavy Turban Snail Megastraea undosa, and white -30 -25 -20 -15 -10 squares denote the White Urchin Lytechinus pictus. C) Winter Consumer stable isotope values 14 were corrected 2.5 ‰ for δ15N and 1 ‰ for δ13C. Sources

12 Drift Kelp included in the mixing model Polysiphonia were nearshore SPOM, SOM, SOM and drift kelp. 10

8 SPOM

6

4

-30 -25 -20 -15 -10

53

Figure 5. Percent diet contribution to the gastropods (A) Lirularia spp. and (B) Megastraea undosa of suspended particulate organic matter, sediment organic matter (SOM) and Macrocystis pyrifera drift kelp tissue. Consumer stable isotope values were corrected by 2.5 ‰ δ15N and 1 ‰ δ13C.

Conceptual model of the rhodolith food web

Incorporating pooled primary producer and consumer isotope values yielded a generalized food web model (Fig. 6). The food web sources representing major pathways incorporated into the model (SPOM, SOM, and drift kelp) contributed differentially to consumers, and indirectly to predators. The coloring of trophic group ellipses and scaling of arrows summarizes the degree of contribution of the different sources. Using this model the flow of energy from suspended particulate organic matter, sediment organic matter, and drift kelp can be traced to consumers and predators and the relative importance of pathways in supporting the food web can be examined.

54

Figure 6. Generalized rhodolith bed food web model based on δ13C and δ15N biplot, incorporating pooled primary producers and consumers from Isthmus Cove. Flow of energy follows the same orientation as the isotope biplot. Ellipse color denotes proportion of each source box: SPOM = suspended particulate organic matter (blue), SOM = sediment organic matter (light brown), and drift kelp subsidy (green). Arrows are scaled to match percent contribution of a source.

DISCUSSION

Although rhodolith beds are globally distributed habitats (Foster 2001) and

recognized as enhancing benthic macroalgal, invertebrate, and vertebrate abundance and

biodiversity (Foster 2001, Steller et al. 2003, Kamenos et al. 2004), little work has been

done to examine the organization of rhodolith bed food webs (Grall et al. 2006) and the

role of spatial subsidies supporting them. My results demonstrate the importance of

55 detritus to the rhodolith bed food web and are consistent with trophic dynamics in an

Atlantic rhodolith bed (Grall et al. 2006) and similar to what has been found in other communities such as seagrass beds (Moncreiff & Sullivan 2001) and mangroves

(Bouillon et al. 2008). As a detritus-based system, rhodolith bed food webs appear to rely on a variety of sources including algal-derived material.

Isotopic results support my hypothesis that rhodolith beds receive important nutrient subsidies from adjacent kelp beds. Pooled sediment organic matter and drift kelp isotope values were comparable to those measured from fresh attached kelp from nearby beds suggesting the sediment receives a dominant organic input from this species of macroalgae. The dominant sources of primary production for detritivores, herbivores, and predators in the Isthmus Cove rhodolith food web were sediment organic matter, which appeared to be composed mostly of drift kelp, and thus likely derived from adjacent kelp beds. This large contribution from fresh or decaying kelp in driving the community is similar to what has been found in studies conducted within kelp beds

(Schaal et al. 2009, 2012, Leclerc et al. 2013). In contrast, Grall et al. (2006) concluded the Atlantic rhodolith food web they studied was detrital-based, however they concluded that it received little contribution from macroalgae, instead hypothesizing large contributions from microalgae.

Kelp tissue appeared to contribute most to the diet of herbivores examined in this study. The pooled isotopic signatures of the gastropod Lirularia spp. and tanaid crustaceans were most similar to drift kelp, suggesting a majority of their diet was derived from this source. Tanaids are likely selective deposit feeding omnivores

(Blazewicz-Paszkowycz & Ligowski 2002) that consume detritus (Bracken et al. 2007),

56 macroalgae, or epiphytes (Blazewicz-Paszkowycz & Ligowski 2002). Tanaids may be deposit feeders consuming detritus, micrograzing on rhodoliths or the sediment, as tanaids have been found to be more detritivorous than carnivorous as previously thought

(Gutu 1986, Blazewicz-Paszkowycz & Ligowski 2002, Gillies et al. 2011). Other invertebrates, such as the gastropod Megastraea undosa, were characterized by an enriched carbon diet, and appeared to consume giant kelp consistently, potentially subsidizing their diet and supporting their primary preference for kelp (Cox & Murray

2005). The importance of giant kelp to the epibenthic inverts Lirularia spp. and

Megastraea undosa support our observations that individuals were found on drift kelp blades within the bed and hypothesized to be grazing the surface of these blades.

Although kelp appeared to be an important diet source to M. undosa and Lirularia spp., the importance was temporally variable for Lirularia spp., potentially as the availability of kelp varied differently for this taxa or they had a greater seasonal preference than M. undosa for kelp (Gerard 1976, Harrold & Reed 1985). The variable impact of kelp to herbivore diet suggests that kelp input should be examined in future diet studies of rhodolith community members.

Pooled SPOM isotope values were distinct relative to the more enriched SOM and drift kelp signatures. Instead, they were similar to those reported from water collected in other studies off southern California (Page et al. 2008, Schaal et al. 2012), deplete in

δ13C, and similar to SPOM from samples collected offshore, and unlikely to have been influenced by adjacent kelp beds. My mixing models indicated that SPOM was the dominant carbon source for rhodolith bed planktivorous invertebrates, indicating spatial subsidies from water column based sources are important in rhodolith bed food webs.

57 Additional long-term sampling of SPOM in the vicinity of rhodolith beds could better elucidate the seasonal importance of this source (Miller et al. 2013). While pooled isotopic values for SPOM collected from nearshore and offshore water were similar, I did observe seasonal variation. During summer, values of both carbon and nitrogen in nearshore water became enriched compared to offshore (Table 1). Seasonal changes could be due to differential mixing, different growth and species compositions of phytoplankton (Page et al. 2008), or potential enrichment by nearshore algal particulates during summer.

While several studies have suggested that suspension feeders can assimilate kelp- derived carbon (Duggins & Eckman 1997, Norderhaug et al. 2003), in this study, the suspension feeding bivalves Americardia biangulata and Limaria hemphilli appear to rely on SPOM derived from offshore sources rather than nearshore kelp particulates.

Because suspension feeders can utilize different size classes of SPOM, their isotopic signatures can be more deplete compared to available SPOM within the water (Grall et al. 2006). The bivalves that I sampled in this study have more nitrogen-depleted isotopic signatures relative to SPOM and SOM, despite living as infaunal filter feeders (Grall et al. 2006). Apparently, these bivalves rely primarily upon SPOM and are thus isotopically distinct from other primary consumers, suggesting an alternate, non kelp-derived, food resource (Grall et al. 2006).

The detritivores in this study were influenced by benthic production, as they had isotopically enriched signatures relative to the isotopic signatures of planktivorous filter- feeding bivalves. Detritivores in this study are likely suspension or deposit feeders consuming suspended particulates or particulates on or within the sediment, similar to

58 infaunal and epifaunal selective deposit feeders found within an Atlantic rhodolith bed

(Grall et al. 2006). Kelp particles could be utilized by the sand dollar Dendraster excentricus as they are deposit feeders capable of trapping large particles (Timko 1976) and Parastichopus parvimensus as they are capable of consuming small kelp particles on the sediment surface (Yingst 1982). Megastraea undosa prefers kelp, however no work has been conducted on whether they are capable of consuming smaller particles (Cox &

Murray 2005), whereas gammarid amphipods consume both fresh and decaying algae

(Martin 1966), and Lytechinus pictus primarily consumes juvenile kelps (Dean et al.

2009). The high degree of isotopic overlap of detritivores suggests that these species have similar food resources and potentially similar feeding strategies.

The temporal assessment of isotopic signatures allowed for identifying a significant temporal change in the isotopic signatures of both Lirularia spp. and

Megastraea undosa, suggesting a feeding shift to a non kelp-derived food resource during spring. During spring, the stable isotope signatures of these herbivores became more depleted in nitrogen, suggesting (1) a significant loss of food resources utilized during summer and winter, or (2) the influx of other food resources such as biofilm or benthic diatoms, living on rhodoliths or within the sediment, increased (Grall et al. 2006).

Similar to Grall et al. (2006), separation of biofilm from rhodoliths was difficult and collections of surface films did not yield sufficient samples for an isotope measurement.

The importance of microphytobenthos, mostly microalgae and bacteria, is still unknown and warrants further investigation as a potential food resource (Grall et al. 2006).

Regardless of the identity of this unknown source, it appears to be seasonally important along with drift kelp in the diet of Lirularia spp., M. undosa, as well as white urchins L.

59 pictus. The temporal variability of isotopic signatures of Lirularia spp. and M. undosa may have dramatic effects on mixing models as their isotopic signatures depend on when these consumers are sampled and this temporal variation should be considered in food web models (Antonio & Richoux 2014).

Invertebrate predator taxa sampled in the rhodolith bed appear to mainly consume prey originating from the detritivore group. Predators do not display an isotopic enrichment indicative of large contributions from planktivorous or herbivorous invertebrates but have significant influence from detritivorous prey, similar to other studies, suggesting a reliance on the detrital pathway (Grall et al. 2006, Schaal et al.

2012). Polychaetes, the decapod Podochela hemphilli, and the gastropod Conus californicus, all appear to consume detritivorous prey, reinforcing the importance of the sources of detritus including pelagic derived food and kelp to this system.

All of the trophic consumer groups sampled (planktivore, detritivore, herbivore, and predator) were potential prey for higher-level predators such as fishes, which were observed foraging within the rhodolith beds. The fishes observed most often within rhodolith beds include Senorita Oxyjulis californica, Rock wrasse Halichoeres semicinctus, Kelp bass Paralabrax clathratus, and Sheephead Semicossyphus pulcher.

Observations and gut content analysis of these fishes in Catalina suggest that they may forage on many of the invertebrates found within the rhodolith beds such as crustaceans, bivalves, gastropods, and ophiuroids (Hobson & Chess 1986, 2001). Incorporating these mobile predators into future food web studies will create a more complete food web depiction and may reveal connectivity to higher trophic levels and the food webs of adjacent foundation species.

60 As kelps are ubiquitous, have high growth rates, and produce large amounts of biomass exported by blade erosion and fragmentation to many different systems (Vetter

& Dayton 1999, Ince et al. 2007, Kelly et al. 2012, Krumhansl & Scheibling 2012), they contribute greatly to secondary production in adjacent systems (Duggins et al. 1989,

Kelly et al. 2012). Catalina rhodolith beds likely may rely on kelp subsidies, similar to other detrital based systems such as beaches (Ince et al. 2007), the intertidal (Rodríguez

2003), offshore low-productivity habitats (Kelly et al. 2012), and submarine canyons

(Vetter 1985, Vetter and Dayton 1998, 1999). These studies have shown kelp drift provides invertebrates with a food subsidy fueling levels of secondary production which with only locally available food resources would be unsustainable (Ince et al. 2007).

However, exposure greatly affects retention of subsidies as kelp bed sites with reduced exposure and increased retention revealed that isotopic enrichment occurs in sediment organic matter, organic matter within kelp holdfasts, and organic matter on rock surfaces, all indicating the large scale influence of kelp organic matter to a local system (Leclerc et al. 2013). The impact of kelp is also seasonally variable as kelp growth and drift production varies (Gerard & North 1984, Harrold & Reed 1985), and storms create variability in drift kelp retention (Vetter 1985, Vetter & Dayton 1998). Distance from kelp sources can also affect utilization as decreases in kelp contribution to diet occurred at distances of around 80 meters from a kelp bed to urchins (Kelly et al. 2012). As kelp beds are adjacent to all rhodolith beds at Santa Catalina Island and these kelp subsidies do appear to contribute toward the main trophic pathway, fluctuations of kelp productivity and drift biomass to rhodolith beds may have large impacts to the rhodolith community, particularly in southern California where kelp beds are widespread. The

61 influence of kelp beds via drift subsidies should be considered in future studies of rhodolith communities and in their management.

62 LITERATURE CITED

Antonio, E. & Richoux, N. (2014) Trophodynamics of three decapod crustaceans in a temperate estuary using stable isotope and fatty acid analyses. Marine Ecology Progress Series, 504, 193–205.

Blazewicz-Paszkowycz, M. & Ligowski, R. (2002) Diatoms as food source indicator for some Antarctic Cumacea and Tanaidacea (Crustacea). Antarctic Science, 14, 11–15.

Bouillon, S., Connolly, R.M. & Lee, S.Y. (2008) Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. Journal of Sea Research, 59, 44–58.

Bracken, M., Gonzalez-Dorantes, C. & Stachowicz, J. (2007) Whole-community mutualism: associated invertebrates facilitate a dominant habitat-forming seaweed. Ecology, 88, 2211–9.

Britton-Simmons, K.H., Rhoades, A.L., Pacunski, R.E., Galloway, A.W.E., Lowe, A.T., Sosik, E. a., Dethier, M.N. & Duggins, D.O. (2012) Habitat and bathymetry influence the landscape-scale distribution and abundance of drift macrophytes and associated invertebrates. Limnology and Oceanography, 57, 176–184.

Carlisle, A., Kim, S. & Semmens, B. (2012) Using stable isotope analysis to understand the migration and trophic ecology of northeastern Pacific white sharks (Carcharodon carcharias). PLoS ONE, 7, e30492.

Cox, T.E. & Murray, S.N. (2005) Feeding preferences and the relationships between food choice and assimilation efficiency in the herbivorous marine snail Lithopoma undosum (Turbinidae). Marine Biology, 148, 1295–1306.

Davenport, S. & Bax, N. (2002) A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Canadian Journal of Fisheries and Aquatic Sciences, 530, 514–530.

Dean, T., Thies, K. & Lagos, S. (1989) Survival of Juvenile Giant Kelp: The Effects of Demographic Factors,Competitors, and Grazers. Ecology, 70, 483–495.

DeNiro, M. & Epstein, S. (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica et cosmochimica acta, 42(5), 495-506.

Duggins, D. & Eckman, J.E. (1997) Is kelp detritus a good food for suspension feeders? Effects of kelp species, age and secondary metabolites. Marine Biology, 128, 489– 495.

Duggins, D., Simenstad, C. & Estes, J. (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science(Washington).

63 Foster, M.S. (2001) Rhodoliths: between rocks and soft places. Journal of Phycology, 37, 659–667.

Foster, M.S., McConnico, L., Lundsten, L., Wadsworth, T., Kimball, T., Brooks, L., Medina-Lopez, M., Riosmena-Rodriguez, R., Hernandez-Carmona, G. & Vasquez- Elizondo, R. (2007) Diversity and natural history of a Lithothamnion muelleri- Sargassum horridum community in the Gulf of California. Ciencias Marinas, 33, 367.

Fredriksen, S. (2003) Food web studies in a Norwegian kelp forest based on stable isotope (δ13C and δ15N) analysis. Marine Ecology Progress Series, 260, 71–81.

Fry, B. (2006) Stable isotope ecology. Springer.

Gerard, V. (1976) Some Aspects of Material Dynamics and Energy Flow in a Kelp Forest in Monterey Bay, California. Ph.D. Dissertation, 172 pp. University of California, Santa Cruz.

Gerard, V. & North, W. (1984) Measuring growth, production, and yield of the giant kelp, Macrocystis pyrifera. Eleventh International Seaweed Symposium.

Gillies, C., Stark, J., Johnstone, G. & Smith, S. (2011) Carbon flow and trophic structure of an Antarctic coastal benthic community as determined by δ13C and δ15N. Estuarine, Coastal and Shelf Science, 97, 44–57.

Grall, J., Leloch, F., Guyonnet, B. & Riera, P. (2006) Community structure and food web based on stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. Journal of Experimental Marine Biology and Ecology, 338, 1–15.

Gutu, M. (1986) Description of Apseudes olimpiae n. sp. and of Tanabnormia cornicauda ng, n. sp.(Crustacea, Tanaidacea). Travaux du Muséum National d’Histoire naturelle “Grigore Antipa,” 30, 129–133.

Harrold, C. & Reed, D.C. (1985) Food Availability , Sea Urchin Grazing , and Kelp Forest Community Structure. Ecology, 66, 1160–1169.

Hobson, E. & Chess, J. (1986) Relationships among fishes and their prey in a nearshore sand community off southern California. Environmental Biology of Fishes, 17(3), 201-226.

Hobson, E.S. & Chess, J.R. (2001) Influence of trophic relations on form and behavior among fishes and benthic invertebrates in some California marine communities. Environmental Biology of Fishes, 60(4), 411-457.

64 Ince, R., Hyndes, G. a., Lavery, P.S. & Vanderklift, M. a. (2007) Marine macrophytes directly enhance abundances of sandy beach fauna through provision of food and habitat. Estuarine, Coastal and Shelf Science, 74, 77–86.

Jaschinski, S., Brepohl, D. & Sommer, U. (2011) Seasonal variation in carbon sources of mesograzers and small predators in an eelgrass community: stable isotope and fatty acid analyses. Marine Ecology Progress Series, 431, 69–82.

Kaehler, S., Pakhomov, E., Kalin, R. & Davis, S. (2006) Trophic importance of kelp- derived suspended particulate matter in a through-flow sub-Antarctic system. Marine Ecology Progress Series, 316, 17–22.

Kamenos, N. a., Moore, P. & Hall-spencer, J.M. (2004) Small-scale distribution of juvenile gadoids in shallow inshore waters; what role does maerl play? ICES Journal du Conseil, 61(3), 422–429.

Kelly, J., Krumhansl, K. & Scheibling, R. (2012) Drift algal subsidies to sea urchins in low-productivity habitats. Marine Ecology Progress Series, 452, 145–157.

Krumhansl, K. & Scheibling, R. (2012) Production and fate of kelp detritus. Marine Ecology Progress Series, 467, 281–302.

Leclerc, J.-C., Riera, P., Leroux, C., Lévêque, L., Laurans, M., Schaal, G. & Davoult, D. (2013) Trophic significance of kelps in kelp communities in Brittany (France) inferred from isotopic comparisons. Marine Biology, 160, 3249–3258.

Lowe, A.T., Galloway, A.W.E., Yeung, J.S., Dethier, M.N. & Duggins, D.O. (2014) Broad sampling and diverse biomarkers allow characterization of nearshore particulate organic matter. Oikos, 123(11), 1341-1354.

Mann, K.H. (1988) Production and use of detritus in various freshwater , estuarine , and coastal rnarine ecosystems. Limnology and Oceanography, 33, 910-930.

Martin, A. (1966) Feeding and digestion in two intertidal gammarids: Marinogammarus obtusatus and M. pirloti. Journal of Zoology, 515–525.

Miller, R.J., Page, H.M. & Brzezinski, M. (2013) δ13C and δ15N of particulate organic matter in the Santa Barbara Channel: drivers and implications for trophic inference. Marine Ecology Progress Series, 474, 53–66.

Moncreiff, C. & Sullivan, M. (2001) Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stable isotope analyses. Marine Ecology Progress Series, 215, 93–106.

65 Norderhaug, K.M., Fredriksen, S. & Nygaard, K. (2003) Trophic importnace of Laminaria hyperborea to kelp forest consumers and the importance of bacterial degradation to food quality. Marine Ecology Progress Series, 255, 135–144.

Ouisse, V., Riera, P., Migné, A., Leroux, C. & Davoult, D. (2012) Food web analysis in intertidal Zostera marina and Zostera noltii communities in winter and summer. Marine Biology, 159, 165–175.

Page, H.M., Brooks, A. & Kulbicki, M. (2013) Stable isotopes reveal trophic relationships and diet of consumers in temperate kelp forest and coral reef ecosystems. Oceanography, 26(3), 180-189.

Page, H.M., Reed, D., Brzezinski, M., Melack, J. & Dugan, J. (2008) Assessing the importance of land and marine sources of organic matter to kelp forest food webs. Marine Ecology Progress Series, 360, 47–62.

Parnell, A.C., Inger, R., Bearhop, S. & Jackson, A.L. (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE, 5, e9672.

Polis, G., Anderson, W. & Holt, R. (1997) Toward an Integration of Landscape and Food Web Ecology: The Dynamics of Spatially Subsidized Food Webs. Annual review of ecology and systematics, 28, 289–316.

Polis, G. & Holt, R. (1996) Time, space, and life history: influences on food webs. Food webs, 435-460.

Raven, J., Johnston, A. & Kübler, J. (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Functional Plant Biology, 29(3), 355-378.

Rodríguez, S.R. (2003) Consumption of drift kelp by intertidal populations of the sea urchin Tetrapygus niger on the central Chilean coast : possible consequences at different ecological levels. Marine Ecology Progress Series, 251, 141–151.

Schaal, G., Riera, P. & Leroux, C. (2009) Trophic significance of the kelp Laminaria digitata (Lamour.) for the associated food web: a between-sites comparison. Estuarine, Coastal and Shelf Science, 85, 565–572.

Schaal, G., Riera, P. & Leroux, C. (2010) Trophic ecology in a Northern Brittany (Batz Island, France) kelp (Laminaria digitata) forest, as investigated through stable isotopes and chemical assays. Journal of Sea Research, 63, 24–35.

Schaal, G., Riera, P. & Leroux, C. (2012) Food web structure within kelp holdfasts (Laminaria): a stable isotope study. Marine Ecology, 33, 370–376.

66 Semmens, B.X., Moore, J.W. & Ward, E.J. (2009) Improving Bayesian isotope mixing models: a response to Jackson et al. (2009). Ecology letters, 12, E6–8.

Steller, D.L., Riosmena-rodríguez, R. & Foster, M.S. (2001) Living Rhodolith Bed Ecosystems in the Gulf of California. Atlas of Coastal Ecosystems in the Western Gulf of California: Tracking Limestone Deposits on the Margin of a Young Sea (2009): 72-82.

Steller, D.L., Riosmena-Rodriguez, R., Foster, M.S.M. & Roberts, C. a. C. (2003) Rhodolith bed diversity in the Gulf of California: the importance of rhodolith structure and consequences of disturbance. Aquatic Conservation: Marine and Freshwater Ecosystems, 13, S5–S20.

Tenore, K. & Hanson, R. (1984) Changes in composition and nutritional value to a benthic deposit feeder of decomposing detritus pools. Bulletin of marine science, 35, 299–311.

Timko, P. (1976) Sand dollars as suspension feeders: a new description of feeding in Dendraster excentricus. The Biological Bulletin, 151, 247-259.

Tompkins, P.A. (2011) Distribution, Growth, and Disturbance of Catalina Island Rhodoliths. Masters Thesis. Moss Landing Marine Laboratories, San Jose State University.

Vafeiadou, A.-M., Materatski, P., Adão, H., Troch, M. & Moens, T. (2013) Food sources of macrobenthos in an estuarine seagrass habitat (Zostera noltii) as revealed by dual stable isotope signatures. Marine Biology, 160, 2517–2523.

Vanderklift, M. a & Ponsard, S. (2003) Sources of variation in consumer-diet delta 15N enrichment: a meta-analysis. Oecologia, 136, 169–82.

Vetter, E.W. (1985) Detritus-based patches of high secondary production in the nearshore benthos. Marine Ecology Progress Series, 120(1), 251-262.

Vetter, E.W. & Dayton, P.K. (1998) Macrofaunal communities within and adjacent to a detritus-rich submarine canyon system. Deep Sea Research Part II: Topical Studies in Oceanography, 45, 25–54.

Vetter, E. & Dayton, P. (1999) Organic enrichment by macrophyte detritus, and abundance patterns of megafaunal populations in submarine canyons. Marine Ecology Progress Series, 120, 251-262.

Yingst, J. (1982) Factors influencing rates of sediment ingestion by Parastichopus parvimensis (Clark), an epibenthic deposit-feeding holothurian. Estuarine, Coastal and Shelf Science, 14(2), 119-134.

67 Zanden, M. Vander & Rasmussen, J. (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnology and oceanography, 46, 2061–2066.

68 CONCLUSIONS

This study described the community associated with rhodolith beds at Santa

Catalina Island and determined potential sources of primary production supporting the rhodolith bed. These data establish important baseline information on species composition, richness and abundance, imperative to making comparisons within Catalina

Island rhodolith beds through time and to other Channel Island rhodolith beds in future studies. Overall the rhodolith bed supported greater overall abundances of attached macroalgae, herbivorous gastropods, and infauna than adjacent sand habitat. Potential drivers increasing richness relative to sand are that rhodoliths provide substrate for epiphytes, increased microhabitats for infauna, and potentially trap food resources creating an important food resource for the community. We determined the main trophic pathways supporting common rhodolith bed invertebrates and determined kelp subsidies from adjacent kelp beds may contribute toward this main trophic pathway. Fluctuations of kelp productivity and drift biomass from adjacent kelp beds to rhodolith beds may have large impacts to the rhodolith community. The influence of kelp beds via drift subsidies should be considered in future studies of rhodolith communities and in their management.

69 LITERATURE CITED

Antonio, E. & Richoux, N. (2014) Trophodynamics of three decapod crustaceans in a temperate estuary using stable isotope and fatty acid analyses. Marine Ecology Progress Series, 504, 193–205.

Blazewicz-Paszkowycz, M. & Ligowski, R. (2002) Diatoms as food source indicator for some Antarctic Cumacea and Tanaidacea (Crustacea). Antarctic Science, 14, 11–15.

Bouillon, S., Connolly, R.M. & Lee, S.Y. (2008) Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. Journal of Sea Research, 59, 44–58.

Bracken, M., Gonzalez-Dorantes, C. & Stachowicz, J. (2007) Whole-community mutualism: associated invertebrates facilitate a dominant habitat-forming seaweed. Ecology, 88, 2211–9.

Britton-Simmons, K.H., Rhoades, A.L., Pacunski, R.E., Galloway, A.W.E., Lowe, A.T., Sosik, E.A., Dethier, M.N. & Duggins, D.O. (2012) Habitat and bathymetry influence the landscape-scale distribution and abundance of drift macrophytes and associated invertebrates. Limnology and Oceanography, 57, 176–184.

Carlisle, A., Kim, S. & Semmens, B. (2012) Using stable isotope analysis to understand the migration and trophic ecology of northeastern Pacific white sharks (Carcharodon carcharias). PLoS ONE, 7, e30492.

Cox, T.E. & Murray, S.N. (2005) Feeding preferences and the relationships between food choice and assimilation efficiency in the herbivorous marine snail Lithopoma undosum (Turbinidae). Marine Biology, 148, 1295–1306.

Davenport, S. & Bax, N. (2002) A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Canadian Journal of Fisheries and Aquatic Sciences, 530, 514–530.

Dean, T., Thies, K. & Lagos, S. (1989) Survival of Juvenile Giant Kelp: The Effects of Demographic Factors, Competitors, and Grazers. Ecology, 70, 483–495.

DeNiro, M. & Epstein, S. (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica et cosmochimica acta, 42(5), 495-506.

Duggins, D. & Eckman, J.E. (1997) Is kelp detritus a good food for suspension feeders? Effects of kelp species, age and secondary metabolites. Marine Biology, 128, 489– 495.

Duggins, D., Simenstad, C. & Estes, J. (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science(Washington), 245, 170-173.

70 Foster, M.S. (2001) Rhodoliths: between rocks and soft places. Journal of Phycology, 37(5), 659–667.

Foster, M.S., McConnico, L., Lundsten, L., Wadsworth, T., Kimball, T., Brooks, L., Medina-Lopez, M., Riosmena-Rodriguez, R., Hernandez-Carmona, G. & Vasquez- Elizondo, R. (2007) Diversity and natural history of a Lithothamnion muelleri- Sargassum horridum community in the Gulf of California. Ciencias Marinas, 33, 367.

Fredriksen, S. (2003) Food web studies in a Norwegian kelp forest based on stable isotope (δ13C and δ15N) analysis. Marine ecology Progress series, 260, 71–81.

Fry, B. (2006) Stable isotope ecology. Springer.

Gerard, V. (1976) Some Aspects of Material Dynamics and Energy Flow in a Kelp Forest in Monterey Bay, California. Ph.D. Dissertation, 172 pp. University of California, Santa Cruz.

Gerard, V. & North, W. (1984) Measuring growth, production, and yield of the giant kelp, Macrocystis pyrifera. Eleventh International Seaweed Symposium.

Gillies, C., Stark, J., Johnstone, G. & Smith, S. (2011) Carbon flow and trophic structure of an Antarctic coastal benthic community as determined by δ13C and δ15N. Estuarine, Coastal and Shelf Science, 97, 44–57.

Grall, J., Leloch, F., Guyonnet, B. & Riera, P. (2006) Community structure and food web based on stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. Journal of Experimental Marine Biology and Ecology, 338, 1–15.

Gutu, M. (1986) Description of Apseudes olimpiae n. sp. and of Tanabnormia cornicauda ng, n. sp.(Crustacea, Tanaidacea). Travaux du Muséum National d’Histoire naturelle “Grigore Antipa,” 30, 129–133.

Harrold, C. & Reed, D.C. (1985) Food Availability, Sea Urchin Grazing, and Kelp Forest Community Structure. Ecology, 66, 1160–1169.

Hobson, E.S. & Chess, J.R. (1986) Relationships among fishes and their prey in a nearshore sand community off southern California. Environmental Biology of Fishes, 17(3), 201-226.

Hobson, E.S. & Chess, J.R. (2001) Influence of trophic relations on form and behavior among fishes and benthic invertebrates in some California marine communities. Environmental Biology of Fishes, 60(4), 411-457.

71 Ince, R., Hyndes, G.A., Lavery, P.S. & Vanderklift, M.A. (2007) Marine macrophytes directly enhance abundances of sandy beach fauna through provision of food and habitat. Estuarine, Coastal and Shelf Science, 74, 77–86.

Jaschinski, S., Brepohl, D. & Sommer, U. (2011) Seasonal variation in carbon sources of mesograzers and small predators in an eelgrass community: stable isotope and fatty acid analyses. Marine Ecology Progress Series, 431, 69–82.

Kaehler, S., Pakhomov, E., Kalin, R. & Davis, S. (2006) Trophic importance of kelp- derived suspended particulate matter in a through-flow sub-Antarctic system. Marine Ecology Progress Series, 316, 17–22.

Kamenos, N.A., Moore, P. & Hall-spencer, J.M. (2004) Small-scale distribution of juvenile gadoids in shallow inshore waters; what role does maerl play? ICES Journal du Conseil, 61(3), 422–429.

Kelly, J., Krumhansl, K. & Scheibling, R. (2012) Drift algal subsidies to sea urchins in low-productivity habitats. Marine Ecology Progress Series, 452, 145–157.

Krumhansl, K. & Scheibling, R. (2012) Production and fate of kelp detritus. Marine Ecology Progress Series, 467, 281–302.

Leclerc, J.C., Riera, P., Leroux, C., Lévêque, L., Laurans, M., Schaal, G. & Davoult, D. (2013) Trophic significance of kelps in kelp communities in Brittany (France) inferred from isotopic comparisons. Marine Biology, 160, 3249–3258.

Lowe, A.T., Galloway, A.W.E., Yeung, J.S., Dethier, M.N. & Duggins, D.O. (2014) Broad sampling and diverse biomarkers allow characterization of nearshore particulate organic matter. Oikos, 123(11), 1341-1354.

Mann, K.H. (1988) Production and use of detritus in various freshwater , estuarine , and coastal rnarine ecosystems. Limnology and Oceanography, 33, 910-930.

Martin, A. (1966) Feeding and digestion in two intertidal gammarids: Marinogammarus obtusatus and M. pirloti. Journal of Zoology, 515–525.

Miller, R.J., Page, H.M. & Brzezinski, M. (2013) δ13C and δ15N of particulate organic matter in the Santa Barbara Channel: drivers and implications for trophic inference. Marine Ecology Progress Series, 474, 53–66.

Moncreiff, C. & Sullivan, M. (2001) Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stable isotope analyses. Marine Ecology Progress Series, 215, 93–106.

72 Norderhaug, K.M., Fredriksen, S. & Nygaard, K. (2003) Trophic importnace of Laminaria hyperborea to kelp forest consumers and the importance of bacterial degradation to food quality. Marine Ecology Progress Series, 255, 135–144.

Ouisse, V., Riera, P., Migné, A., Leroux, C. & Davoult, D. (2012) Food web analysis in intertidal Zostera marina and Zostera noltii communities in winter and summer. Marine biology, 159, 165–175.

Page, H.M., Brooks, A. & Kulbicki, M. (2013) Stable isotopes reveal trophic relationships and diet of consumers in temperate kelp forest and coral reef ecosystems. Oceanography, 26(3), 180-189.

Page, H.M., Reed, D., Brzezinski, M., Melack, J. & Dugan, J. (2008) Assessing the importance of land and marine sources of organic matter to kelp forest food webs. Marine Ecology Progress Series, 360, 47–62.

Parnell, A.C., Inger, R., Bearhop, S. & Jackson, A.L. (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE, 5, e9672.

Polis, G., Anderson, W. & Holt, R. (1997) Toward an Integration of Landscape and Food Web Ecology: The Dynamics of Spatially Subsidized Food Webs. Annual review of ecology and systematics, 28, 289–316.

Polis, G. & Holt, R. (1996) Time, space, and life history: influences on food webs. In: G. Polis and K. Winemiller (eds.), Food Webs: Contemporary Perspectives. Chapman and Hall, New York. pp. 435-460.

Raven, J., Johnston, A. & Kübler, J. (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Functional Plant Biology, 29(3), 355-378.

Rodríguez, S.R. (2003) Consumption of drift kelp by intertidal populations of the sea urchin Tetrapygus niger on the central Chilean coast : possible consequences at different ecological levels. Marine Ecology Progress Series, 251, 141–151.

Schaal, G., Riera, P. & Leroux, C. (2009) Trophic significance of the kelp Laminaria digitata (Lamour.) for the associated food web: a between-sites comparison. Estuarine, Coastal and Shelf Science, 85, 565–572.

Schaal, G., Riera, P. & Leroux, C. (2010) Trophic ecology in a Northern Brittany (Batz Island, France) kelp (Laminaria digitata) forest, as investigated through stable isotopes and chemical assays. Journal of Sea Research, 63, 24–35.

Schaal, G., Riera, P. & Leroux, C. (2012) Food web structure within kelp holdfasts (Laminaria): a stable isotope study. Marine Ecology, 33, 370–376.

73 Semmens, B.X., Moore, J.W. & Ward, E.J. (2009) Improving Bayesian isotope mixing models: a response to Jackson et al. (2009). Ecology letters, 12, E6–8.

Steller, D.L., Riosmena-rodríguez, R. & Foster, M.S. (2001) Living Rhodolith Bed Ecosystems in the Gulf of California. Atlas of Coastal Ecosystems in the Western Gulf of California: Tracking Limestone Deposits on the Margin of a Young Sea (2009): 72-82.

Steller, D.L., Riosmena-Rodriguez, R., Foster, M.S.M. & Roberts, C. a. C. (2003) Rhodolith bed diversity in the Gulf of California: the importance of rhodolith structure and consequences of disturbance. Aquatic Conservation: Marine and Freshwater Ecosystems, 13, S5–S20.

Tenore, K. & Hanson, R. (1984) Changes in composition and nutritional value to a benthic deposit feeder of decomposing detritus pools. Bulletin of marine science, 35, 299–311.

Timko, P. (1976) Sand dollars as suspension feeders: a new description of feeding in Dendraster excentricus. The Biological Bulletin, 151, 247-259.

Tompkins, P.A. (2011) Distribution, Growth, and Disturbance of Catalina Island Rhodoliths. Masters Thesis. Moss Landing Marine Laboratories, San Jose State University.

Vafeiadou, A.M., Materatski, P., Adão, H., Troch, M. & Moens, T. (2013) Food sources of macrobenthos in an estuarine seagrass habitat (Zostera noltii) as revealed by dual stable isotope signatures. Marine Biology, 160, 2517–2523.

Vanderklift, M.A. & Ponsard, S. (2003) Sources of variation in consumer-diet delta 15N enrichment: a meta-analysis. Oecologia, 136, 169–82.

Vetter, E.W. (1985) Detritus-based patches of high secondary production in the nearshore benthos. Marine Ecology Progress Series, 120(1), 251-262.

Vetter, E.W. & Dayton, P.K. (1998) Macrofaunal communities within and adjacent to a detritus-rich submarine canyon system. Deep Sea Research Part II: Topical Studies in Oceanography, 45, 25–54.

Vetter, E.W. & Dayton, P. (1999) Organic enrichment by macrophyte detritus, and abundance patterns of megafaunal populations in submarine canyons. Marine Ecology Progress Series, 120, 251-262.

Yingst, J. (1982) Factors influencing rates of sediment ingestion by Parastichopus parvimensis (Clark), an epibenthic deposit-feeding holothurian. Estuarine, Coastal and Shelf Science, 14(2), 119-134.

74 Zanden, M. Vander & Rasmussen, J. (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnology and oceanography, 46, 2061–2066.

75 APPENDICES

Appendix A. Biodiversity of California rhodolith beds. Lowest taxonomic level of individuals observed in rhodolith beds from all surveys.

ALGAE Name Classification Chaetomorpha spp. Chlorophyta Chondracanthus canaliculatus Rhodophyta Lithothrix aspergillum Rhodophyta Plocamium cartilagineum Rhodophyta Polysiphonia spp. Rhodophyta Rhodymenia spp. Rhodophyta Colpomenia spp. Heterokontophyta Dictyopteris undulata Heterokontophyta Dictyota binghamiae Heterokontophyta Hydroclathrus clathratus Heterokontophyta Macrocystis pyrifera Heterokontophyta Sargassum horridum Heterokontophyta Sargassum muticum Heterokontophyta Zonaria farlowii Heterokontophyta Zostera marina Tracheophyta

INVERTEBRATES Name Phylum Class Anthopleura artemisiab Cnidaria Anthozoa Aplysia californicaa,b Mollusca Gastropoda Bulla gouldianab Mollusca Gastropoda Caprellidaea Arthropoda Malacostraca Chitona Mollusca Polyplacophora Chlamys hastataa Mollusca Bivalvia Conus californicusa,b Mollusca Gastropoda Cumaceaa Arthropoda Malacostraca Decapodaa Arthropoda Malacostraca Dendraster excentricusb Echinodermata Echinoidea Gammaridaea Arthropoda Malacostraca Hemisquilla ensigera californiensisb Arthropoda Malacostraca Hermissenda crassicornisb Mollusca Gastropoda Isopodab Arthropoda Malacostraca Kelletia kelletiib Mollusca Gastropoda Leptostracaa Arthropoda Malacostraca Lima hemphillia Mollusca Bivalvia

76 Lirularia spp.a,b Mollusca Gastropoda a,b Lytechinus pictus Echinodermata Echinoidea Marine mite (Halacaridae) a Arthropoda Arachnida Maxwellia gemmab Mollusca Gastropoda Megastraea undosaa,b Mollusca Gastropoda Navanax inermisb Mollusca Gastropoda Ophiopteris papillosaa Echinodermata Ophiuroidea Ophiothrix spiculataa Echinodermata Ophiuroidea Ostracodaa Arthropoda Ostracoda Pachycerianthus fimbriatusb Cnidaria Anthozoa Parastichopus parvimensusb Echinodermata Holothuroideaia Phoronopsis californicab Phoronida Platyhelminthesa Platyhelminthes

Podochela hemphillib Arthropoda Malacostraca Phyllactis spp. Cnidaria Anthozoa a Polychaeta Annelida Polychaeta Spiochaetopterus costarumb Annelida Polychaeta Strongylocentrotus purpuratusa,b Echinodermata Echinoidea Tanaidaceaa Arthropoda Malacostraca Thelepus crispusb Annelida Polychaeta a Denotes infauna b Denotes epifauna

FISHES Name Caulolatilus princeps Chromis punctipinnis Citharichthys sordidus Girella nigricans Halichoeres semicinctus Heterostichus rostratus Hypsypops rubicundus Myliobatis californica Oxyjulis californica Paralabrax clathratus Paralabrax nebulifer Pleuronichthys coenosus Rhinogobiops nicholsii Sardinops sagax Scorpaena guttata Semicossyphus pulcher Syngnathus spp.

77 Suspended Particulate Organic Matter Sediment Organic Matter (SOM) Taxonomic group or species Macrocystis pyrifera (fresh) Parastichopus parvimensus Macrocystis pyrifera (drift) Americardia biangulata Dendraster excentricusDendraster ECHINODERMATA Lirularia acuticostata Lytechinus anamesus Podochela hemphilli Megastraea undosa Rhodolith (3 & 7m) Conus californicusConus MACROALGAE Offshore (3 & 7m) Limaria hemphilliLimaria ARTHROPODA Polysiphonia MOLLUSCA ANNELIDA Polychaetes Gammarid Tanaid

spp.

Aug-12 (n) 6 6 6 6 2 6 6 4 6 6 -18.22 -14.41 -15.73 -17.62 -27.60 -16.57 -15.50 -19.54 -21.92 -23.27 δ 13 C 1.02 0.49 0.47 0.33 0.47 1.28 1.97 1.16 0.40 0.32 SD base food webdepiction. Coveby Isthmusoverall were Samplesfrom an season. to rhodolith pooled produce Stable B. Appendixratios, isotope 12.02 14.15 13.41 10.17 10.45 11.79 9.78 9.69 8.59 6.83 δ 15 N 0.30 0.32 0.16 0.13 0.08 0.09 0.70 1.23 0.77 0.34 SD Apr-13 (n) 4 2 3 5 4 2 8 3 7 7 4 6 6 -17.54 -13.53 -21.29 -20.47 -17.54 -16.99 -15.71 -17.05 -16.58 -15.85 -17.93 -22.37 -22.77 δ

13 C 1.17 0.63 0.33 0.32 0.60 0.77 0.86 0.71 2.14 1.98 0.21 0.37 0.51 SD 10.34 10.21 10.77 9.80 8.51 8.91 9.13 13.3 9.55 9.64 9.53 7.88 7.94 δ 15 N δ 13 0.80 0.12 0.27 0.29 0.54 0.58 0.59 0.54 0.57 0.54 0.81 1.07 0.8 SD δ andC 15 N, for primary producers and producers primary N, consumers for and Dec-13 (n) 8 8 6 5 6 3 3 8 8 4 3 -14.98 -14.93 -15.84 -16.65 -14.41 -28.97 -16.36 -14.77 -16.18 -23.87 -16.6 δ 13 C 0.89 0.58 0.66 0.62 0.57 0.83 1.55 1.96 1.00 0.66 0.9 SD 11.25 11.12 13.71 11.69 10.36 10.91 11.62 10.84 10.62 9.41 7.88 δ 15 N 0.36 0.37 0.41 0.69 0.16 0.38 0.42 0.34 0.58 0.44 1.11 SD Pooled Food Web (n) 18 16 12 13 21 21 12 15 12 3 5 4 2 6 3 3 6 5 bed -16.68 -14.37 -21.29 -15.57 -20.47 -17.54 -16.99 -15.98 -14.41 -17.05 -17.62 -28.42 -16.49 -15.33 -17.88 -22.49 -23.02 -16.6 δ 13 C 0.82 0.33 0.61 0.32 0.60 0.77 0.91 0.57 0.71 0.33 0.98 1.62 1.93 1.65 0.85 0.48 1.8 0.9 SD 11.24 11.49 14.02 10.21 10.77 11.69 10.36 13.41 10.46 10.38 10.25 8.51 8.91 9.39 13.3 10.2 8.16 7.39 δ 15 N 0.63 0.84 0.27 0.46 0.29 0.54 0.58 0.82 0.16 0.38 0.13 0.69 1.06 0.96 0.91 0.78 0.96 0.8 SD Herbivore/Micrograzer Detritivore/Herbivore Feeding strategy Planktivore Planktivore Detritivore Detritivore Detritivore Herbivore Herbivore Predator Predator Predator

78