CALIFORNIA STATE UNIVERSITY, NORTHRIDGE

DIRECT AND INDIRECT IMPACTS OF FISHING ON THE TROPHIC STRUCTURE

OF FOREST OFF SOUTHERN

A thesis submitted in partial fulfillment of the requirements

for the degree of Masters of Science in Biology

By

Parker Henry House

May 2015

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The thesis of Parker H. House is approved by:

______Maria S. Adreani, Ph.D. Date

______Peter J. Edmunds, Ph.D. Date

______Mark A. Steele, Ph.D. Date

______Larry G. Allen, Ph.D., Chair Date

California State University, Northridge

! ii ACKNOWLEDGEMENTS

I would like to express my gratitude to the following people for making this research possible. First and foremost, I would like to thank my advisor and mentor Dr.

Larry “Gandalf” Allen for accepting a guy who was pulling seine nets in the Louisiana bayou and teaching me all things related to the fishes of the northeastern Pacific. I could not have done this project without your enthusiasm for research, continual support, friendship, and knowledge. Thank you to Dr. Mark Steele and Dr. Mia Adreani for their invaluable input, insight, and reviewing of this thesis. I would also like to thank Dr. Peter

Edmunds for his valued discussions, support, edits to this thesis, and always asking “so where’s the Ecology manuscript?”

My upmost gratitude goes to those who helped me in the field. Thank you to

Jennifer “JSmo” Smolenski for selflessly, continuously, and saintly helping me throughout my first field season, even after hour long surface swims off La Jolla, long cold days at Anacapa Island, and throughout the summer putting up with consistently eating peanut butter and pop-tarts for lunch. Thank you to Michael “Abalone” Abernathy for guidance and help at Anacapa Island and for teaching me the skills necessary to operate a boat. I would especially like to thank J.R. Clark for his immeasurable help researching , being an exceptional field assistant and lab mate, but even more so a great friend.

I am very grateful to Juan Aguilar and the staff at the USC Wrigley Institute for

Environmental Studies for field assistance and allowing me to do research from out of the one and only Big Fisherman Cove. Upmost thanks to Dr. Jack Engle and Dr. Ed Parnell for their proficient advice and input to this study, and to Dr. Steve Dudgeon for being a

iii! ! fellow night owl and letting me stalk and ask questions on statistical analyses late at night in Magnolia Hall. I would also like to thank Myron Hawthorne and the highly skilled

CSUN Science Shop team for constructing the laser outfitted DPVs for giant sea bass, as well as the “zombie killer.”

Many thanks to the Allen Lab, fellow friends/graduate students at

CSUN, and particularly Nick Evensen, Edwin “Yoda” Leung, and Barbara “Babs”

Sanchez for all their help. I would like to give a very special thank you to Kelcie

“Chiquita” Chiquillo for countless discussions about this project, unwavering and continual encouragement and support, and for hundreds of opaleye grandbabies.

This research was funded by the CSUN Graduate Thesis Support Program,

Nearshore Marine Research Program, Sigma Xi Grants in Aid of Research, Southern

California Academy of Sciences, and the USC Wrigley Summer Fellowship Program.

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DEDICATION

This work is dedicated to my loving mother and father, Debbie and Randy House, who have always supported my brothers and myself to pursue our passions in life as long as we work hard doing it.

! v TABLE OF CONTENTS

Signature Page ii

Acknowledgements iii

Dedication v

Abstract vii

Chapter 1 Differences in trophic and community structure of fishes inside and outside of three long-standing MPAs in the Southern California Bight

Introduction 1 Materials and Methods 15 Results 24 Discussion 29 Table 39 Figures 48

Chapter 2 Stock biomass, numerical densities, population characteristics, and community presence of giant sea bass ( gigas) off Santa Catalina Island, California

Introduction 60 Materials and Methods 65 Results 67 Discussion 69 Table 75 Figures 76

References 85

vi

Abstract

Direct and Indirect Impacts of Fishing on the Trophic Structure of Kelp Forest Fishes off

Southern California

By

Parker H. House

Masters of Science in Biology

In many marine ecosystems worldwide, overfishing is a prominent cause in removing large predatory fishes from ecological communities. Fluctuation in the abundance of higher trophic level can transform an ecosystem’s structure and function by altering trophic interactions through density-mediated top-down control.

Accordingly, understanding the extent to which humans indirectly influence a community through altering predator abundance is of critical importance. Thus, during the summer of

2013 and 2014 the impacts of fishing on the trophic structure and community assemblage of kelp forest fishes were examined within the Southern California Bight.

In 2013, I tested whether decreased abundance through fishing for higher trophic level predators relieves predation pressure on lower trophic level prey. Using a combination of underwater survey techniques, density (no. fish/100 m2) and biomass

(g/100 m2) of conspicuous fish species were sampled inside and outside of three long- standing Marine Protected Areas (MPAs) off La Jolla, Santa Catalina Island, and

Anacapa Island, California. I found that secondary and herbivore/omnivore trophic levels significantly decreased outside of MPAs. Inversely, the primary carnivore trophic level biomass increased outside of MPAs. Species-level results revealed a lower

! vii abundance outside MPAs of large kelp bass (> 25 cm) and higher densities of its prey, kelp perch. My results show overall fish trophic level changes due to fishing pressure, and provide support for a weakening of top-down control on the kelp perch population through the removal of predatory fishes outside MPAs.

To investigate the possible return of the historically overfished apex predator of the kelp forest fish community, I censused the giant sea bass (Stereolepis gigas) population at eight sites off Santa Catalina Island from mid-June through mid-August,

2014. Three possible spawning aggregations were identified at the sites Twin/Goat, The

V’s, and Little Harbor. The giant sea bass population at these sites primarily consisted of individuals 1.2 - 1.3 m long (total length, TL) with small and probably newly mature fish

(estimated to be 10 - 11 years old) observed in aggregations. However, larger individuals

1.8 - 1.9 m TL accounted for the majority of the population biomass. Overall, mean spawning stock biomass of giant sea bass was 36.3 kg/1000 m2. Providing a general comparison of mean biomass among the trophic levels of kelp forest fishes off Santa

Catalina Island revealed a nearly top-heavy biomass pyramid. The relatively high abundance of giant sea bass provides evidence that this species is recovering at kelp forests off Santa Catalina Island, and possibly throughout the Southern California Bight.

The removal or recovery of predators can greatly influence an ecosystem. As more recent studies suggest that indirect community effects of fishing and protection can take up to decades to detect, it is necessary to document the continued changes on the structure, function, and dynamics of the kelp forests and rocky reefs off southern

California.

! viii Chapter 1

Differences in trophic and community structure of kelp forest fishes inside and

outside of three long-standing MPAs in the Southern California Bight

Introduction

The partitioning of food resources among different species in a community determines the trophic structure of an ecosystem. Fluctuations in species abundance within various trophic levels can alter the composition and function of a community by means of bottom-up and top-down influences. Bottom-up processes are fundamental to the foundation of an ecosystem by altering community composition through variation in abiotic influences and primary production. On the other hand, top-down control regulates how fixed carbon resources are distributed throughout a community (Estes et al. 2001).

Neither bottom-up nor top-down processes are mutually exclusive, functioning together to influence the abundance and diversity of organisms within an ecosystem. Due to recent declines in abundance of large globally (Estes et al. 2011), there have been a growing number of studies focused on understanding the effects of top-down pressures on ecological interactions within communities. However, measuring the effects of declines in predator abundance on a community can be problematic, as there are small amounts of historical baseline data for comparing current community structure (Dayton et al. 1998). Although impacts of top-down control can be difficult to detect, there has been a considerable number of studies documenting predator effects on communities. From the regulation of zebras by lions in the Serengeti (Grange and Duncan 2006), recovery of aspen trees after wolf reestablishment in Yellowstone National Park (Ripple and Beschta

1! !

2007b), fluctuations of plankton abundance due to experimental manipulations of lake fishes in Wisconsin (Carpenter and Kitchell 1988), to the decimation of Alaskan kelp forests after decreases in sea otter populations (Estes and Palmisano 1974), many ecosystems are subject to a release in prey abundance, and in some cases, cascading effects through multiple trophic levels when predatory species either recover or decline.

Regarding marine ecosystems, fishing is the most exploitative anthropogenic influence on the abundance and diversity of organisms within these communities

(Jackson et al. 2001). Intense fishing pressure has directly affected the abundance, size structure, and genetic diversity of targeted fished populations (Pauly et al. 1998, Bianchi et al. 2000, Hauser et al. 2002, Dayton et al. 2003). Many of these target species are large-bodied, higher trophic level fishes (Myers and Worm 2003). Direct removals of these large predators can indirectly increase prey abundance and shift the consumer dominance to lower trophic levels (Baum and Worm 2009). An example of higher trophic level species releasing predation pressure on prey abundance was documented after the collapse of the cod fishery off Newfoundland in 1992, which led to the outbreak in the population abundance of dogfish, skates, shrimp, sea urchins, and (Worm and

Myers 2003, Steneck et al. 2004, Frank et al. 2005). Similarly, the overharvest of great sharks off the U.S. Atlantic coast released skate, ray, and small shark mesopredator populations from predatory control, and further suppressed the abundance of prey scallops (Myers et al. 2007). However, indirect effects of fishing on an ecosystem are not exclusive to large commercial fisheries or more depauperate temperate regions. On the coral reefs of Jamaica, Hughes (1994), hypothesized that increases in macroalgae on the

! ! ! 2 ! reefs were primarily an indirect result of removing sharks, snappers, jacks, triggerfish, and groupers within the region. !

An increasingly common way to combat the effects of overfishing has been the implementation of ‘no-take’ marine protected areas (MPAs), and due to the protracted influence by humans on nearshore marine communities, MPAs may serve as the best available means to test the ecosystem effects of fishing (Tegner and Dayton 2000). MPAs have greatly increased the biomass and numerical densities of targeted fish populations

(Halpern 2003, Barrett et al. 2007, Froeschke et al. 2006, Tetreault and Ambrose 2007,

Hamilton et al. 2009, Lester et al. 2009). In temperate systems, mean biomass for these species inside reserves can increase as much as 554% (Lester et al. 2009) compared to nearby fished locations.

Of the kelp forest fishes off southern California, the two most abundant predators targeted by fishing are the ( pulcher) and kelp bass

(). Both species have been shown to respond well to protection by increasing in densities, size structure, and biomass inside MPAs throughout the Southern

California Bight (Froeschke et al. 2006, Tetreault and Ambrose 2007, Hamilton et al.

2009). Differences in sheephead abundance can regulate the size of red populations (Cowen 1983) and black sea urchin behavior (Nelson and Vance 1979).

Furthermore, the decrease of sheephead biomass due to fishing outside MPAs has indirectly alleviated predation pressure on strongylocentrotid urchins, and through cascading effects, suppress kelp abundance (Babcock et al. 2010). Unlike the specialist invertivore, sheephead, kelp bass is the predominant generalist piscivore on rocky reef kelp forests off southern California, and are the most important predator of reef fishes off

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Santa Catalina Island (Carr 1991, Steele 1997a, 1997b, and Steele et al. 1998) and likely throughout the Southern California Bight. Therefore, kelp bass have the potential to regulate lower trophic level fishes.

Kelp bass are one of the most important species in southern California recreational marine fisheries (Allen and Hovey 2001b, Jarvis et al. 2004), and their overall biomass has decreased by 90% since the 1980’s (Erisman et al. 2011). However, protection via MPAs appears to be beneficial, as orders of magnitude higher biomass of kelp bass have been reported inside compared to outside protected areas (Froeschke et al.

2006, Tetreault and Ambrose 2007, Hamilton et al. 2009). Kelp bass are known to decrease population sizes of conspicuous (Schmitt and Holbrook 1985, Anderson 2001) and cryptic prey reef fishes (Steele 1997a, 1997b, Steele et al. 1998, and Steele 1999).

However, changes in prey fish population sizes have not been observed due to decreases in kelp bass abundance via fishing off southern California.

Two studies have investigated differences in abundance of target and non-target kelp forest fish species off southern California. Hamilton et al. (2009) researched the changes in species and functional trophic groups in relation to protection and biogeographic differences throughout the northern Channel Islands marine reserve network five years after its inception. The most recent study analyzing target and non- target species of the kelp forest fish community inside and outside of long-standing

MPAs encompassing the entire Southern California Bight was from underwater benthic surveys conducted 15 years ago (1997-1998) by Tetreault and Ambrose (2007). Both studies found decreases in target secondary carnivores (kelp bass and sheephead), but no indirect effects on non-target lower trophic level fishes.

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Although indirect effects of fishing on the kelp forest fish community have not been observed off southern California, this community may be changing. After the

Proposition 132 gill net ban in 1994, the endangered apex tertiary carnivore, giant sea bass (Stereolepis gigas), has shown signs of a return and gradual increase to the southern

California kelp forest ecosystem since the population collapse due to overfishing

(Pondella and Allen 2008). Giant sea bass feed on a wide variety of larger fish species, including the heavily fished kelp bass (Domeier 2001, Love 2011). The growing emergence of this top predator can further influence ecosystem dynamics off southern

California with the potential to exacerbate the effects of fishing and trophic relationships within the kelp forest community. The possible return of giant sea bass, coupled with growing evidence that indirect effects of fishing on marine communities can take decades to detect (Daan et al. 2005, Babcock 2010, Estes et al. 2011), warrants investigation into fish community dynamics off southern California. I evaluated how fishing pressure may directly and indirectly influence the trophic structure of kelp forest fishes off southern

California.

To address this question, I used a combination of survey methods to assess biomass and numerical densities of fish trophic levels and community assemblage at the species level. I surveyed three sites containing over 25-year-old MPAs as a control for nearby locations subject to fishing pressure throughout a wide geographic range (235 km) within the Southern California Bight. The objective of this study was to determine whether a direct decrease through fishing of higher trophic level predators indirectly releases predation pressure on lower trophic level prey species within the fish community. With fish numerical and biomass densities as my response variables, I tested

! ! ! 5 ! the hypotheses that 1) the secondary carnivore trophic level will have a lower abundance outside of MPAs; 2) the primary carnivore level will have a higher abundance, while the herbivore/omnivore level will not significantly change outside of MPAs; and 3) lower abundance of large > 25 cm piscivorous kelp bass will alternatively show a higher abundance in prey species outside MPAs.

Natural History

Kelp Forest and Rocky Reef Habitat of Southern California

The kelp forests of the eastern Pacific are submarine forests dominated by giant kelp (Macrocystis pyrifera) and other large brown algae of the class Phaeophyceae.

These underwater algal forests are distributed along the California coast, they have a high annual biomass production of ~1000-2000 g/m2/yr (Mann 1973), and develop best where there is some protection from heavy surge. In southern California, the gently sloping continental shelves, protective offshore islands, and upwelling provide optimal conditions to support giant kelp forests (North and Hubbs 1968). Kelp forests occur where their holdfasts can fix on to solid objects such as rocky reefs. The rocky reefs south of Point

Conception are 90% sedimentary rock formations (sandstone, mudstone, and shale), as well as metamorphic formations, igneous formations, and boulders (Emery 1960). primarily grow at nearshore shallow depths from the intertidal zone to ~30 m (Feder et al.

1974). Within this depth range, giant kelps have a towering distribution in the water column, and similar to terrestrial forests, the vertical structure provided by the kelp stipes allows for different space/habitat niches for several fishes. These different vertical habitats within the water column can be divided into three distinct regions: 1) the canopy

! ! ! 6 ! region, consisting of dense stipe patches near the surface to about 3 m deep; 2) the mid- water kelp region, located in the middle of the water column between the and the canopy where kelp structure is more scarce and the abundance and diversity of fishes are lower; 3) The holdfast region, consisting of the substratum and kelp holdfasts and extends to a few meters above. Fish diversity and abundance is the greatest within the holdfast region. However, though these vertical regions do provide specialized habitat niches to some kelp-associated fish species, many species will use several vertical regions (Ebeling et al. 1980a).

Along with different vertical regions in kelp forests, variations in bottom depths, benthic characteristics, and kelp abundance can also influence fish assemblages. A number of fish species have distinct depth-dependent distributions. These distributions appear to be associated with algal diversity and density (Ebeling et al. 1980a, DeMartini

1981), as well as by thermocline gradients (Terry and Stephens, 1976). Various components and characteristics of the reef itself also provide important functions to the kelp forest fish assemblage such as shelter, food availability, and nesting sites. The diversity and abundance of many benthic-associated kelp forest fishes is directly dependent on the degree of relief and rugosity of the rocky substratum, and not as much on the abundance of kelp (Limbaugh 1955, Quast 1968b, Ebeling et al. 1980a). However, the presence of kelp can greatly influence several canopy and water column-associated fishes, including kelp perch ( frenatus), (Medialuna californiensis), giant kelpfish (Heterostichus rostratus), kelp bass (Paralabrax clathratus), and señorita ( californica) (Larson and DeMartini 1984), and may have a strong effect on these fish populations over a low relief bottom (DeMartini and

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Roberts 1990). With these kelp forest and rocky reef habitat characteristics in mind, fish surveys in this study were conducted in areas with similar topographical complexity, substratum composition, depth, and kelp abundance inside and outside of MPAs at each site.

Fish Community

The merging of the cold California Current and the warmer Southern California

Counter Current creates a transitional biogeographic zone as well as a unique and diverse fish assemblage within the Southern California Bight. In the kelp forests off southern

California, there are >150 fish species associated with kelp forests (Stephens et al. 2006).

These species can be grouped into three categories as defined by Quast (1968b) and

Stephens et al. (2006): cryptic, transient, and conspicuous species.

Cryptic species of kelp forests can be found primarily within rock crevices on the reef as well as in the water column among Macrocystis stipes and blades. They are usually small-bodied fishes from the families Hexagrammidae, Cottidae, Labrisomidae,

Clinidae, Stichaeidae, Gobiesocidae, Syngnathidae, and Gobiidae (Stephens et al. 2006).

However, some larger species are also a part of this category including giant kelpfish

(Heterostichus rostratus), California scorpionfish (Scorpaena guttata), treefish (Sebastes serriceps), and the California moray eel (Gymnothorax mordax). These species contribute greatly to the fish diversity within kelp forests, although, their contribution to the overall fish biomass in this ecosystem is only ~10% (Allen et al. 1992).

Transient pelagic species are associated with, but not dependent, on kelp forests.

They use the habitat as a nursery and/or feeding ground and include fishes from the

! ! ! 8 ! families Atherinopsidae, Clupeidae, Engraulidae, Haemulidae, Malacanthidae

Scombridae, Carangidae, Sphyraenidae, Pleuronectidae, Paralichthyidae, and several species of elasmobranchs (Stephens et al. 2006). Though not considered residents of kelp forests, transient species are likely to contribute to the energetics of this system.

Conspicuous species are typically larger-bodied and spend majority of their post- settlement life history within rock reefs and kelp forests. This group encompasses fishes from the families Embiotocidae, Sebastidae, Scorpaenidae, Pomacentridae, Labridae,

Kyphosidae, , and Polyprionidae (Stephens et al. 2006). The majority of fish biomass within kelp forests is contributed by these species, and it is the focal assemblage in the present study.

Trophic Structure of the Conspicuous Fish Assemblage

Phytoplankton, smaller macroalgae, and kelps provide the carbon available for transfer to higher trophic levels in the kelp forests off southern California (Horn and

Ferry-Graham 2006). The feeding interactions among conspicuous fishes are complex, and many species are trophic generalists. After extensive gut content analysis of kelp forest fishes off southern California, Quast (1968e) determined 46% are carnivores, 46% are omnivores, and 8% are herbivores. Though many species are opportunists, the functional food web of the kelp forest fish community can be categorized into four trophic levels above primary producers; herbivore/omnivore, primary carnivore, secondary carnivore, and tertiary carnivore (Cross and Allen 1993).

The fishes that make up the herbivore/omnivore trophic level include species that consume macroalgae for almost their entire diet after settlement (Horn 1989). The three

! ! ! 9 ! species within this trophic level are the sea chubs (Kyphosidae) opaleye ( nigricans), halfmoon (Medialuna californica), and zebraperch (Hermosilla azurea). The zebraperch feeds primarily on red, but also green and brown algae (Sturm and Horn

1998). Halfmoon are found most frequently in the water column and feed on ~80% algae, and ~20% of gut content is generally comprised of polychaetes, , and bryozoans

(Quast 1968b). A highly abundant and common inhabitant of the kelp forest reefs off southern California is the opaleye. Opaleye inhabit all vertical regions of the water column and often schools with the halfmoon. They are voracious grazers feeding on green (Leighton 1971), red (Foster et al. 1984), and brown algae (Harris et al. 1984,

Hobson and Chess 2001). Like many fishes, the opaleye undergoes an ontogenetic shift in diet. In its early life, opaleye are omnivorous plankton feeders and become predominantly algal grazers shortly after settlement to shallow tidepools and understory beds (Mitchell 1953, Williams and Williams 1955, Barry and Ehret 1992, Bredvik et al

2011). Roughly 90% of the opaleye diet consists of macroalgae, with the remaining

~10% of the diet consisting of gammarid amphipods, polychaetes, mysids, caprillids, and other small (Quast 1968b). No digestive enzymes for algae (alginase) have been found for Californian Kyphosids (Sturm and Horn 1998), however, it is likely they digest algae through acid lysis in the stomach and microbial gut fermentation in the hindgut, similar to other closely related Australian Kyphosids (Rimmer 1986, Sturm and

Horn 1998, Zemke-White et al. 1999). In temperate waters, herbivorous fishes are considerably less speciose than those of the tropics. This is likely due to lower food processing rates in colder temperatures (Harmelin-Vivien, 2002). However, these three herbivorous fishes, in particular opaleye and halfmoon, are abundant in southern

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California kelp forests, and are likely to play a key role in reef structure, function, and trophic energetics.

The majority of fishes in California kelp forests are carnivores (Quast 1968b).

Fishes that can be categorized as primary carnivores feed either in the water column on zooplankton, on the benthos and other surfaces for small invertebrates, or a combination of both (Horn and Ferry-Graham 2006). A trend found in many marine systems (Horn

1989), and likewise found in southern California, is the dominance of as food resources for fishes in both benthic and open water habitats (Horn and Ferry-Graham

2006).

The blacksmith () is likely the most abundant of all rock reef and kelp forest fishes and is the obligate planktivore of this community, feeding on larvaceans, calanoid and cyclopoid copepods, and fish larvae throughout the water column (Hobson and Chess 1976). Other transient planktivores include Pacific sardine

(Sardinops sagax), northern anchovy (Engraulis mordax), and topsmelt (Atherinops affinis).

The majority of primary carnivore fishes are benthic feeders. Several relatively large (Embiotocidae) feed on the small invertebrates within the rocky substrate algal “turf” on kelp forest reefs (Laur and Ebeling 1983). The black perch

(Embiotoca jacksoni) winnows for amphipods, caprellids, and worms along the benthos of rocky reefs. The closely related striped seaperch is not a winnowing species, but has a similar diet to the black perch feeding on amphipods, caprillids, worms, and shrimps

(Laur and Ebeling 1983). The medium sized Labrid, the rock (Halichoeres semicinctus), feeds on a wide variety of benthic invertebrates including crustaceans,

! ! ! 11 ! polychaetes, gastropods, and bryozoans (Love 2011). The larger member of the kelp forest Pomacentrids, the (Hypsypops rubicundus), feeds on bryozoans, hydrozoans, ascideans, polychaetes, and gammarid amphipods, but also on large amounts of algae (Hobson and Chess 2001). Quast (1968b) found that algae was the third most frequent food resource consumed for all species, although, only three species were considered herbivores. Many primary carnivores ingest algae. It is presumed that algae are secondarily ingested by fishes in the pursuit of small invertebrates living on blades and stipes, or embedded in algal turf (Horn and Ferry-Graham 2006). This is thought to be the case for the garibaldi, where ~70% of gut content can contain (Quast

1968b). However, the digestive utilization of algae for many species is not well understood (Horn and Ojeda 1999)

The fishes from kelp forests off southern California that incorporate both planktivorous and substrate picking methods in feeding are the embiotocid kelp perch

(Brachyistius frenatus) and the labrid señorita (Oxyjulis californicus). Young-of-the-year and smaller sized señorita < 100 mm SL pluck zooplankton from out of the water column

(Hobson and Chess 2001). Along with feeding on zooplankton, larger individuals are facultative cleaners by picking external parasites off many fish species, and also feed on kelp and rock substrates for gammarideans, bryozoans, caprillids, polycheates, and isopods (Hobson and Chess 2001). Juvenile kelp perch < 100 mm SL tend to feed on zooplankton (Bray and Ebeling 1975) in the canopies and midwater of the kelp forest.

Adults feed by taking small crustaceans (gammaridean, caprillid, calanoids, and isopods) and bryozoans off Macrocystis (Limbaugh 1955, Quast 1968b, Hobson and Chess 2001).

Other primary carnivores categorized in the present study are young-of-the-year and

! ! ! 12 ! juvenile fishes that have secondary carnivore feeding habits as adults. These fishes include small pile perch (Rhacochilus vacca), rubberlip seaperch (Rhacochilus toxotes), kelp bass, sheephead, and several species of rockfish (Sebastes). My study recognizes ontogenetic dietary shifts and categorized fishes in trophic level based on size/age of each individual recorded during surveys.

The secondary carnivore trophic level is made up of species that as adults feed on larger macro-invertebrates and/or smaller lower trophic level fishes. Several members of this trophic level are important in the southern California recreational fishery. The two

Embiotocids categorized as secondary carnivores are the pile perch, and the rubberlip seaperch. Both species feed on benthic invertebrates (Quast 1968b). Pile perch select relatively large, hard-shelled invertebrates, such as bivalves, shelled gastropods, and brittle stars (Laur and Ebeling 1983). The rubberlip seaperch is a winnowing species that will feed on small invertebrates (amphipods), as well as and larger invertebrates

(Hobson and Chess 2001). The sheephead (Semicossyphus pulcher) is a highly sought after species in commercial and recreational fisheries off southern California and Mexico

(Alonzo et al. 2004). Sheephead feed on a variety of macroinvertebrates including mollusks, echinoids, brachyurans, polychaetes, and bryozoans (Cowen 1986, Hobson and

Chess 1986, 2001, Johnson et al. 1994). Larger individuals specialize on sea urchins and indirectly affect kelps within their relatively small home ranges (Cowen 1983, 1986,

Dayton et al. 1998, Topping et al. 2005).

There are several fishes within the secondary carnivore level that can be classified as piscivores depending on the size of the individual. However, many of these species also feed on macroinvertebrates. The olive rockfish (Sebastes serranoides) is more

! ! ! 13 ! common north of Point Conception, but can also occur in southern California. They eat small rockfish, shiner perch, northern anchovies, topsmelt, and cottids, as well as many nektonic invertebrates and octopuses (Love and Westphal 1981). The treefish (Sebastes serriceps) is a nocturnal species that lives cryptically within caves and crevices on the reef and feeds on benthic invertebrates and fishes (Hobson et al. 1981, Kosman et al.

2007). One of the more abundant shallow-living rockfishes within southern California kelp forests is the kelp rockfish (Sebastes atrovirens). Unlike many demersal rockfish, kelp rockfish inhabit all areas of the water column and are crepuscular feeders (Van

Dykhuizen 1983). Adult kelp rockfish eat zooplankton, shrimps, isopods, crabs, and small fishes (Love 2011). The most abundant and common piscivorous kelp forest fish is the kelp bass of the family Serranidae. On rocky reefs off Santa Catalina Island, kelp bass make up about 90% of piscivorous predators (Steele 1997a, 1997b, and Steele et al.

1998), and is likely the case on other reefs off southern California. In addition, kelp bass are also highly important in the southern California recreational fishery (Allen and Hovey

2001b, Jarvis et al. 2004). They are crepuscular ambush feeders of a wide variety of both benthic and water column prey (Hobson and Chess 2001). Smaller fish feed on zooplankton and macroinvertebrates. However, large individuals > 400 mm SL feed nearly exclusively on fishes, many of which are reef-associated (Quast

1968d). Prey fishes include giant kelpfish, señorita, blacksmith, kelp perch, shiner perch, young rockfish, cryptic species such as cottids and gobiids, and transient pelagic fishes including clupeiforms and topsmelt (Quast 1968d, Steele 1997a, 1997b, and Steele et al.

1998, Anderson 2001, Hobson and Chess 2001).

! ! ! 14 !

The only fish residing at the tertiary carnivore level in the kelp forest is the critically endangered giant sea bass Stereolepis gigas (Polyprionidae). This massive

(>250 kg) apex predator consumes spiny , octopus, and as well as many demersal and conspicuous fishes associated with kelp forests, such as sting rays, skates, small sharks, flatfishes, barred sand bass, blacksmith, , , sheephead, and kelp bass (Domeier 2001, Love 2011). However, much is still unknown about the feeding habits of giant sea bass because of their population collapse due to overfishing in

1935 and protected status in 1982. They are likely to prey on many larger kelp forest fishes from May-October when they frequent kelp forests and rocky reefs.

Conspicuous kelp forest fishes that were observed during the present study have a variety of feeding habits that allow them to be grouped into specific functional trophic levels and occur in different vertical regions of the kelp forest (Table 1.1).

Materials and Methods

Study Sites

I surveyed kelp forest fishes at three sites off southern California containing the oldest MPAs within the Southern California Bight and nearby unprotected areas of comparable habitat where fishing was permitted (non-MPAs). This design was implemented to investigate the effects of fishing on the kelp forest fish community. Sites were located off La Jolla, Santa Catalina Island, and Anacapa Island, CA (Figure 1.1).

Sampling was conducted from June 6 to August 9, 2013.

The MPA located off Point La Jolla is the Matlahuayl State Marine Reserve

(SMR). Boundaries of the Matlahuayl SMR to the coastline are located at 32° 51.964' N.

! ! ! 15 ! lat. 117° 15.233' W. long.; 32° 51.964' N. lat. 117° 16.400' W. long.; and 32° 51.067' N. lat. 117° 16.400' W. long. The Matlahuayl SMR (Figure 1.1) was originally established as the San Diego-La Jolla Ecological Reserve in 1971, and prohibits take of all living resources. Transects in non-MPA locations (32° 51' 10.40” N. lat. 117° 16' 45.57” W. long.) were conducted off Boomer Beach in areas containing similar substrate composition of red algal turf reefs, relief 1-3 m high, and comparable Macrocystis density to the Matlahuayl SMR (Parnell et al. 2006). Fishing effort at Point La Jolla is likely focused on the line of the MPA, as is shown in California Department of Fish and

Wildlife commercial passenger fishing vessel (CPFV) catch per unit effort (CPUE) maps, and was observed (including and private fishing boats) during this study.

Transects in the non-MPA were at least 0.5 km west from the Matlahuayl SMR boundary.

Santa Catalina Island is located 35 km southwest of Los Angeles. The MPA off the southeastern side of the isthmus (Figure 1.1) is the no-take Blue Cavern Onshore

State Marine Conservation Area (SMCA). This MPA has expanded from the original boundary at Chalk Cliffs (33° 26.64' N. lat. 118° 29.30' W. long.) to Yellowtail Point

(33° 25.96' N. lat. 118° 27.00' W. long.) as a part of the Marine Life Protection Act

(MLPA). The MLPA was implemented in southern California in January 2012 to reevaluate existing and design new MPAs. Surveys for this study were only done in the original Catalina Marine Science Center State Marine Reserve established in 1988, encompassing an area of ~0.21 km2. Surveys within this MPA were located from the

USC Wrigley Institute’s intake pipes (33° 26' 47.50” N. lat. 118° 29' 09.89” W. long.) to the Pumpernickle Cove mooring (33° 26' 53.79” N. lat. 118° 28' 45.64” W. long.) and

! ! ! 16 ! east of Pumpernickle (33° 26' 56.70” N. lat. 118° 28' 33.63” W. long.). No surveys were located in Big Fisherman Cove as habitat was not comparable to available non-MPA areas. Non-MPA surveys were conducted off Lion Head (33° 27' 12.08” N. lat. 118° 30'

04.62” W. long.), Sphinx Rock (33° 27' 20.08” N. lat. 118° 30' 29.48” W. long.), Eel

Cove (33° 27' 21.34” N. long. 118° 30' 38.33” W. long.), Little Geiger (33° 27' 27.07” N. lat. 118° 30' 51.39” W. long.), and Howland’s Landing (33° 27' 31.32” N. lat. 118° 30'

57.97” W. long.). This area is a part of the Arrow Point to Lion Head SMCA. However, only take of invertebrates is prohibited within this SMCA and it served as the non-MPA location for fish surveys. Non-MPA locations were at least 1.6 km from the MPA boundary. Previous studies have observed increases in abundance and size of kelp bass and sheephead inside the Catalina Marine Science Center State Marine Reserve compared to unprotected reefs at non-MPA locations surveyed in the present study

(Froeschke et al. 2006, Hamilton et al. 2007, Tetreault and Ambrose 2007).

Anacapa Island is a part of the Channel Islands National Park and is 18 km off the coast of Port Hueneme, California. The island is the smallest and furthest east of the northern Channel Islands and is comprised of three islands running east to west (Figure

1.1). On the north side of the island lie the Anacapa SMR and the Anacapa SMCA. The

Anacapa SMR was originally established as the Anacapa Island Ecological Reserve in

1978. Boundaries of the Anacapa SMR to the coastline are 34° 00.417' N. lat. 119°

24.600' W. long.; 34° 04.998' N. lat. 119° 24.600' W. long.; 34° 04.998' N. lat. 119°

21.400' W. long.; 34° 01.000' N. lat. 119° 21.400' W. long.; and 34° 00.960' N. lat. 119°

21.449' W. long., and encompass the east and west islets. This MPA prohibits take of all living resources and has an area of 29.9 km2. Likewise, the Anacapa SMCA was

! ! ! 17 ! originally a part of the Anacapa Island Ecological Reserve with seasonal openings to fishing. As of 2003, this MPA was designated as a no-take of living, geological, or cultural resources except for the recreational take of spiny lobster and pelagic finfish.

Pelagic finfish are transient species to the rock reef/kelp forest system and use a wide range of habitats. The SMCA has been fully protected against fishing for at least ten years, therefore, the Anacapa SMCA was treated as a part of the MPA region surveyed at this site. The boundaries for the Anacapa SMCA are 34° 00.828' N. lat. 119° 26.623' W. long.; 34° 00.800' N. lat. 119° 26.700' W. long.; 34° 04.998' N. lat. 119° 26.700' W. long.; 34° 04.998' N. lat. 119° 24.600' W. long.; and 34° 00.417' N. lat. 119° 24.600' W. long. The waters off the northern side of Anacapa Island are protected from fishing.

Although potential oceanographic differences in currents and wave exposure could be present, the best available reference location for non-MPA surveys was located off the southern side of the island, where habitat conditions were similar to those of the northern facing MPAs. The western Northern Channel Islands lie within the cool California

Current while the eastern islands, of which Anacapa is one, are in the warmer Southern

California Countercurrent (Hamilton et al. 2009). The sharp gradients between eastern and western islands in sea surface temperature, productivity, wind stress, and wave exposure put the Northern Channel Islands within three separate bioregions and within these regions the kelp forest fish community changes significantly (Harms and Winant

1998, Dever 2004, Blanchette et al. 2006, Hamilton et al. 2009). However, the bioregion and sea surface temperature are similar on both protected and unprotected sides of

Anacapa Island as well as the eastern side of Santa Cruz Island (Hamilton et al. 2009).

One transect for the deepest depth bin (>12 - 18 m) was done on the eastern side of Santa

! ! ! 18 !

Cruz Island where fishing was permitted and habitat conditions were comparable to those of the MPA location off Anacapa Island. This transect was conducted in order for a balanced depth design in MPA and non-MPA locations for this site, and to maintain surveys over similar habitat inside and outside MPAs. MPA and non-MPA areas were separated by at least 0.8 km. Protection from fishing off Anacapa Island has benefitted invertebrate and algal species (Behrens and Lafferty 2004, Lafferty 2004, Babcock et al.

2010) as well as kelp bass and sheephead (Tetreault and Ambrose 2007, Hamilton et al.

2009).

Sampling Design

Fish surveys within MPA and non-MPA locations were conducted during daylight hours (08:00-16:00) using belt-transects conducted on SCUBA (Brock 1954). Each site was surveyed during the same season and within 7-day interval (one day for scouting similar reef habitat and six for surveys) to get a representative snapshot in time of the kelp forest fish community. For surveys, depth was standardized for both MPA and non-

MPA locations at each site. Four transects were conducted within three depth bins of < 6 m, 6 - 12 m, and >12 - 18 m, for a total of 12 replicate transects in each MPA and non-

MPA per site. Before surveys, divers trained sizing fish to the nearest centimeter, and

MPA and non-MPA locations were scouted for reefs with comparable substrate composition, relief, and kelp density. The outer edges of reefs were not surveyed to limit possible . Fish surveys did not begin until comparable reefs were identified within the established depth bins for the MPA and non-MPA locations. Substrate composition was noted at the beginning and end of each transect, and number of

! ! ! 19 !

Macrocystis holdfasts were counted within the first 10 m. Transects were haphazardly placed within the location area. Each underwater transect was composed of separate transects at three vertical regions of the water column (holdfast, mid-water, and canopy).

Divers reeled out the 50 m transect behind them as they swam, identifying, counting, and visually estimating size to the nearest cm TL of transient and conspicuous fishes that occurred within the 50 x 2 x 1 m swath. The total volume surveyed per replicate, including the three depth strata was 300 m3, over a benthic area of 100 m2. Transects were separated from each other by at least 25 m to avoid surveying fish that may have moved between transects. Fish that swam up from behind the divers were not recorded during the survey to avoid recounting individuals. Holdfast and mid-water region transects were done simultaneously. To avoid recounting species that could possibly move between the two vertical regions during counts and keep a digital record of the transects, digital video transects (Ebeling et al. 1980a,b, Stephens et al. 1984; Larson and

DeMartini 1984) were performed using a GoPro HD Hero2 camera during the mid-water transect, along with standard counts and size estimation. Video recordings of the mid- water videotransects were viewed and analyzed on the same day. Fishes that were video recorded moving between the vertical strata during transects were removed from the second vertical strata observed to limit double counting fish. After conducting the holdfast and mid-water transects, the canopy region was surveyed using the same compass heading within 3 m of the surface.

In addition to estimating fish sizes to the nearest cm TL for each vertical stratum of the transect, “size surveys” within the transect area were obtained using parallel, length-calibrated lasers projected onto fishes and recorded with a mounted HD GoPro

! ! ! 20 !

Hero2 video camera (Gingras et al. 1998, Colin et al. 2003, Heppell et al. 2012). Fish size surveys were conducted after each vertical region within the transect area to validate length estimations during the transect. Two sets of lasers were set at 2.6 and 10.2 cm apart, and were accurate and visible up to 9 m underwater with good visibility. To reduce size estimation error fish were not measured at a distance greater than 2.5 m (Heppell et al. 2012). During fish size surveys, all fishes within the transect area for each vertical region were targeted by the lasers and a video record was taken. Though an attempt was made to laser and video all fishes within the transect area, the species and sizes of the fish similar to those that occurred during the survey were targeted. In the lab, fish that occurred 90° to the video camera for each transect were sized (SL and TL cm) using the software program ImageJ (Figure 1.2). The lengths obtained from the size surveys were used to validate size estimations for fishes counted during the corresponding transect and pass of similar lengths. To determine biomass of each fish, lengths for each individual were converted to weights (g WWt) using length-weight relationships for each species

(Table 1.2) and converted to biomass using the estimated transect area (g/100m2).

Analysis of the fish trophic structure included all conspicuous species (n = 23) observed during surveys. Several species occurred on transects that as adults are secondary carnivores, but as young-of-the-year are primary carnivores. Black and yellow rockfish

(Sebastes chrysomelas), blue rockfish (Sebastes mystinus), chilipepper rockfish (Sebastes goodei), gopher rockfish (Sebastes caranatus), and California scorpionfish (Scorpaena guttata) were only observed as young-of-the-year, and thus considered primary carnivores. Also, young-of-the-year kelp bass < 7 cm SL, juvenile sheephead, and young- of-the-year kelp rockfish were categorized as primary carnivores due to their feeding on

! ! ! 21 ! zooplankton and other microinvertebrates during this life stage. Transient pelagic fishes were recorded during surveys, but they were not included in analyses. It was assumed that these species use a variety of habitats and roam over large expanses of open ocean, and thus their assemblages would not differentially affect nor be affected by protection in

MPAs. Hence, transient species were not included in analyses.

Statistical Analyses

To analyze fluctuations in fish trophic structure abundance (numerical and biomass density) in relation to fishing pressure, each conspicuous fish species was grouped into a trophic level based on dietary habits and life stage according to Cross and

Allen (1993). Trophic levels included in this study were herbivore/omnivore, primary carnivore, and secondary carnivore. The tertiary carnivore level included only giant sea bass, which was not observed during the surveys, and therefore, was not included in statistical analyses. Before analyses, a Shapiro-Wilk test (Shapiro and Wilk 1965) was used to test for homogeneity of variance among treatments. Biomass density (g/100 m2) was log10 (x+1) transformed to fit assumptions of normality. Numerical density (#/100 m2) was square root transformed (y’= √y’) to meet assumptions and retain information regarding relative abundance (Clarke and Green 1988). I investigated fish trophic structure differences of the three trophic level biomass and numerical densities with a two-fixed factor sampling design (Site: 3 levels; Protection [MPA/non-MPA]: 2 levels) using multivariate analysis of variance (MANOVA). Multivariate analyses were done on log10 (x +1) transformed data to meet assumptions of multivariate normality, homoscedasticity, and equal covariance matrices that are required for MANOVA. To

! ! ! 22 ! evaluate the hypotheses that secondary carnivores decrease, primary carnivores increase, while herbivore/omnivores show no differences outside versus inside of MPAs, I performed three, two-factor univariate analysis of variances (ANOVAs) for each trophic level to the factors of site and protection with biomass and numerical densities as response variables. MANOVA and ANOVAs were run in the statistical software program

R (R Core Team 2013).

Furthermore, to address my hypothesis that lower abundance of large kelp bass

(>25 cm) will show higher abundance in specific prey species outside MPAs, and to investigate fishing effects at the species-level, I used PERMANOVA. Data for the analysis of the abundance of individual fish species inside and outside MPAs included many zeros, was positively skewed, and could not fit the assumption of normality required for parametric statistical testing. To analyze heterogeneous dispersions, which occur frequently in nature (Anderson and Millar 2004), the use of permutational methods allows ecologists to effectively analyze biological interactions in ecological communities.

Univariate permutational analysis of variance with PERMANOVA+ for PRIMER-E ver.

6 (Anderson 2001, Anderson and Millar 2004) was used to test for differences in individual species’ densities between the fixed factors of site and protection.

PERMANOVA+ allows multivariate and univariate data to be tested by any resemblance matrix (e.g., Bray-Curtis dissimilarity), and all tests of hypotheses are done using permutations for robustness (Anderson et al. 2008). If there is only one variable in the analysis and Euclidean distances are used, then the PERMANOVA F-ratio is identical to the F-statistic (Fisher 1924) in traditional ANOVA (Anderson et al. 2008). However, the statistic used in PERMANOVA is the pseudo-F-statistic because it has an unknown

! ! ! 23 ! distribution under a true null hypothesis (Anderson et al. 2008). Significant differences in

PERMANOVA are determined as P(perm)<0.05. Data was log10 (x+1) transformed for biomass densities and square root transformed for numerical densities. The resemblance matrix used in this study was calculated Euclidean dissimilarity distances for each species for 999 permutations. Eleven species were included in PERMANOVA biomass and numerical density analyses under the criteria of having a considerable abundance on reefs at all sites, being potential target species in the recreational fishery, and/or prey species to piscivorous fishes. Of the eleven species, kelp bass were categorized into three size/age classes; YOY = <7 cm, Small = 7-25 cm, and Large = >25 cm SL. Sheephead were categorized by three gender/life stages, namely Juvenile, Female, and Male.

Results

Trophic Structure: Numerical Densities

Multivariate analysis for numerical densities (#/100 m2) of the three trophic levels

(Table 1.3; Figure 1.3) showed significant differences in relation to the two factors Site

(F=6.47, P<0.001) and Protection (F=15.87, P<0.001). Differences among sites were largely attributed to lower numerical densities at the mainland site (La Jolla) in comparison to the two island sites (Catalina and Anacapa). Numerical densities for La

Jolla were 3.7x less than Catalina and 1.7x less than Anacapa.

Further univariate analyses of each trophic level (Table 1.4) revealed that herbivore/omnivores (Figure 1.4) had lower numerical densities outside of MPAs

(F=8.69, P=0.004). Similarly, secondary carnivores (Figure 1.4) had lower densities outside of MPAs (F=23.67, P<0.001), as well as showed differences in abundance among

! ! ! 24 ! sites (F=8.33, P<0.001). Site differences for secondary carnivores were likely due to higher total numerical densities observed at Catalina compared to La Jolla (2x) and

Anacapa (1.6x). In an inverse trend to the secondary carnivores and herbivore/omnivores, the primary carnivores (Figure 1.4) showed a non-significant trend in higher numerical densities outside of MPAs (F=3.22, P=0.07). A significant difference among sites was observed (F=23.57, P<0.001). Differences among sites were attributed to total numerical densities at Catalina being higher than both La Jolla (3.5x) and Anacapa (2x). Mean numerical densities (Figure 1.3) were higher inside MPAs for herbivore/omnivore (12.64

± 2.12 no. fish/100 m2) and secondary carnivore (19.61 ± 2.3 no. fish/100 m2) trophic levels compared to corresponding non-MPA locations (herbivore/omnivore: 6.14 ± 1.57 no. fish/100 m2; secondary carnivore: 8.8 ± 1.25 no. fish/100 m2). Primary carnivores showed a trending inverse relationship of overall lower mean numerical densities inside

MPAs (152.94 ± 18.67 no. fish/100 m2) compared to non-MPAs (206.64 ± 30.4 no. fish/100 m2).

Trophic Structure: Biomass Densities

Biomass densities (g/100 m2) of the fish community showed stronger contrasts among trophic levels due to protection than numerical densities. Multivariate analysis of the three trophic levels (Table 1.5; Figure 1.5) differed with the main effects of Site

(F=9.19, P<0.001) and Protection (F=13.02, P<0.001). Site differences in trophic structure were attributed to considerably lower biomass densities between La Jolla and

Catalina/Anacapa. Biomass densities for La Jolla were 2.6x less than Catalina and 3.1x less than Anacapa.

! ! ! 25 !

Univariate analyses for the biomass densities of each trophic level (Table 1.6;

Figure 1.6) showed results similar to numerical densities, where herbivore/omnivores

(F=10.36, P=0.002) and secondary carnivores (F=32.97, P<0.001) significantly decreased outside of MPAs. The secondary carnivore level also showed differences between sites (F=10.38, P<0.001), as overall biomass densities among sites were different, but displayed similar patterns inside and outside of MPAs. The primary carnivores (Figure 1.6) exhibited an opposite pattern with biomass being significantly higher outside MPAs (F=4.23, P=0.04). Primary carnivore biomass also differed between sites (F=38.63, P<0.001), and was likely attributed to higher overall biomass between the island sites (Catalina and Anacapa) and the mainland site (La Jolla). Mean biomass inside

MPAs of herbivore/omnivores (7.90 ± 1.44 kg/100 m2) and secondary carnivores (10.26

± 1.65 kg/100 m2) were higher compared to non-MPA locations (herbivore/omnivore:

2.68 ± 0.71 kg/100 m2; secondary carnivore: 1.95 ± 0.32 kg/100 m2). Primary carnivores had a lower mean biomass inside MPAs (4.49 ± 0.55 kg/100 m2) in contrast to non-

MPAs (6.78 ± 0.93 kg/100 m2).

Species-Level Analysis

Two of the three target secondary carnivores showed significantly lower abundances outside MPAs as well as biogeographic differences per site. Sheephead

(Figure 1.7) were grouped by males, females, and juveniles. Male sheephead numerical densities (Table 1.7) were significantly lower outside of MPAs (pseudo-F=24.03,

P(perm)<0.001) with a significant interaction between site and protection (pseudo-F=3.95,

P(perm)=0.03), attributed to a non-significant decrease outside of MPAs in La Jolla.

! ! ! 26 !

Biomass of male sheephead (Table 1.8) followed a similar trend (pseudo-F=29.26,

P(perm)<0.001) with an interaction (pseudo-F=3.99, P(perm)=0.023). Overall, large male sheephead were almost exclusively found in MPAs. Female sheephead biomass (Table

1.8) and numerical densities (Table 1.7) did not significantly differ across sites or due to protection. Juvenile sheephead showed a difference among sites for both numerical

(pseudo-F=22.81, P(perm) <0.001) and biomass densities (pseudo-F=19.03, P(perm) <0.001).

Piscivore results (Table 1.7, 1.8) showed significant site differences for kelp rockfish (Figure 1.9) numerical densities (pseudo-F=3.02, P(perm)=0.04). The most abundant piscivore, kelp bass (Figure 1.8) numerical (Table 1.7) and biomass densities

(Table 1.8), showed a large decrease outside of MPAs for individuals >25 cm (numerical densities: pseudo-F=30.16, P(perm)<0.001; biomass: pseudo-F=28.84, P(perm)<0.001). Kelp bass 7-25 cm showed differences in relation to sites (numerical densities: pseudo-

F=19.93, P(perm)< 0.001; biomass: pseudo-F=8.63, P(perm)=0.002) and had lower densities outside of MPAs (numerical densities: pseudo-F=8.37, P(perm)= 0.009; biomass: pseudo-

F=6.19, P(perm)= 0.02). Kelp bass 7-25 cm also had a significant interaction effect for biomass densities (pseudo-F=3.28, P(perm)=0.046) , as there was no significant difference in biomass between MPAs and non-MPAs for Catalina. Kelp bass <7 cm showed strong differences among sites (numerical densities: pseudo-F=68.72, P(perm)<0.001; biomass: pseudo-F=50.63, P(perm)<0.001) with a significant interaction (numerical densities: pseudo-F=6.85, P(perm))=0.004; biomass: pseudo-F=6.93, P(perm)=0.003), as overall densities were considerably greater at Catalina and in the non-MPA location for that site.

However, no discernible pattern inside and outside MPAs for kelp bass <7 cm was consistently found among the three sites.

! ! ! 27 !

Of the primary carnivores included in species level analysis, two of the species

(black perch and garibaldi) were included for being abundant during surveys, occurring at all sites, and for potential population regulation by kelp bass due to predation on recruits.

Black perch (Figure 1.9) significantly differed among sites for both numerical (Table 1.9: pseudo-F=5.14, P(perm)=0.02) and biomass densities (Table 1.10: pseudo-F=4.6,

P(perm)=0.005), and a significant interaction (numerical densities: pseudo-F=4.45, P(perm)=

0.02; biomass: pseudo-F=4.13, P(perm)= 0.01), due to large disordered fluctuations inside and outside of MPAs. Likewise, garibaldi (Figure 1.9) only differed among sites in numerical (Table 1.9: pseudo-F=9.6, P(perm))< 0.001) and biomass densities (Table 1.10: pseudo-F=6.1, P(perm)< 0.001), as a total higher abundance was observed at Catalina compared to La Jolla and Anacapa.

The four fishes included in the species level analysis as prey species for large kelp bass (Figure 1.10: kelp perch, blacksmith, señorita; Figure 1.11: rock wrasse) showed varying relationships for the factors site and protection. Both blacksmith (Figure 1.10) and rock wrasse (Figure 1.11) showed no significant pattern related to protection. The abundance of blacksmith differed to site in numerical (Table 1.9: pseudo-F=15.94,

P(perm)< 0.001) and biomass densities (Table 1.10: pseudo-F=12.5, P(perm)< 0.001), with high numbers of recruits at Catalina and larger individuals at the Anacapa non-MPA location. Rock wrasse biomass was significantly different among sites (pseudo-F=7.35,

P(perm)=0.001). There also was a significant interaction for rock wrasse (numerical densities: pseudo-F=8.12, P(perm)=0.002; biomass: pseudo-F=10.08, P(perm)=0.001), attributed to inconsistent differences inside versus outside of MPAs per site. Señorita

(Figure 1.10) numerical densities (Table 1.9) showed no significant effect to protection or

! ! ! 28 ! site. On the other hand, señorita biomass (Table 1.10) was significantly different in respect to site (pseudo-F=6.24, P(perm)= 0.003), as much higher biomass was observed at

Anacapa compared to La Jolla and Catalina. Likewise, señorita showed a trend of larger individuals and higher biomass outside of MPAs. However, this increase was not statistically significant (pseudo-F=3.75, P(perm)=0.052). Kelp perch (Figure 1.10) numerical densities (Table 1.9) were significantly higher outside of the MPAs (pseudo-

F=6.94, P(perm)=0.012). However, the trend in higher kelp perch biomass (Table 1.10) outside MPAs among sites was not significant (pseudo-F=2.92, P(perm)=0.08).

Two of the three species within the herbivore/omnivore level were included in species level analysis for having high abundances on surveys and occurring at all three sites. Halfmoon (Figure 1.11) showed no significant differences in relation to protection or sites for both numerical (Table 1.11) and biomass densities (Table 1.12). On the other hand, opaleye (Figure 1.11) followed a similar pattern to target secondary carnivore species, with lower numerical (Table 1.11: (pseudo-F=8.99, P(perm)=0.007) and biomass densities (Table 1.12: pseudo-F=11.91, P(perm)=0.002) outside MPAs.

Discussion

Trophic Level Response to Fishing

The results of this study provide several insights into the direct and indirect impacts of fishing on the kelp forest fish community throughout a wide geographic range within the Southern California Bight. Overall, numerical and biomass densities within trophic levels differed among sites and protection (inside and outside MPAs). Secondary carnivores strongly decreased overall in biomass (5.3x) and densities (2.2x) outside MPA

! ! ! 29 ! locations at all three sites, providing support for my first hypothesis that the secondary carnivore trophic level will decrease outside of MPAs. This result was expected as the secondary carnivores included several important target species in the southern California recreational fishery. The greater decrease of biomass relative to numerical densities for secondary carnivores outside MPAs was attributed to smaller individuals outside of the

MPAs coupled with lower numerical densities.

In the absence of large piscivores, smaller prey fishes can grow to larger body sizes (DeMartini et al. 2008), and can potentially allow them to escape predation

(Mumby et al. 2006). In an inverse pattern to predatory secondary carnivores, the primary carnivore trophic level was significantly higher in biomass densities (1.5x) outside of

MPAs, supporting my second hypothesis that primary carnivores, which consist of many smaller prey fishes, would increase outside of MPAs. However, this hypothesis was only partially supported, as the slight trend of increasing densities outside MPAs (1.3x) was not significant for the trophic level. This suggests that the primary carnivores as a whole were larger in body size outside MPAs, and though increases were observed in numerical densities, these were not significant. Herbivore/omnivores had unexpectedly lower biomass (3.0x) and numerical densities (2.0x) outside MPAs in a similar fashion to secondary carnivores. This decrease of the herbivore/omnivore level further confounded a full acceptance of my second hypothesis, as no change was expected due to the larger body size of these species, which should protect them from predation by reef associated piscivorous fishes, and for not being targeted in the southern California recreational fishery.

! ! ! 30 !

There were considerable differences in both numerical and biomass densities among the three sites. This was largely attributed to biogeographic differences, where lower overall numerical and biomass densities occurred at the mainland site (La Jolla) compared to island sites (Catalina and Anacapa Island). Likewise, at La Jolla, the abundance of primary carnivores was similar inside and outside of the MPA. While,

Catalina contained the largest number of recruits both in MPA and non-MPA locations showing higher densities at this site. Furthermore, Anacapa contained higher biomass densities among the secondary carnivores due to larger sheephead and kelp bass. Thus, the biomass density of secondary carnivores was highest at Anacapa compared to

Catalina and La Jolla. Despite these site differences, a strikingly similar pattern in the overall trophic structure biomass was observed in MPA and non-MPA locations. At each site, secondary carnivores and herbivore/omnivores dominated the trophic fish biomass within the MPAs. On the other hand, the primary carnivores dominated the fish biomass outside of protection in the non-MPA locations (Figure 1.5). This was attributed to several combined increases of planktivorous and mesograzer species or overall biomass stability (La Jolla) within the primary carnivore trophic level, and decreases of target secondary carnivores and abundant herbivore/omnivores. This pattern suggests a fishing induced shift in the trophic structure of kelp forest fishes outside of protected areas.

However, these findings are in contrast to those found in the marine reserve meta- analysis by Halpern (2003) where all functional groups (invertebrates, herbivorous fishes, planktivores/invertebrate eating fishes, and carnivorous fishes) increase inside MPAs in almost all cases. However, an explanation for this result could be that the detection of top down control or trophic cascades within a community could be masked when analyzing a

! ! ! 31 ! large number of species (Polis and Strong 1996, Halpern 2003). Furthermore, my results are different than those of Hamilton et al. (2009) who found that after the first five years of protection in the northern Channel Islands marine reserve network, piscivore and other carnivore functional groups increased within the reserves, but no discernible difference was detected for planktivores or herbivores relative to protection. However, Hamilton et al. (2009) found differences in community structure over relatively small spatial scales due to differences in sea surface temperature and other environmental changes among the northern Channel Islands. It is also possible that Hamilton et al. (2009) were unable to detect lower trophic level effects because of the shorter time period in which the reserve network had been established. Despite these conclusions, top down influences have been observed in relation to fishing pressure in other marine ecosystems on the level of trophic/functional groups (Daskalov et al. 2007) and in extensive analysis of species within communities (Watson et al. 2007). In the Black Sea, Daskalov et al. (2007) showed decreases in the overall trophic group of piscivores led to a dominant abundance of planktivorous fishes. While in the temperate-tropical transition zone off the Abrolhos

Islands, Watson et al. (2007), documented that lower abundance of five prominent smaller-bodied reef fishes was likely related to increases of target piscivores inside

MPAs. The findings of my study are indicative of trophic structure changes in relation to fishing pressure within the southern Californian kelp forest fish community with decreases in larger secondary carnivore predators and herbivore/omnivores, and increases in smaller bodied primary carnivores.

! ! ! 32 !

Response of Target Species to Fishing

Changes in individual populations fluctuated to varying degrees in MPA and non-

MPA locations. Of target secondary carnivores included in the species level analysis, two of the three species showed decreases in fished locations. The effect of fishing on the target invertivore, sheephead, differed among life stages (Figure 1.7). Male sheephead densities (10x) and biomass (96.1x) were much lower outside MPAs. This large difference was because most individuals were much larger and almost exclusively observed in MPAs (e.g., no male sheephead were observed during Anacapa non-MPA surveys). However, neither females nor juveniles showed discernible differences or patterns relative to protection. Of the two abundant piscivores (kelp bass and kelp rockfish), only kelp bass were influenced by fishing as no apparent pattern was observed for kelp rockfish. Large legal size kelp bass (>25 cm SL) greatly decreased in numerical

(3.7x) and biomass (6.5x) densities outside MPAs at each site. Smaller kelp bass 7-25 cm

SL followed a more mild decrease outside of MPAs. However, this trend was not apparent at Catalina. Kelp bass young-of-the-year < 7 cm SL showed site-specific differences, but not relative to protection. The dramatic response of large target fishes to protection from fishing is in concordance with the numerical and biomass density findings of previous studies in southern California kelp forests (Halpern 2003, Froeschke et al. 2006; Tetreault and Ambrose, 2007).

Herbivore/Omnivore Decreases in Non-MPAs

An unexpected result from the trophic structure analysis was the decrease in the herbivore/omnivore trophic level outside MPAs. Two abundant species within this

! ! ! 33 ! trophic level are the opaleye and halfmoon (Figure 1.11). Halfmoon presence was considerably less than opaleye, and besides being largely abundant in the MPA location at Catalina and smaller individuals in La Jolla, halfmoon did not appear to benefit from the protection afforded by the MPAs. On the other hand, the more abundant opaleye, had consistently lower numerical (2.1x) and biomass densities (3.2x) outside MPAs. Due to their large body size reaching up to 65 cm TL and 6 kg, predation by kelp bass should not have a large effect on adult opaleye reef populations. However, it is possible that decreases in target species (sheephead and kelp bass) that could be preferred food to predators with larger home-ranges than set MPA boundaries (i.e. pinnipeds, soupfin sharks, angel sharks, Brandt’s cormorants, and/or giant sea bass) or cryptic reef predators

(California moray eel), could switch to a more accessible prey (Murdoch and Smyth

1975). for opaleye was also expected to have little effect on population size as they are categorized as an “incidental-catch” species and therefore not targeted by anglers. However, from the years 2003-2013 mean total recreational catch of opaleye off southern California (56,060 ± 6,866) was as high if not higher than several target species such as olive rockfish (21,298 ± 5,363), kelp rockfish (17,588 ± 4,103), as well as the highly sought after sheephead (49,504 ± 4,215). Comparing sheephead and opaleye CPUE (Figure 1.12), a steady decrease in catch was seen in sheephead from

2003-2013. However, the trend in opaleye CPUE is harder to discern. After a peak in

2004 and subsequent decrease in 2005, there was a strong increase in CPUE from 2006-

2010, with sharp decreases until 2013. Altogether, the mean number of harvested opaleye per angler is 4.1x that of sheephead, suggesting that though they may not be a target species they are taken in considerable number by anglers in southern California.

! ! ! 34 !

However, there are still other explanations for opaleye decreases in areas outside MPAs.

The increase of large bodied reef associated herbivores inside MPAs has also been documented in other ecosystems (Mumby et al. 2006, Watson et al. 2007). It is possible that large bodied herbivores can escape predation by reef piscivores (Mumby et al. 2006), and possibly out compete less abundant smaller bodied individuals for habitat and food within MPAs (Watson et al. 2007). In addition, a possible explanation to this pattern could be of fine-scale habitat characteristics that are difficult to detect (Watson et al.

2007). MPA and non-MPA locations were surveyed in similar substrate composition and kelp density at each site, and opaleye are commonly found in deforested reefs (Graham

2004), suggesting kelp presence to not be a definitive factor for population abundance.

However, other possibilities could be that of spatial secondary habitat characteristics that were not detected during my study. Opaleye appear to show a preference for large reefs in close proximity to adjoining reefs (E. Parnell unpub. data). As many MPAs are selected for areas rich in available habitat for many reef fishes, the overall size and proximity of individual reefs and the distance to each other could also influence opaleye population abundances.

Indirect Impacts of Fishing on Predator-Prey Interactions!

Direct removals of predators can indirectly release top-down pressure on prey populations. As evidenced from previous studies in other marine ecosystems (Mueter and

Norcross 2000, Dulvy et al. 2004, Blanchard et al. 2005, Daan et al. 2005, Frank et al.

2005, Watson et al. 2007, DeMartini et al. 2008), my study found an indirect effect of fishing by observed increases of a non-target prey species, and the primary carnivore

! ! ! 35 ! trophic level, in areas subject to fishing pressure. Kelp perch numerical densities significantly increased (2.9x) in non-MPA locations. This result is likely due to strong decreases in fished areas of large kelp bass in fished areas, the primary piscivore of this system. This suggests weakened top-down control by kelp bass on the kelp perch population, and provides support for my third hypothesis that decreases in large >25 cm piscivorous kelp bass will alternatively show increases in prey reef fishes outside MPAs.

Fluctuations in abundance of kelp perch could further influence ecosystem dynamics on the primary producer level (Davenport and Anderson 2007). However, the biomass densities of kelp perch showed a non-significant increase outside MPAs. The higher numerical densities compared to biomass outside MPAs was attributed to more juveniles and smaller individuals being present in non-MPA locations compared to larger adults in

MPAs, possibly large enough to evade predation by smaller kelp bass. Likewise, another prey reef fish, señorita, showed a non-significant trend of higher biomass densities (2.3x) and overall larger individuals outside of MPAs. This is a trend that if biologically significant could likewise affect kelp forest structure. Señorita, similar to kelp perch, are important predators of mesograzers that feed on Macrocystis blades and fluctuations in the abundance of these fish could either alleviate pressure on Macrocystis from mesograzers (Bernstein and Jung 1979, Davenport and Anderson 2007), or decimate kelp forests while feeding on encrusted blades (Bernstein and Jung 1979). Similar to my results, Tetreault and Ambrose (2007) found a trend toward higher señorita biomass outside of MPAs. However, they provided little information on kelp perch densities. The fourth prey species analyzed, rock wrasse, showed no discernible pattern in relation to

! ! ! 36 ! fishing pressure. Likewise, no pattern was detected among sites for black perch and garibaldi in and out of MPAs.

Empirical studies have shown that large piscivores affect the abundance of prey reef fishes (Doherty and Sale 1985, Caley 1993, Carr and Hixon 1995, Hixon and Carr

1997). Additionally, there is experimental support for kelp bass influencing abundance and distributions of local populations and post settlement juveniles of kelp forest fishes

(Carr 1991, Steele 1997b, Steele 1998, Steele 1999, Anderson 2001) therefore potentially effecting community dynamics. In particular, Anderson (2001) found that aggregative predation responses of kelp bass negatively affected numerical densities of kelp perch.

However, there has yet been a study detecting an increase of prey reef fish assemblages due to kelp bass decreases in areas subject to fishing (Tetreault and Ambrose 2007,

Hamilton et al. 2009). A possible answer could lie in the life history of the kelp perch.

Kelp perch were found throughout the water column in kelp forests, however, juveniles tend to seek shelter in the kelp canopy. Tetreault and Ambrose (2007) surveyed in and out of five MPAs throughout southern California (several of which have now changed or consolidated), but underwater belt transects for estimating fish abundance and size were located on the benthos (holdfast region), and could likely fail to survey key species residing in the kelp canopies and midwater column. Also, a survey method was implemented in my study that provided more precise size estimations by reducing diver size estimation error. I used parallel length calibrated lasers mounted on a video camera for high resolution size surveys after transect counts. Another explanation for my findings besides variability in survey methods could be fluctuations of overall community dynamics in the 15 years since Tetreault and Ambrose (2007). Indirect effects of fishing

! ! ! 37 ! could take decades to manifest (Daan et al. 2005, Babcock 2010, Estes et al. 2011). This lag could explain a more recent change in the fish community makeup as differences between protected and nearby unprotected areas greaten over time. However, arguably the preeminent difference may be the return of the apex tertiary carnivore of this system.

Evidence suggests that the giant sea bass population is recently returning to southern

California waters since the mid-1990s (Pondella and Allen 2008) after close to 70 years of near extirpation. A contemporary presence of these large megacarnivores could greatly influence community dynamics within southern California kelp forests.

Future research should focus on documenting continued differences inside and outside of these long-standing MPAs, as well as newly formed MPAs from the Marine

Life Protection Act as of 2012, over longer periods of time throughout the Southern

California Bight. This is necessary in order to further learn and provide information for fisheries management on what impacts fishing for higher trophic level species may have, not just within the fish community, but the kelp forest ecosystem off southern California.

My study provides evidence that fishing not only directly affects targeted fishes in higher trophic levels, but also indirectly influences the trophic structure and community makeup of kelp forest fishes off southern California. The large reductions of the most ubiquitous piscivore of this system, kelp bass, released predation pressure on an abundant prey species as well as an overall increase in primary carnivore biomass outside

MPAs. This result suggests a weakening of top-down control on kelp forest reefs deficient in large kelp bass off southern California.

! ! ! 38 !

Table 1.1. Adult kelp forest/rocky reef conspicuous fishes observed during surveys. Species described by water column position (Holdfast, Midwater, and Canopy) and appropriate adult trophic level above primary producers: HO=Herbivore/Omnivore; PC=Primary Carnivore; SC=Secondary Carnivore. Compiled from Cross and Allen 1993, and Allen et al. 2006.

Trophic Scientific Name Common Name Canopy Mid Holdfast Level Brachyistius frenatus Kelp perch x x PC Cymatogaster aggregata Shiner perch x x PC Embiotoca jacksoni Black perch x PC Embiotoca lateralis Striped seaperch x PC Rhacochilus toxotes Rubberlip seaperch x x x SC Rhacochilus vacca Pile perch x SC Opaleye x x x HO Hermosilla azurea Zebraperch x x x HO Medialuna californiensis Halfmoon x x x HO Oxyjulis californica Señorita x x x PC Halichoeres semicinctus Rock wrasse x PC Semicossyphus pulcher California sheephead x x SC Chromis punctipinnis Blacksmith x x x PC Hypsypops rubicundus Garibaldi x PC Sebastes atrovirens Kelp rockfish x x x SC Sebastes serranoides Olive rockfish x x x SC Sebastes serriceps Treefish x SC Paralabrax clathratus Kelp bass x x x SC Paralabrax nebulifer Barred sand bass x SC

! ! ! 39 !

Table 1.2. Equations used for each conspicuous kelp forest fish species to convert length (TL or SL) to g Wwt (gram wet weight). Equations from Cailliet et al. (2000).

Species Length/Weight Equations Kelp bass g Wwt = 0.000002716(mm TL)3.28 Opaleye g Wwt = 0.00002(mm SL)3.08 Halfmoon g Wwt = 0.000003(mm SL)3.454 Señorita g Wwt = 0.00000128(mm SL)3.5 Blacksmith g Wwt = 0.0000185(mm SL)3.09 California sheephead g Wwt = 0.00002952(mm TL)2.9066 Garibaldi g Wwt = 0.000036(mm SL)3.10 Kelp perch g Wwt = 0.00001184(mm SL)3.1686 Black perch g Wwt = 0.00002(mm SL)3.149 Rock wrasse g Wwt = 0.0000045(mm TL)3.16 Shiner perch g Wwt = 0.000017(mm SL)3.125 Olive rockfish g Wwt = 0.00000631(mm TL)3.136 Kelp rockfish g Wwt = 0.0239(cm TL)2.862 Blue rockfish g Wwt = 0.0158(cm TL)2.988 Pile perch g Wwt = 0.0156(cm TL)2.998 Rubberlip seaperch g Wwt = 0.00000457(mm SL)3.36 Striped seaperch g Wwt = 0.0000000154(mm TL)3.01 California scorpionfish g Wwt = 0.0000398(mm SL)2.98 Treefish g Wwt = 0.014(cm TL)3.081 Gopher rockfish g Wwt = 0.0186(cm TL)2.957 Chilipepper g Wwt = 0.0076(cm TL)3.12 Barred sand bass g Wwt = 0.000006844(mm TL)3.1128

! ! ! 40 !

Table 1.3. Results of multivariate analysis of variance (MANOVA) comparing numerical densities of fishes in the three trophic levels among sites and between protection status (inside and outside MPAs).

Source df Pillai trace F Num. df P Site 2 0.46 6.47 6 < 0.001 Protection 1 0.43 15.87 3 < 0.001 Site x Protection 2 0.09 1.07 6 0.39 Residual 66

Table 1.4. Results of univariate analyses of variance (ANOVA) comparing the numerical densities of fishes in each of the three trophic levels (Herbivore/Omnivore, Primary Carnivore, Secondary Carnivore) among sites and between protection status (inside and outside MPAs).

Source df MS F P Herbivore/Omnivore Site 2 5.09 1.5 0.23 Protection 1 29.47 8.69 0.004 Site x Protection 2 0.96 0.28 0.75 Residual 66 3.39 Primary Carnivore Site 2 393.61 23.57 < 0.001 Protection 1 53.83 3.22 0.07 Site x Protection 2 24.07 1.44 0.24 Residual 66 16.7 Secondary Carnivore Site 2 13.12 8.33 < 0.001 Protection 1 37.25 23.67 < 0.001 Site x Protection 2 1.56 0.99 0.38 Residual 66 1.57

! ! ! 41 !

Table 1.5. Results of multivariate analysis of variance (MANOVA) comparing biomass densities of fishes in the three trophic levels among sites and between protection status (inside and outside MPAs).

Source df Pillai trace F Num. df P Site 2 0.6 9.19 6 < 0.001 Protection 1 0.38 13.02 3 < 0.001 Site x Protection 2 0.05 0.52 6 0.8 Residual 66

Table 1.6. Results of univariate analyses of variance (ANOVA) comparing the biomass densities of fishes in each of the three trophic levels (Herbivore/Omnivore, Primary Carnivore, Secondary Carnivore) among sites and between protection status (inside and outside MPAs).

Source df MS F P Herbivore/Omnivore Site 2 3.72 1.51 0.23 Protection 1 25.49 10.36 0.002 Site x Protection 2 0.01 0.004 0.99 Residual 66 2.46 Primary Carnivore Site 2 4.29 38.63 < 0.001 Protection 1 0.47 4.23 0.04 Site x Protection 2 0.08 0.74 0.24 Residual 66 0.11 Secondary Carnivore Site 2 3.56 10.38 < 0.001 Protection 1 11.3 32.97 < 0.001 Site x Protection 2 0.22 0.64 0.53 Residual 66 0.34

! ! ! 42 !

Table 1.7. Results of PERMANOVA comparing numerical densities of target secondary carnivores among sites and between protection status.

Source df MS F P Paralabrax clathratus > 25 cm Site 2 2.64 2.09 0.14 Protection 1 38.2 30.16 < 0.001 Site x Protection 2 1.92 1.51 0.23 Residual 66 1.27 Paralabrax clathratus 7-25 cm Site 2 18.71 19.93 < 0.001 Protection 1 7.86 8.37 0.009 Site x Protection 2 1.07 1.14 0.32 Residual 66 0.94 Paralabrax clathratus < 7 cm Site 2 88.14 68.72 < 0.001 Protection 1 2.26 1.8 0.188 Site x Protection 2 8.79 6.85 0.004 Residual 66 1.28 Sebastes atrovirens Site 2 3 3.02 0.04 Protection 1 0.017 0.017 0.89 Site x Protection 2 0.55 0.55 0.58 Residual 66 Semicossyphus pulcher (Male) Site 2 0.38 1.64 0.21 Protection 1 5.55 24.03 < 0.001 Site x Protection 2 0.91 3.95 0.03 Residual 66 Semicossyphus pulcher (Female) Site 2 1.3 2.63 0.09 Protection 1 0.37 0.76 0.42 Site x Protection 2 0.18 0.36 0.7 Residual 66 Semicossyphus pulcher (Juvenile) Site 2 4.66 22.81 < 0.001 Protection 1 0.16 0.81 0.41 Site x Protection 2 0.18 0.9 0.41 Residual 66 0.2

! ! ! 43 !

Table 1.8. Results of PERMANOVA comparing biomass densities of target secondary carnivores among sites and between protection status.

Source df MS F P Paralabrax clathratus > 25 cm Site 2 5.56 5.96 0.004 Protection 1 26.9 28.84 < 0.001 Site x Protection 2 0.95 1.02 0.35 Residual 66 0.93 Paralabrax clathratus 7-25 cm Site 2 5.06 8.63 0.002 Protection 1 3.63 6.19 0.017 Site x Protection 2 1.92 3.28 0.046 Residual 66 0.59 Paralabrax clathratus < 7 cm Site 2 19.14 50.63 0.001 Protection 1 0.02 0.06 0.791 Site x Protection 2 2.62 6.93 0.003 Residual 66 0.38 Sebastes atrovirens Site 2 1.35 1.11 0.32 Protection 1 0.13 0.1 0.74 Site x Protection 2 1.43 1.18 0.29 Residual 66 1.22 Semicossyphus pulcher (Male) Site 2 3 1.93 0.14 Protection 1 45.58 29.26 < 0.001 Site x Protection 2 6.22 3.99 0.023 Residual 66 1.56 Semicossyphus pulcher (Female) Site 2 4.51 2.31 0.11 Protection 1 2.78 1.43 0.24 Site x Protection 2 0.75 0.38 0.67 Residual 66 1.95 Semicossyphus pulcher (Juvenile) Site 2 6.13 19.03 < 0.001 Protection 1 0.24 0.75 0.4 Site x Protection 2 0.27 0.84 0.5 Residual 66 0.84 !

! ! ! 44 !

Table 1.9. Results of PERMANOVA comparing numerical densities of non-target primary carnivores among sites and between protection status.

Source df MS F P Brachyistius frenatus Site 2 55.64 5.15 0.012 Protection 1 74.95 6.94 0.012 Site x Protection 2 6.78 0.63 0.56 Residual 66 Embiotoca jacksoni Site 2 2.84 5.14 0.02 Protection 1 0.22 0.4 0.55 Site x Protection 2 2.46 4.45 0.02 Residual 66 0.55 Chromis punctipinnis Site 2 299.37 15.94 < 0.001 Protection 1 0.417 0.42 0.52 Site x Protection 2 0.32 0.32 0.76 Residual 66 Hypsypops rubicundus Site 2 9.25 9.6 < 0.001 Protection 1 0.77 0.8 0.37 Site x Protection 2 0.83 0.86 0.43 Residual 66 0.86 Oxyjulis californicus Site 2 21.08 1.63 0.22 Protection 1 4.73 0.37 0.54 Site x Protection 2 11.12 0.87 0.42 Residual 66 12.01 Halichoeres semicinctus Site 2 1.7 1.75 0.17 Protection 1 2.46 2.54 0.14 Site x Protection 2 7.88 8.12 0.002 Residual 66 0.97 !! !!

! ! ! 45 !

! ! Table 1.10. Results of PERMANOVA comparing biomass densities of non-target primary carnivores among sites and between protection status.

Source df MS F P Brachyistius frenatus !! Site ! 2 ! 7.01 ! 9.95 0.002 Protection 1 2.05 2.92 0.08 Site x Protection 2 0.29 0.41 0.66 Residual 66 0.7 Embiotoca jacksoni Site 2 8.56 4.6 0.005 Protection 1 1.67 0.9 0.38 Site x Protection 2 7.67 4.13 0.013 Residual 66 1.86 Chromis punctipinnis Site 2 22.19 12.5 < 0.001 Protection 1 0.08 0.05 0.84 Site x Protection 2 0.85 0.48 0.48 Residual 66 1.78 Hypsypops rubicundus Site 2 12.92 6.1 0.003 Protection 1 0.87 0.41 0.55 Site x Protection 2 3.06 1.44 0.24 Residual 66 2.12 Oxyjulis californicus Site 2 5.82 6.24 0.003 Protection 1 3.5 3.75 0.052 Site x Protection 2 1.34 1.44 0.241 Residual 66 0.93 Halichoeres semicinctus Site 2 7.14 7.35 0.001 Protection 1 0.92 0.95 0.331 Site x Protection 2 9.78 10.08 0.001 Residual 66 0.97

! ! ! 46 !

Table 1.11. Results of PERMANOVA comparing numerical densities of herbivore/omnivores among sites and between protection status.

Source df MS F P Girella nigricans Site 2 4.72 1.53 0.21 Protection 1 27.83 8.99 0.007 Site x Protection 2 0.43 0.14 0.86 Residual 66 3.09 Medialuna californica Site 2 0.81 0.61 0.55 Protection 1 0.99 0.76 0.39 Site x Protection 2 1.82 1.38 0.28 Residual 66 1.32 ! ! ! ! ! ! Table 1.12. Results of PERMANOVA comparing biomass densities of herbivore/omnivores among sites and between protection status.

Source df MS F P Girella nigricans Site 2 6.45 2.55 0.08 Protection 1 30.21 11.91 0.002 Site x Protection 2 0.003 0.001 0.99 Residual 66 2.54 Medialuna californica Site 2 2.63 1.28 0.27 Protection 1 5.99 2.93 0.09 Site x Protection 2 5.99 2.93 0.06 Residual 66 2.04 !

! ! ! 47 !

Figure 1.1. Map of study sites within the Southern California Bight. A=Anacapa Island, B=Santa Catalina Island, C=La Jolla. Non-MPA locations were located west-southwest of Matlahuayl SMR, within the Arrow Point to Lion Head Point SMCA, and the leeward side of Anacapa Island.

! ! ! 48 !

! Figure 1.2. Example images from video taken during size surveys using parallel lasers projecting spots onto fishes. Top: kelp perch with 2.5 cm spaced lasers. Middle: example of size estimation using the software program ImageJ. Image shows señorita measured with 2.5 cm spaced lasers and length (cm TL) being determined. Bottom: example of size estimation using the software program ImageJ. Image shows a measured kelp bass with 10.2 cm spaced lasers and length (cm SL) being determined.

! ! !

! ! ! 49 !

!

! Figure 1.3. Mean numerical densities of fishes for secondary carnivore, primary carnivore, and herbivore/omnivore trophic levels in MPA and non-MPA locations for each site. Densities are log transformed to show patterns due to large differences in abundance between the trophic levels. !

! ! ! 50 !

Herbivore/Omnivore Protection: P < 0.001 25 20 15 10

)

2 5 0 Primary Carnivore

500 Site: P < 0.001 400 300 200 100 0

Secondary Carnivore Site: P < 0.001 Protection: P < 0.001 40 Mean Fish Numerical Density (#/100 m (#/100 Density Numerical Fish Mean 30 MPA

20 NON

10

0 La Jolla Catalina Anacapa ! Figure 1.4. Differences in mean numerical densities of fishes in the three trophic levels per site.

! ! ! ! ! !

51! !

!

! Figure 1.5.!Mean biomass densities of fishes for secondary carnivore, primary carnivore, and herbivore/omnivore trophic levels in MPA and non-MPA locations for each site.

! ! ! 52 !

Herbivore/Omnivore Site: P < 0.001 15 Protection: P < 0.001

10

)

2 5

0

Site: P < 0.001 Primary Carnivore Protection: P = 0.04 15

10

5

0

Site: P < 0.001 Secondary Carnivore Protection: P < 0.001 20

Mean Fish Biomass Density (kg/100 m (kg/100 Density Biomass Fish Mean 15 MPA 10 NON 5

0 La Jolla Catalina Anacapa ! Figure 1.6. Differences in mean biomass densities of fishes in the three trophic levels per site.

! ! ! ! ! ! ! ! ! !

! ! ! 53 !

!

! Figure 1.7. California sheephead (Semicossyphus pulcher) mean numerical and biomass density among sites and between protection status (MPA and Non-MPA). A = Juvenile, B = Female, C = Male. ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! !

! ! ! 54 !

Figure 1.8. Kelp bass (Paralabrax clathratus) mean numerical and biomass density among sites and between protection status (MPA and Non-MPA). A = < 7 cm, B = 7 - 25 cm, C = > 25 cm. !

! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! !

! ! ! 55 !

!

Figure 1.9. Mean numerical and biomass density of kelp rockfish (Sebastes atrovirens), black perch (Embiotoca jacksoni), and garibaldi (Hypsypops rubicundus) among sites and between protection status (MPA and Non-MPA).!

! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! !

! ! ! 56 !

!

! Figure 1.10. Mean numerical and biomass density of señorita (Oxyjulis californica), kelp perch (Brachyistius frenatus) and blacksmith (Chromis punctipinnis) among sites and between protection status (MPA and Non-MPA).

! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! !

! ! ! 57 !

! Figure 1.11. Mean numerical and biomass density of rock wrasse (Halichoeres semicinctus), opaleye (Girella nigricans) and halfmoon (Medialuna californiensis) among sites and between protection status (MPA and Non-MPA).!

! ! ! 58 !

4 3.5 3 2.5 2 1.5 Opaleye 1 Sheephead 0.5

CPUE (Total Harvest/Angler) CPUE (Total 0

Year ! Figure 1.12. Total fish harvested per number of anglers (CPUE) from the years 2003-2013 for opaleye (Girella nigricans) = green, and sheephead (Semicossyphus pulcher) = red. Data from Recfin.

! ! ! 59 !

Chapter 2

Stock biomass, numerical densities, population characteristics, and community

presence of giant sea bass (Stereolepis gigas) off Santa Catalina Island, California

Introduction

The giant sea bass (Stereolepis gigas) is the largest teleost to inhabit nearshore rocky reefs and kelp forests in the northeastern Pacific (Hawk and Allen 2014). Though previously taxonomically classified as a serranid, the giant sea bass is actually a , in the family Polyprionidae (Shane et al. 1996). Unlike most , they are a relatively shallow water species, inhabiting depths from 3 - 40 m. Their historical range is from Humboldt Bay, CA to Baja Mexico (Point Abreojos) and into the northern

Gulf of California. However, they are primarily found south of Point Conception.

Although, the giant sea bass is the largest member of the southern California rocky reef and kelp forest fish community, very little is known about its basic biology and life history (Allen and Andrews 2012). Giant sea bass have been documented to grow over

250 kg (Domeier 2001) and live up to 76 years old (Hawk and Allen 2014). However, there are reports of giant sea bass living as old as 90 -100 years and over 270 kg (Fitch and Lavenberg 1971), and even possibly reaching sizes of 360 kg as noted by author

Charles F. Holder at the turn of the twentieth century (Holder 1910). These early reports of giant sea bass size and age remain unverified.

Along with being a long-lived and slow growing species, with the exception of growing rapidly within the first year of life (Hawk and Allen 2014), they are also relatively late to mature. It is believed that giant sea bass mature between 11 - 13 years of

! ! ! 60 ! age (Fitch and Lavenberg 1971). However, there have been no studies explicitly confirming age at sexual maturity. To maintain their large body mass, giant sea bass feed on a wide variety of demersal and conspicuous rocky reef fishes as well as cephalopods and crustaceans. They have been documented to feed on rays, guitarfish, skates, flatfish, small sharks, barred sand bass, kelp bass, blacksmith, ocean whitefish, sargo, sheephead, octopus, lobster, cephalopods and squid (Domeier 2001, Love 2011). However, they are likely capable of feeding on nearly any species inhabiting nearshore rocky reefs and kelp forests off southern California, as they are the apex, tertiary megacarnivore of this system

(Cross and Allen 1993, Horn and Graham 2006).

Like many slow growing, late maturing, large bodied apex predators worldwide

(Pauly et al. 1998, Jackson et al. 2001, Dayton et al. 2002, Meyers and Worm 2003), the giant sea bass population has historically been depleted due to overfishing and has been rare off southern California (Domeier 2001, Pondella and Allen 2008). During most of the twentieth century, giant sea bass were highly sought after throughout the Southern

California Bight and Mexico by both commercial and recreational fishermen. During the early twentieth century, the commercial fishery which began using hand lines had switched to gill nets providing peak landings during the early 1930’s at over 114 mt before the crash of the commercial fishery off southern California in 1935 to under 10 mt

(Crooke 1992). The commercial fishery of giant sea bass taken from Mexican waters had greater landings and durability than those off southern California. Peaking in the early

1930’s at over 362 mt with a steady decrease throughout the 1960’s (Crooke 1992). The recreational fishery for giant sea bass off southern California peaked in 1963, and in

Mexico in 1973. That these peaks in recreational landings were after the crash of the

! ! ! 61 ! commercial fishery is due to the later development of the recreational fishery, and not the population size itself (Domeier 2001). By the mid 1970’s, several boats would target presumed spawning aggregations sites throughout the month of July off southern

California and Mexico, consistently landing high numbers (Crooke 1992) and in one case up to 255 fish in three days (Domeier 2001). Likewise, during the 1960’s and 70’s the practice of spearfishing grew in popularity. The gregarious and bold disposition of giant sea bass did not help this apex predator against the increasing numbers of spearfishers, as they were easy targets and landed at high frequencies (Fitch and Lavenberg 1971, Crooke

1992). This combination of various fishing pressures led to their near disappearance during the 1970’s (Pondella and Allen 2008), and by 1981 both southern California and

Mexico landings dropped below 5 mt (Crooke 1992, Domeier 2001). In 1981, a law was passed prohibiting the take of any giant sea bass off California, with the exception of two fish per vessel trip for commercial fishermen using gill or trammel nets, and the moratorium was put into effect in 1982. This law was later amended in 1988, allowing one incidental fish per trip off California waters. However, though this amendment limited the number able to be sold in California by commercial fishermen, it still allowed fishing via gill and trammel nets over nearshore rocky reefs and kelp forest habitat (Pondella and Allen 2008). These nearshore habitats that were targeted are those used by giant sea bass, especially during aggregation months from May

- October, and the incidental bycatch of giant sea bass was discarded at sea (Crooke

1992, Domeier 2001), or rumored to be shared among commercial fisherman. Due to concerns over the viability of the giant sea bass population off southern California, this

! ! ! 62 ! species was red listed by the International Union for Conservation of Nature (IUCN) as a critically endangered species (Cornish 2004).

It is rare to find evidence of a long-lived, slow growing, and late maturing species recovering after being strongly affected by overfishing (Hutchings 2000). However, after the gill net fishery was banned within three nautical miles of the mainland and one nautical mile of the islands with Proposition 132 in 1994, the population began to recover

(Pondella and Allen 1998). After being seldom seen in southern California from the

1970s -1990s (Domeier 2001), and not being observed in quarterly surveys by the

Vantuna Research Group off the Palos Verdes coast between 1974 - 2001, giant sea bass began to be observed in 2002, and have been seen to present day (Figure 2.1, Pondella and Allen 2008, + unpubl. data). Likewise, incidental commercial catch and CPUE from the Ocean Resource Enhancement Hatchery Program (OREHP) scientific gill net surveys showed a significant positive increase from 1995 - 2004, an increase that was not correlated to fluctuations in environmental factors (Pondella and Allen 2008). These findings allude to a nascent return of giant sea bass within the Southern California Bight.

Giant sea bass frequented yearly site-specific aggregations for presumed spawning purposes in the past, as fishermen targeted and depleted these areas during the

1970’s (Crooke 1992). Due to the elimination of previous spawning aggregations and the majority of the southern California giant sea bass population, modern day locations of aggregation sites are largely unknown. For conspicuous aggregation sites to reappear it is likely that population numbers would have to reach a certain abundance (Domeier 2001).

However, anecdotal reports by the recreational dive community today suggests that historical spawning aggregations are returning primarily off La Jolla, Santa Catalina

! ! ! 63 !

Island, and Anacapa Island, California. Surveying spawning aggregation sites allows for a unique opportunity to access a larger percentage of the reproductive population that would otherwise be spread over a greater geographic distribution (Johannes et al. 1999,

Whaylen et al. 2004, Heppell et al. 2012). For giant sea bass, the believed sex ratio is 1:1 male to female (Gaffney et al. 2007). Fecundity has not been estimated, but a single large female had weighing 21.3 kg containing an estimated 60 million eggs (Fitch and

Lavenberg 1971). Knowledge of an at-risk population’s size distribution of individuals within a spawning aggregation, fecundity, and sex ratios can provide a more informed estimate on the reproductive potential of a species. Furthermore, with information on a spawning aggregation biomass, through a length-weight relationship for the species and an estimate of total abundance, the spawning stock biomass of a species can be estimated

(Jennings et al. 1996).

My study uses a non-invasive method (Gingras et al. 1998, Colin et al. 2003,

Heppell et al. 2012) to provide the first population assessment of the endangered tertiary carnivore, the giant sea bass, of the rocky reefs and kelp forests off southern California at

Santa Catalina Island, CA. The objectives of my study were to 1) identify and document spawning aggregation sites and peak aggregation periods throughout the summer; 2) establish baseline mean spawning stock biomass, numerical densities, and length/biomass distribution frequencies; and 3) provide a general trophic biomass pyramid estimate of kelp forest fishes off Santa Catalina Island, CA during the summer season.

! ! ! 64 !

Materials and Methods

Study Sites

A total of eight sites were surveyed off Santa Catalina Island, CA during the summer of 2014 from 6/9/14 - 8/13/14 (Figure 2.2). To get a representation sample for the island, the eight sites were located at Johnson’s Rock (33°28'37.08” N lat.

118°35'22.57” W. long.), Little Geiger (33°27'27.62” N lat. 118°30'51.03” W. long.),

Empire Landing (33°25'59.96” N lat. 118°26'52.44” W. long.), between Twin Rocks and

Goat Harbor (Twin/Goat) (33°25'04.49” N lat. 118°23'38.24” W. long.), Italian Gardens

(33°24'39.92” N lat. 118°22'32.50” W. long.), Casino Point (33°20'58.68” N lat.

118°19'30.56” W. long.), The V’s (33°18'45.94” N lat. 118°22'11.38” W. long.), and

Little Harbor (33°23'08.10” N lat. 118°28'48.94” W. long.). Of the eight sites, four were chosen for being possible spawning aggregation sites for giant sea bass (Twin/Goat,

Italian Gardens, Casino Point, and The V’s). The remaining four sites (Johnson’s Rock,

Little Geiger, Empire Landing, and Little Harbor) were selected for their suitability as a possible spawning aggregation habitat off rocky reefs containing Macrocystis kelp forests to 24 m deep. Sites averaged 7 km apart and encompassed both the leeward and windward side of the island.

Survey Methods

Surveys at each site were conducted from 10:00 to 14:00. Surveys at each site consisted of five, three-minute, approximately 100 x 10 m SCUBA transects (1000 m2) using Sea Doo Vs Supercharged Plus Sea Scooter diver propulsion vehicles (DPVs).

DPVs were outfitted with two parallel waterproof length-calibrated lasers, set at 10.2 cm

! ! ! 65 ! apart, and a mounted GoPro Hero3 Black Edition video camera (Figure 2.3). Before surveys began, divers practiced and trained using the DPVs and timed fin kicks to cover

100 m in three minutes. The five timed transects per site were spaced at least 50 m apart and were comprised of depths from 27.5 m - 6 m to obtain an extensive survey of the reef habitat. Along each transect, giant sea bass occurring in front of divers and within the transect area were counted, and their size estimated to the nearest 25 cm. Transects were video recorded for photo identification of separate individuals. Upon the conclusion of each transect, size-surveys were done by video recording individuals observed at a 90° angle to the video camera with the parallel lasers spaced 10.2 cm apart (Gingras et al.

1998, Colin et al. 2003, Heppel et al. 2012). To reduce possible size estimation error, giant sea bass recorded during size surveys were measured within 2.5 - 3 m of the individual fish. Images of fish from the size-survey videos that displayed broadside and perpendicular to the video camera with visible measurement laser markings (Figure 2.4) were taken and length cm SL and TL were estimated using the software program ImageJ.

The lengths obtained from the size surveys were used to validate size estimations during the transects. Lengths were converted to biomass (kg/1000 m2) using the length-weight relationship for this species: kg = (0.0000001)*(SL mm)2.8173 (Williams et al. 2013). Age of sized individuals was back-calculated using the published von Bertalanffy growth

-0.044(t-0.345) curve (von Bertalanffy 1938) for giant sea bass: lt = 2026.2(1-e ) (Hawk and

Allen 2014). The eight sites were surveyed once every two weeks, for a total of four samples. The surveys were conducted during 6/9 - 6/24, 6/28 - 7/12, 7/15 - 8/2, and 8/4 -

8/13/2014.

! ! ! 66 !

Statistical Analyses

The biomass (kg/1000 m2) and numerical density (#/1000 m2) estimates of giant sea bass included many zeros and did not fit the assumptions of normality required for parametric analyses. Numerical and biomass densities of giant sea bass for Site (fixed factor: 8 levels) and Sampling Period (fixed factor: 4 levels) were compared using a

Kruskal-Wallis nonparametric analysis of variance (Kruskal and Wallis 1952) with individual transects used as samples. For length frequency and biomass distribution analysis, lengths (mm TL) were grouped into 100 mm increments to investigate the length and biomass frequency distributions of the surveyed giant sea bass population off

Santa Catalina Island.

In order to investigate the community presence of giant sea bass on the trophic structure of the kelp forest fishes off Santa Catalina Island, mean biomass of giant sea bass (Tertiary Carnivore) was generally compared to the mean biomass of conspicuous kelp forest fishes and their corresponding trophic levels from surveys conducted during the summer of 2013 (Herbivore/Omnivore, Primary Carnivore, and Secondary Carnivore) to provide a possible fish biomass pyramid model off Santa Catalina Island (kg/ha).

Results

Giant sea bass numerical densities (no. fish/1000 m2) were not statistically significant among the four sampling periods (H=1.48, P=0.69). Despite not being significant, total number of individuals observed during surveys (Figure 2.5) increased from the first sampling period until the third sampling period, and a decrease thereafter into the fourth sampling period (Table 2.1). Similar to numerical densities, spawning

! ! ! 67 ! stock biomass (kg/1000 m2) was not statistically different among the four sampling periods (H=0.53, P=0.91). However, the spawning stock biomass of giant sea bass

(Figure 2.6) was lowest within the first sampling period, and the highest and nearly equal biomass observed during the second and third periods, and a subsequent decrease in the fourth (Table 2.2).

Giant sea bass were observed at six of the eight sites around the island (Little

Geiger, Empire Landing, Twin/Goat, Italian Gardens, The V’s, and Little Harbor). No giant sea bass were observed at Johnson’s Rock or Casino Point. Numerical (Figure 2.7:

H=18.20, P=0.01) and biomass densities (Figure 2.8: H=19.31, P=0.007) significantly differed among sites. Aggregations were found at Twin/Goat, The V’s, and Little Harbor.

The site containing the largest number of giant sea bass was The V’s, where 23 were seen on the second sampling and 24 on the third sampling. Mean numerical densities at the

V’s was 2.6 ± 1.6 per 1000 m2 with a mean spawning stock biomass of 157.6 ± 99.3 kg/1000 m2. Little Harbor and Twin/Goat had the next highest numerical densities and spawning stock biomass. An aggregation of ten fish was observed on transects at Little

Harbor, while at Twin/Goat an aggregation of six was found. However, both sites had essentially the same mean numerical densities: Little Harbor (0.8 ± 0.5 per 1000 m2) and

Twin/Goat (0.8 ± 0.3 per 1000 m2). Although, mean biomass was higher at Twin/Goat

(81.2 ± 29.8 kg/1000 m2) than Little Harbor (34.0 ± 18.67 kg/1000m2) due to larger individuals aggregating at Twin/Goat. The remaining sites where giant sea bass were surveyed contained too few individuals to be considered aggregations. Only two individuals were recorded at Italian Gardens, and a solitary fish was observed at both

Little Geiger and Empire Landing.

! ! ! 68 !

Size of surveyed giant sea bass ranged from 0.9 - 2.3 m TL. According to the established age-length curve for giant sea bass (Hawk and Allen 2014), the smallest individual (0.9 m TL) was estimated to be 10 - 11 years old. The length frequencies of separate individuals showed the typical giant sea bass at Santa Catalina Island to be 1.2 -

1.3 m TL (Figure 2.9). However, most of the population’s biomass was found in individuals between 1.8 - 1.9 m TL (Figure 2.10). Based on image identification of separate individuals at each site and sampling period, a conservative estimate is that 45 separate individuals were observed from June 9 to August 13, 2014 off Santa Catalina

Island, CA. Overall mean biomass of giant sea bass off Santa Catalina Island during the summer was 36.3 kg/1000 m2. This biomass was converted to kg/ha to provide a possible biomass pyramid model for kelp forest fishes off Santa Catalina Island (Figure

2.11).

Discussion

My results suggest at least three giant sea bass aggregation sites occurred off

Santa Catalina Island, CA in 2014. These sites were located on both the leeward

(Twin/Goat) and windward (The V’s and Little Harbor) side of the island. Twin/Goat is the only of these three sites residing in a Marine Protected Area (MPA) as of 2012. The placement of the Long Point State Marine Reserve (SMR) was to protect the best-known aggregation area for giant sea bass off southern California from Long Point to Goat

Harbor (CA MLPA South Coast Project 2009), and is a popular site for recreational divers. However, though this site had a consistent aggregation during each of the four sampling periods, it did not possess the largest giant sea bass aggregation. The largest

! ! ! 69 ! spawning aggregation was found at the V’s with a total of 23 and 24 individuals occurring on transects during the second and third sampling period at 18 m depth. The individuals at the V’s were typically larger, 1.2 - 2.3 m TL. Throughout the summer human presence was minimal, as the V’s is located in a more remote area of the windward side of the island. However, commercial squid fishing vessels were observed in close proximity to the reef where the giant sea bass aggregation was observed

(personal obs.). The third aggregation site was located on the reefs just outside and west of Little Harbor, CA. The consistency of this aggregation varied. However, on the third and fourth sampling periods, 6 and 10 giant sea bass were observed respectively. Little

Harbor consisted primarily of smaller individuals (eight individuals under 1.2 m TL) compared to the other two aggregation sites at Twin/Goat and the V’s. The two sites where no giant sea bass were seen during surveys were Johnson’s Rock and, surprisingly,

Casino Point, as this location is generally believed to have resident giant sea bass.

Besides the two sites containing no giant sea bass, the Little Geiger and Empire Landing sites contained solitary individuals that were observed only once during the four sampling periods. Italian Gardens had a pair of giant sea bass that were likewise only observed during one sampling period.

Densities and biomass of giant sea bass did not differ among the four sampling periods from June 9th - August 13th. However, a trend was observed from nine individuals during the first sampling period to 36 during the third sampling period in mid-late July.

The decrease to 19 individuals during the fourth sampling period from early-mid August was largely due to the aggregation not being observed at the V’s. Also during the fourth sampling period, the number of giant sea bass increased at Little Harbor, and individuals

! ! ! 70 ! were observed at both Italian Gardens and Empire Landing for the first time during the summer. It is likely that the resident aggregation at the V’s moved and could be explained by surge and storms on the east windward side of the island caused by the tropical storm

Marie. The large variation in biomass and numerical densities during the four sampling periods can be largely attributed to the patchy distribution that resulted in the high number of transects where no giant sea bass were observed. Overall, the mean estimated

Santa Catalina Island biomass was 36.3 ± 13.6 kg/1000 m2 with a mean numerical density estimate of 0.6 ± 0.2 per 1000 m2.

If the giant sea bass population off southern California is indeed recovering, then there is likely to be a larger proportion of smaller and younger fish within the population, which could manifest as a positive skew in length frequencies of the population (Heppell et al. 2012). In the case of a spawning aggregation, smaller size classes represent newly mature fish entering the reproductive population. My results do not show a strong positive skew as the majority of reproductive giant sea bass off Santa Catalina Island were ~1.3 m TL and were estimated to be 18 - 19 years-old. However, smaller individuals were observed during surveys in Catalina spawning aggregations. These individuals were estimated to be 10 - 11 years old. Age at sexual maturity has not been adequately explored for giant sea bass, however, Fitch and Lavenberg (1971) estimated sexual maturity to begin between 11 and 13 years of age. My findings of young 10 - 11 year old giant sea bass within presumed spawning aggregations support Fitch and

Lavenberg’s estimates. These young fish are likely new recruits to the reproductive population off Santa Catalina Island that were born after the 1994 Proposition 132 gill net

! ! ! 71 ! ban in coastal waters. My results also suggest that these young individuals were able to find site-specific spawning aggregations that were likely once decimated by overfishing.

Although the majority of the reproductive population censused in the present study was made up of individuals 1.2 - 1.3 m in total length, these individuals did not account for the majority of the spawning stock biomass. The size class accounting for the majority of the biomass in the reproductive population was older (estimated to be 32 - 35 years) and larger (1.8 - 1.9 m TL) individuals. The total biomass distribution per size class was skewed toward the larger individuals due to a very large 2.3 m TL (1.9 m SL) individual that was estimated at 67 years old and 177.9 kg. However, this was not the largest giant sea bass measured during the summer of 2014. An individual that was measured during underwater observations, but that did not occur within a survey transect was seen at Twin/Goat and measured 2.7 m TL. This would be the largest giant sea bass ever measured, and supports early, unverified accounts of much older and larger giant sea bass (Holder 1910).

To investigate the community presence of the apex tertiary carnivore, mean biomass for giant sea bass (362.8 kg/ha), was generally compared to the mean biomass of the functional fish trophic levels of herbivore/omnivore (655.5 kg/ha), primary carnivore

(683.7 kg/ha), and secondary carnivore (645.3 kg/ha) from surveys (House unpub. dat) conducted off Santa Catalina Island during the summer of 2013 (Figure 2.11). Although, this biomass pyramid only represents a portion of the ecosystem, as primary producers and invertebrates were not included in analysis, the shape of the pyramid can provide insight into the fish community biomass structure off Santa Catalina Island. The biomass distribution among levels of the trophic pyramid shows a strong presence of tertiary and

! ! ! 72 ! secondary carnivores on reefs, displaying an approaching top-heavy fish biomass pyramid. A top-heavy or inverse trophic pyramid may at first seem improbable.

However, a top-heavy biomass pyramid indicates that the production pyramid must be bottom-heavy, with high levels of turnover rates at lower trophic levels, to support the large biomass present at higher levels (Odum 1959, Brown et al. 2004, Sandin et al.

2008). The presence of a large number of top predators resulting in a top-heavy community biomass pyramid is indicative of a pristine reef ecosystem, and found in other healthy reef communities worldwide (DeMartini et al. 2008, Sandin et al. 2008, Aburto-

Oropeza et al. 2011).

Altogether, this study provides evidence of the return of giant sea bass to the rocky reefs and kelp forests off Santa Catalina Island, and possibly the Southern

California Bight, by documenting new spawning aggregation sites, considerable spawning stock biomass, newly mature individuals recruiting to aggregations, and a large community presence at the island. Similar to Pondella and Allen (2008), fish survey data collected by the Channel Islands Research Program (CIRP) beginning in 1964 suggests a similar trend to the Palos Verdes coast in number of giant sea bass sightings off Santa

Catalina Island. From the CIRP surveys no giant sea bass were observed until the late

1990’s and early 2000’s and further increasing to the present day (J. Engle unpub. data).

However, although these data suggest a recent return of giant sea bass, historical accounts document fisherman consistently taking 70 - 100 giant sea bass from summer aggregations (Domeier 2001), suggesting that present day aggregation densities are still well under historical levels. The two aggregation sites containing the highest abundance

(the V’s) and younger individuals (Little Harbor) of the three spawning aggregation sites

! ! ! 73 ! are currently in unprotected areas where fishing is allowed. Schroeder and Love (2002) estimated how incidental catch and release mortality of giant sea bass could affect population sizes. Their estimates suggest that 100 giant sea bass, at a standard catch and release mortality rate of 20%, could be completely eradicated through incidental catch and release in just 16 years assuming no immigration. With the aggregation sizes found in my study, the largest being an aggregation of 24 fish, this incidental catch and release mortality rate could decimate the reproductive population off Santa Catalina Island during the summer spawning months. Seasonally established MPAs at identified giant sea bass spawning aggregation sites, similar to those set in place to protect Nassau grouper spawning aggregations in the Caribbean, could aid in reducing the incidental catch of giant sea bass near these areas. Furthermore, monitoring of aggregations after baseline estimates would allow temporal tracking of biomass, numerical densities, and population dynamics of giant sea bass off Santa Catalina Island and other sites within the Southern

California Bight. My study provides an effective way to survey these aggregations through the use of video and length calibrated lasers mounted on underwater DPVs enabling surveyors to cover a large area via SCUBA while obtaining size estimates and image identification of individuals. Further surveys of the kelp forest community is needed to document what potential influences a return of a long absent top predator may have to the dynamics of this ecosystem.

! ! ! 74 !

Table 2.1. Mean numerical densities (± SE) and total individuals observed per each of the four sampling periods from 6/9 - 8/13/2014.

Sampling Period Mean ± SE Total Individuals

6/9 - 6/24 0.2 ± 0.1 9

6/28 - 7/12 0.7 ± 0.6 26

7/15 - 8/2 0.9 ± 0.6 36

8/4 - 8/13 0.5 ± 0.3 19

Table 2.2. Mean biomass densities (± SE) and total individuals observed per each of the four sampling periods from 6/9 - 8/13/2014.

Sampling Period Mean ± SE Total

6/9 - 6/24 18.1 ± 8.9 723.7

6/28 - 7/12 48.7 ± 41.4 1947.3

7/15 - 8/2 47 ± 32.3 1919

8/4 - 8/13 30.4 ± 12.9 1216.2

! ! ! 75 !

!

1.0

0.8

0.6

0.4 # per survey protected gill net 0.2 status closure

0.0 1974 1976 1978 1980 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 2010 2012 2014

YEAR ! Figure 2.1.!Number of giant sea bass observed per quarterly survey conducted by the Vantuna Research Group from 1974 – 2014 off Ranchos Palos Verdes, Los Angeles County, CA. Data compiled from Pondella and Allen 2008 + unpublished data.!!!

! ! ! 76 !

! ! Figure 2.2. Location of the eight sites surveyed off Santa Catalina Island, CA from 6/9 - 8/13/2014.

! ! ! 77 !

! ! Figure 2.3. Image of a dive propulsion vehicle (DPV) with mounted length calibrated lasers and GoPro Hero 3 Black Edition video camera used for giant sea bass surveys.

! ! ! 78 !

! ! Figure 2.4. Image of a giant sea bass showing broadside length calibrated laser markings at 10.2 cm.

! ! ! 79 !

2 H = 1.48, P = 0.69 1.8 ) 2 1.6

1.4

1.2

1

0.8

0.6

0.4

0.2 Mean Numerical Density (#/1000 m

0 1 2 3 4 Sampling Period

Figure 2.5. Mean numerical densities (#/1000 m2) of giant sea bass per two-week sampling period.

! ! ! 80 !

120 ) 2 H= 0.53, P= 0.91 100

80

60

40

20 Mean Biomass Density (kg/1000 m 0 1 2 3 4 Sampling Period

Figure 2.6. Mean spawning stock biomass densities (kg/1000 m2) of giant sea bass per two-week sampling period.

! ! ! 81 !

Figure 2.7. Mean numerical densities (#/1000 m2) of giant sea bass per site.

Figure 2.8. Mean spawning stock biomass densities (kg/1000 m2) of giant sea bass per site. !

! ! ! 82 !

14 n = 45 12

10

8

6

4 Number of Individuals

2

0 0 500 1000 1500 2000 2500 3000 Length (mm)

Figure 2.9. Length frequencies (mm TL) of separate giant sea bass observed during survey transects.

! !

600 ) 2

500

400

300

200

100 Total Biomass Density (kg/1000 m Total 0 0 500 1000 1500 2000 2500 3000 Length (mm) ! Figure 2.10. Total biomass density (kg/1000 m2) per length (mm TL) distribution of giant sea bass observed during survey transects.

! ! ! 83 !

Figure 2.11.!Estimated mean trophic structure biomass density (kg/ha) of conspicuous kelp forest fishes during the summer season off Santa Catalina Island, CA. Functional trophic levels from bottom to top are Herbivore/Omnivore, Primary Carnivore, Secondary Carnivore, and Tertiary Carnivore.!

! ! ! 84 !

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