California State University, Northridge

Home , Aquarium of the Pacific, Giant sea bass, Oxyjulis

CALIFORNIA STATE UNIVERSITY, NORTHRIDGE

RECRUITMENT, GROWTH RATES, PLANKTONIC LARVAL DURATION, AND

BEHAVIOR OF THE YOUNG-OF-THE-YEAR OF GIANT SEA BASS,

STEREOLEPIS GIGAS, OFF SOUTHERN CALIFORNIA

A thesis submitted in partial fulfillment of the requirements

for the degree of Masters of Science in Biology

By: Stephanie A. Benseman

December 2017

The thesis of Stephanie A. Benseman is approved by:

______Michael P. Franklin, Ph.D. Date

______Mark A. Steele, Ph.D. Date

______Advisor: Larry G. Allen, Ph.D., Chair Date

California State University, Northridge

ACKNOWLEDGEMENTS

I would like to express my gratitude to the following people for making this research possible. To all my family, friends, and loved ones. To all my diver buddies who braved the cold to help me search for hours for a needle in a haystack. To my Biology girls (Leah, Dani, Beth, and Stacey) for always being there to support me. To Larry Allen for your inspirations, Mike Couffer for your dedication, Mike Franklin for the laughs, Richard Yan for your countless hours of otolith work, Chris Mirabal for your confidence in me, Milton Love for your support, CSUN for your generosity, and just because babies. Thank you all.

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DEDICATION

This work is dedicated to my family, who drive me crazy but I love and could not image being the person I am today without them.

TABLE OF CONTENTS

Signature Page ii

Acknowledgements iii

Dedication iv

Abstract v

Introduction 1

Methods 7

Results 13

Discussion 17

References 27

Appendix: Figures 34

Abstract

Recruitment, Growth Rates, Planktonic Larval Duration, and Behavior of the Young-of-the-Year

of Giant Sea Bass, Stereolepis gigas, off Southern California.

By: Stephanie A. Benseman

Master of Science in Biology

Little is known about the life history of Stereolepis gigas due to the over exploitation of their fishery in the early 1900’s, and depressed populations have prevented much research. A completed life history information on an ecologically, and once economically, important species such as the Giant Sea Bass (GSB) is critical for both the continued successful management of that fishery and a baseline for successful scientific studies. Therefore, the goals of this study include 1) determining distribution and general ecology for the YOY of S. gigas populations in the wild, 2) estimating growth rates, based on site aggregations in the wild, and otoliths analysis in the lab, and finally 3) confirming pelagic larval duration and the general temporal scale of their spawning period. One hundred and fifty SCUBA surveys were conducted to census waters with sandy benthos across southern California from 2013-2016. I documented early life ecology, including behaviors such as the “kelping” mimickery, cruising, & resting, as well as their active predator avoidance of burying and their diet of mysids based on field observations & confirmed through gut content analysis. I uncovered a specific distribution pattern spatially along the coast adjacent to underwater canyons, and temporally from July through February. This study was also able to establish a growth rate for the YOY, finally determined their planktonic larval duration

vi around 24 days, and the morphological color changes from black to orange. This study is the first of its kind to examine the YOY of this endangered species making it a key component to their life history, and a baseline for future work on S. gigas and similar long-lived and slow-growing species.

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Introduction

In most marine ecosystems worldwide, overfishing is obviously the most devastating cause of the removal of large predatory fishes from ecological communities. Knowledge of life history, such as age and growth, of such a target fish species is the starting point for any effective management frame work (King & MacFarlane 2003), and is crucial to the sustainability of that species. Specifically early developmental processes and recruitment patterns are crucial for completing the life history for any species, allowing us to make increasingly intelligent decisions about current fisheries management policies as well as future conservation efforts (Cailliet et al.

1996, Craig et al. 1999, Myers & Worm 2003). Basic life history information is also a staple in the scientific community and necessary before any hypothesis or conclusions can be made through experimentation.

Large brown algae such as the giant kelp, Macrocystis pyrifera, dominates in the southern California waters and creates an underwater forest which allows for multitude of species to thrive amongst the numerous niches created (Feder 1974, Graham 2004, Stephens

2006). Giant Sea Bass (GSB), Stereolepis gigas, were once extremely common in these southern

California kelp forests (Crooke 1992) and can be seen on occasion, just outside the kelp forest walls as the apex tertiary carnivore of this system (Cross & Allen 1993, Horn & Ferry-Graham

2006, House et al. 2016). GSB feed on a variety of kelp forest species from small crustaceans to larger fish species such as the California sheephead, kelp basses, perches, rockfish, small sharks, squid, sargo, ocean whitefish, octopus, spiny lobsters, crabs, snails, cephalopods, and other

1 macroinvertebrates (Eschmeyer et al. 1983, Domeier 2001, Horn & Ferry-Graham 2006, Love

2011).

In its adult form, the GSB is the largest near-shore teleost off the southern California coast (Pondella & Allen 2008, Hawk & Allen 2014) (Figure 1) found ranging from depth of 5-46 meters (Love 2011). GSB may look similar to a grouper in the family Serranidae, however they are actually a member of the small family of wreckfishes (Polyprionidae) (Shane et al. 1996).

They have a wide range found from Humboldt Bay to Baja California, but can be found in relatively high concentrations south of Point conception, from the Channel Islands south, and along the coast (Miller & Lea 1972, Love 2011, House et al. 2016).They have been historically recorded at over 250 kg (Domeier 2001) and estimated to live up to 76 years old (Hawk & Allen

2014), but recent studies have them reaching a length of almost 275 cm (9 ft.) and a weight 381 kg (839 lbs.) (House et al. 2016). This new information is closer to historical reports of fish living between 90-100 years and weighing over 270 kg (Fitch & Lavenberg 1971), and some even as large as 360 kg (Holder 1910).

Historically GSB have been targets for both recreational and commercial fishermen since the 1800’s (Pondella & Allen 2008) due to their massive size and the fact that they can also be observed in large semi-predictable aggregations (Sadovy de Mitcheson et al. 2008). These aggregations --believed to be spawning aggregations-- occur during the summer months (Crooke

1992, House et al. 2016) had often been targeted by fishermen, (Meyers & Worm 2003), landing relatively high catches (Crooke 1992), and even up to 255 fish in three days (Domeier 2001).

Targeting aggregations can lead to an “illusion of plenty”, usually ending in a population crash

(Sadovy & Domeier 2005, Sadovy de Mitcheson et al. 2008, Erisman et al. 2011). Targeting a

2 species can directly affect the genetic diversity, abundance, and size structure of that species

(Pauly et al. 1998, Bianchi et al. 2000, Hauser et al. 2002, Dayton et al. 2003), and the direct removal of these apex predators can cause drastic shifts in the ecosystem’s community diversity

(Jackson et al. 2001).

The once economically important fishery was soon devastated as their catch rates began to fall dramatically in the early 1900s. In fact, in 1934 the commercial catches were close to

114,000 kg until a rapid decline to less than 15,000 kg not more than two years later (Pondella &

Allen 2008) (Figure 2). In 1981 the California State Legislature created a moratorium prohibiting the recreational take and limiting commercial take of GSB, which came into effect in 1982. This essentially closed the commercial and recreational fisheries, except for a two-fish per trip bycatch allowance for commercial fishers, later amended to one in 1988. Additionally, Prop 132, known as the Marine Resources Protection Act, was passed in 1994 to close the gill and trammel net fisheries near shore and eventually the GSB were placed on the International Union for

Conservation of Nature red list as critically endangered species (Cornish et al. 2004). The GSB populations remain protected but depressed compared to historical values, however, the population does appear to be recovering slowly (Pondella & Allen 2008, House et al. 2016).

Estimations of their effective populations size remain around 500 (Chabot et al. 2015), they have been observed more frequently in the last 15 years (Pondella & Allen 2008), with juveniles continuously being caught and released in the recreational fisheries (Baldwin & Kaiser 2008). It is usually uncommon to find evidence of a slow growing long-lived tertiary carnivore species recovering after such heavy fishing pressure (House et al. 2016), however the quarterly surveys conducted by the Vantuna Research group of Occidental college, finally showed an increase in

3 the population after almost 30 years (Pondella & Allen 2008) (Figure 3). Therefore, S. gigas may be an excellent model of recovery for long lived slow growing fishes when the proper management is implemented.

The depressed populations in the wild have hindered the ability to complete numerous aspects of the life history of the GSB. They are believed to reach sexual maturity around 11-13 years (Fitch & Lavenberg 1971), but currently there have not been any studies that confirm this estimation. They are oviparous, broadcast spawners with planktonic eggs (Crooke 1992, M oser

1992), believed to spawn during the warmer water months (Peres & Klippel 2003) and recently there is evidence to suggest they do so in pairs (Hovey 2001, Clark unpublished data). The larvae remain in the plankton for an unknown period of time known as the planktonic larval duration

(PLD). After transformation from their larval body morphology, they recruit to near shore areas as young-of-the-year (YOY) (Love 2011). Very little is known about this species at this age, including their diet, growth rates, habitat preference and ecological interactions. These YOY

GSB are also known to undergo several morphological changes during the first few months after recruitment and are almost unrecognizable as a GSB (Moser 1992, Love 2011) (Figure 4).

Information on their planktonic larval duration can directly yield inferences into temporal scales of their spawning periods, which has only been speculated on so far. There is also no information on the growth rates in the first year of life. Fitch & Lavenberg (1971) reported that they are around 178 mm at one year, and double that by year 2, but details of their age estimation processes were not provided. Hawk and Allen (2014) completed a growth rate curve, but only had one juvenile individual who was already one year at the time of collection. Some

4 documentation is provided on their larval transformation in captivity around 12.4 mm (Shane et al. 1996), but there is still no data on their daily growth in the wild.

Quite opposite their large silvery adult counterparts, the YOY are very small, round, and perch like and are brightly colored, usually appearing as a bright orange/reddish fish with black and white spots, an enlarged black pelvic fin, and transparent pectoral, caudal, and anal fins

(Love 2011) (Figure 4). With the low visibility in these turbid areas, this unique size and shape could allow the GSB to blend in among the sand dollars, or simply disguise their fish body morphology, and perhaps why there have been so few sightings of the YOY. Using SCUBA transects I was able to document, the early life ecology of the YOY of GSB in the wild. To investigate this I examined the literature where juveniles have been documented previously.

Several factors were investigated such as common behaviors, feeding, predator/prey interactions, and the dramatic morphological changes that these YOY undergo after recruitment. Information on the recruitment, settlement sites and growth rates are all unknown pieces of the early life history. Growth rates can be determined by analyzing the otolith rings. Reading those rings, either annual or daily rings, can allow us to determine the age of a fish (Summerfelt & Hall

1987). Once daily growth rates are established a von Bertalanffy growth curve can be applied and then added to the one Hawk & Allen (2014) created to help confirm this as a long-lived slow growing species.

The goal of this study is to finally fill in the gaps in the early life history of the giant sea bass by 1) determining distribution and general ecology for the YOY of S. gigas populations in the wild, 2) estimating growth rates based otoliths analysis, and 3) confirming pelagic larval duration and general temporal scale of their spawning period. Allowing for baseline of

5 information for this elusive and endangered teleost species. My hypothesis states that the highest number of individuals will be at sites adjacent to an underwater canyon, when compared with a site not adjacent to an underwater canyon.

Methods

Sample Locations

Fourteen beaches in southern California were chosen as potential GSB settlement sites based on the availability of sandy beach bottoms, and is the habitat in which they had been previously observed. I searched through literature and online resources for photographs containing YOY GSB and the majority of them showed soft sandy bottom, or the occasional sand dollar bed which lead me to seek out locations with similar characteristics. All 14 sites were surveyed, but I chose the five sites with the highest probability of encountering these juvenile giants. Sites had to have soft sandy beach bottoms with little to no rock bottom nearby, and usually had some known sand dollar beds in the area. These sites include: Zuma Beach in Malibu

(34° 1'14.56"N, 118°49'54.01"W); Veterans Park in Redondo (33°50'10.42"N, 118°23'30.06"W);

Cabrillo Beach in San Pedro (33°42'27.73"N, 118°16'53.83"W); Big Corona Del Mar State

Beach in Newport Bay (33°35'29.70"N, 117°52'30.39"W); and La Jolla shores in San Diego

(32°51'19.63"N, 117°15'45.03"W). Big Corona was the adjusted to the Newport Beach Pier in

Newport (33°36'26.63"N, 117°55'54.80"W) after more investigation yielded higher abundances directly at the Newport canyon head. After another year of data collection I reduced the number of collection sites to only two sites as the main focus of our study: Veterans Park in Redondo

Beach, and the Newport Pier in Newport Beach, CA. At both of these locations there was a sizable underwater canyon at both of these sites. I then tested this by looking at other underwater canyons adjacent to sandy beaches and found the Newport Canyon on Balboa Island adjacent to

7 the Newport Pier. The first survey in January 2014 also yielded a YOY GSB, and confirmed the presence of them at the Newport Canyon.

SCUBA Transects

A total of 150 surveys were conducted from July 2013 through September 2016. SCUBA transects were conducted about every 1-3 weeks at rotating locations as weather and conditions allowed. Transects were run at various depths, ranging from 2-18 meters, with depths being haphazardly chosen for typically three 100 meter transects at a relatively “shallow”, “mid”, and

“deep” location when possible. During the underwater transects, a dive team --consisting of 2 divers-- swam 2 meters apart and recorded individuals seen within approximately 2 meters on each side of the diver. This helped maximize the effectiveness of the diver’s survey, as individuals can appear cryptic and be missed in low visibility. GoPro© video cameras were used to record each of SCUBA transects. These video records were later analyzed in the lab and used to estimate YOY populations, their distribution across microhabitats, and behaviors. Size estimation was taken with the use of a small ruler in the field and/or compared to known measurements recorded on the GoPro© camera and estimated later in lab. Seventy-five individuals whose location could be determined with the use of Google Earth and GPS were recorded to compare distance from the canyon heads. I also recorded the abundance of other epifaunal benthic organisms to compare similarities between the two locations. In addition to surveying the canyon adjacent sites, I also conducted transects to the north and south of each of my selected locations.

Collection of Specimens & Growth Rates

Thirty individuals were collected and sacrificed for growth rate analysis, under California

State Wildlife permit #13028 from December 2014 through December 2015. Individuals were obtained from Newport Beach (n=14) and Redondo Beach (n=16), with additional samples donated by the Southern California Marine Institute off the Palos Verde peninsula (n=2),

University of California, Santa Barbara collected off the coast of Santa Barbara (n=1), and from

Occidental College outside Los Angeles Harbor (n=1). The individuals obtained directly for this study were collected with the use of dip nets during SCUBA surveys, placed in plastic Ziploc® bags, and then placed on ice for euthanization. Each fish was weighed, measured, and photographed before an internal dissection was conducted to remove otoliths, intestines, gill rakers and any parasites. The Sagittal otoliths removed --as described in Craig et al. (1999)-- and then weighed, measured, and polished to observe otolith increments and estimate growth rates.

The otoliths were weighed to the nearest 0.001 gram, length measured from the longest axis parallel to the sulcus, and width measured from the widest point perpendicular to the sulcus. The thin otoliths were mounted with glue to glass slides then sanded down first with 3M® Wet/Dry

500 grit sandpaper, then 3M® Wet/Dry 1000 grit, and finally polished with Fandeli® 1500 grit sandpaper. Since the otoliths were in a variety of conditions based on how old the sample was, or time spent frozen, either the left or right otolith was read based on which yielded the clearest images. When available we compared both the left and right otolith to ensure consistency in reads between the two respected otoliths. After polishing they were oil immersed and photographed under an Olympus BX51 compound microscope, and the images analyzed using

ImageJ software. The use of the ImageJ software was used in place of traditional two person

9 otolith readings alternative method. A line was drawn from the center of the nucleus of each otolith to the outer most edge to ensure the accuracy of the ring count, then the line was then processed and plotted in a grayscale XY plot. By quantifying the number of distinct valleys in the grayscale plot, we were able to estimate age (in days) for each individual collected to establish a growth curve. These rates were compared to growth rates of YOY individuals in captivity including Monterey Bay Aquarium (n=1), Cabrillo Aquarium (n=1), and the Ocean

Institute (n=1) for validation. I then estimated PLD based on the presence of the first settlement check, or where the bands show a band, or the first obvious differentiation in width as is an accepted proxy of the PLD for juvenile fishes. This usually represents the time of recruitment out of the plankton which may indicate a drastic change in temperature, or a significant change in diet (Cordes & Allen 1997), and can be used to establish a recruitment period. I did add 4 days to each otolith count which accounts for the time spent hatching and yoke absorption, during the first few days before feeding as the bone form and before the rings are laid down, which is a standard for daily otolith counts (Cordes & Allen 1997).

Gut Content Analysis

The digestive tract of the individuals collected were removed and analyzed to establish diet. The gut contents were removed and weighed to the nearest 0.001 gram, as were the empty stomach casing, and then stored in glass vials in 70 % EtOH. The stomach contents were visually analyzed under a dissecting scope and any identifiable species recorded to the lowest taxonomical level possible. Unidentifiable material was stored for future analysis.

Behavioral Analysis

Behavior of these YOY is yet another unknown variable in the early life history of the

GSB therefore I quantified the most frequent behaviors observed. I quantified the behaviors into three main behaviors: kelping, cruising, and resting. The behaviors were recorded only one time for each individual during transects. I also documented 80 individuals on video with a GoPro©

Hero 3 for 1-4 minutes. Behaviors were then categorized into kelping, cruising, or resting. The first behavior that was the most common seen among the various size classes was the “kelping” behavior, as it appeared to be mimicking the small pieces of drift kelp attached to the benthos, mostly the giant kelp, Macroscystis pyrifera, which is common in these areas. This would entail the individual being stationed directly behind a piece of kelp similar in size to the individual, and swaying back and forth to the oncoming surge, each tine turning into the oncoming current and then back as it recedes. The next behavior was a cruising, where an individual would be cruising along just above the bottom in a slow but steady fashion. The fish would occasionally extend both the dorsal fin, and pelvic fin when the surge came back and forth. The fish would also extend its pelvic fin and drag it gently across the soft sandy bottom substrate as it swam. The next behavior was the resting behavior. This was where an individual would remain in the same spot or sand pocket, and “rest” relatively still. Usually this behavior was abandoned when approached, the individual would slowly abandon this resting behavior and start to drift away, very similar to the cruising behavior. On a rare occasion the individual would startle and then dart away quickly, but mostly the individual would casually drift away as if just a detached piece of algae, again mimicking the drift kelp commonly seen in these areas. The last behavior is the feeding. The individual would quickly turn its head, and suck in mysids one-by-one. This

11 behavior was excluded from the behavioral counts as they were observed sporadically feeding during all three previous behaviors. To establish prey types, I examined the YOY of GSB in the wild visually during transects, and confirmed with gut content analysis.

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Results

Morphology

A total of 150 transects were recorded over the three year period (Figure 5). Three distinct color morphs were observed; the black, the brown, and the orange. The black morph follows the PLD and is the smallest of the three morphs occurring just after the larval stage, ranging in size from 10.3-20.9 mm (Figure 6). The body is round with short snout, and a laterally compressed body with a faint lateral line runs the length of the body. There are also a number of white blotches surrounding around the face and a few scattered down the body, and the pectorals, anal, and rounded caudal fins are transparent, the dorsal fin fades from black to dark brown, and the enlarged pelvic fins are solid black. The brown morph is the slightly larger ranging from

23.4-32.6 mm (Figure 7) and is similar is shape to the black morph. The white blotches remain around the face and body, and black spots that vary in pattern can now been seen sporadically covering the body, with the background color changing to a dark brown in color. The pectorals, anal, and caudal fins remain transparent, as does the dorsal fin fading from black to dark brown, and the enlarged pelvic fins remains enlarged and a solid black. The largest of the three YOY morphs is the orange morph, ranging from 40.9-185.4 mm (Figure 8). It has a similar body shape to the other two previous morphs except it is increasingly larger in size as their bodies elongate, but maintaining that very round body shape. The body of the fish changes from the dark brown to a bright orange to reddish in color, with the white and black spots remaining. The transparent fins begin to fill in with a color matching the rest of the body, in a slow and systematic fashion.

Based on the amount of fin color filled in, one can almost determine with confidence at the total length of the fish, but further work in the exact amount has yet be determined.

Distribution

During our initial surveys we checked 14 beach sites along the coast, all with sandy beaches, and all with sand dollar beds which was previously believed to be a nursery areas. I surveyed at numerous times throughout the year and throughout the day during our study. I did not find any daily temporal patterns, in fact, these YOY appeared to be out during the day and even into the evening as reported by citizen scientist divers. They did however, show an obvious temporal pattern throughout the year with their peak abundances occurring in the late summer months from August through October. It did became apparent that the spatial distribution for the

YOY of GSB appears to be very patchy, or unevenly distributed. The apparent patchy distribution or “hotspots” for the YOY of GSB observed during transect surveys, have been almost exclusively at sandy beach areas adjacent to underwater canyons such as Redondo Beach

(#40/ha), Newport Beach (#33/ha), and La Jolla (#33/ha) in southern California (Figure 9). The similarities between these three sites include sandy beach areas with little vertical substrate, little to no algae cover, and the presence of an underwater canyon. The underwater canyon being the most distinguishing similarity between the sites. There are 14 other sandy beaches surveyed with little to no algae cover that did not yield any YOY of GSB present. Despite several other sites that were surveyed that fit the sandy beach with plenty of available habitat, we did not ever see another GSB in an area that was not adjacent to an underwater canyon. Also, despite the fact that

I conducted surveys throughout 2014, the YOY were only found from July through February

(Figure 9). The most noticeable pattern of distribution occurs along the depth contour line where the heads of underwater canyons ended abruptly at shallow sandy beach ecosystems (Figure 10).

Densities of YOY GSB were significantly higher (Kruskal-Wallis test (H (19,350) = 31.3; p =

0.037)) at the six locations nearest the heads of submarine canyons (Figure 11). In fact, when measured, the majority of the occurrences of YOY GSB were actually within 300 meters of the canyon heads (Figure 12). There was also a strong correlation between depth and body size, with the smaller individuals found shallower and the larger ones found deeper (p<0.001) (Figure 13).

Behaviors

The three most common behaviors observed include kelping, cruising, and resting. The behavior I defined as kelping is where the individual mimics kelp, cruising where the individual is just slowly moving just above the sand, and resting where the individual would remain in one place usually a small divet or sand pocket. I then ran a contingency analysis to test whether the frequencies of behaviors were similar across the three size morphs of YOY. The kelping behavior was shown to be the most common behavior we came across, especially in the larger orange morphs (X2 = 10.24, p=0.03) (Figure 14). There was also a burying behavior that was witnessed by one of the divers during a survey, where one individual was startled and turned sideways, undulated like a flatfish, and completely submerged itself under the soft sandy bottom substrate (Figure 15).

Diet

Based on the GoPro video I was able to analyze the feeding behaviors. On numerous occasions I witnessed large blooms of mysids, later identified as Opossum shrimp or mysid shrimp (Americamysis bahia). I was able to photograph and video record these feeding behaviors many times (Figure 16). To confirm the observations in the field, I used gut content analysis in the lab. I did confirm that these mysid were being consumed by the YOY, as well as a variety of organisms including Calanoid copepods, Crangonid shrimp, and Hisyeotuethis squid (Figure 17,

Table 1). Other organics were observed in the gut, but analysis of this material has yet to be conducted.

Growth rates

Otoliths that were photographed (Figure 18) was plotted in grayscale (Figure 19) to indicate daily growth increments. I counted each of the major valleys in the grayscale plot for a total number of days to calculate the average daily growth at 1.07 mm/day, with a standard deviation of 0.25 mm, then plotted this in Microsoft Excel to show the average growth rates

(Figure 21). Based on these growth rates I was able to calculate that the individuals collected ranged from 23 days to 79 days old. The planktonic larval duration was also calculated based on the presence of the first settlement check. I estimated the planktonic larval duration to be around

24.4 days on average with a standard deviation of 2.7 days.

Discussion

A robust amount of knowledge on the life history is needed to properly manage any heavily fished teleost species. This study provides an overview of the first year of life of the critically endangered giant sea bass off Southern California. Over 160 YOY of GSB have been observed with nonrandom patterns of their distribution and behaviors described for the first time, as well as finally providing information on their expedited growth rates during the first year of life.

During my surveys, I saw three distinct color pigmentations. Previous studies describe the larvae have been described as being heavily pigmented with both black and yellow chromatophores, having well developed fins, a rounded caudal fin, and undergoing several pigmentation phases (Shane et al.1996) but they do not go into specific details of these pigmentations. The orange/brick red pigmented morph has been seen and photographed the most, possibly because they the most conspicuous due to their bright color and larger size. The brown morph had been photographed on a few occasions but is smaller than the orange morph, less recognizable as a GSB. The black morph is even smaller still, and very cryptic as it spends a good deal of time cruising and at first glance appears as nothing but a spec drifting in the surge.

This is probably why the black morph has not been photographed or described in the wild before, coupled with the fact that both the black and brown color morph are short before they transition to this bright orange/red. The largest individual (178 mm) was still a brilliant orange-red color which varies slightly to the description in Shane et al. (1996), where they describe the individuals over 150 mm as being dusky with pale mottling. This is most likely due to the natural

17 variation among individuals, or their natural ability to change pigmentation. Adults have been reported loosing or expressing their spots while adolescent GSB (around 50 cm) have been video recorded undergoing dramatic color changes in a matter of seconds, so it is possible they have this ability during their first year. This is presumably an adaptation for predator avoidance, or possible in adult mating pairs as a form of communication. The fact that they undergo such dramatic color changes during their development is possibly a way of responding to their environment. The Macrocystis pyrifera that they mimic is a similar color --also a burnt orange/brown-- and the GSB may actually express their pigmentation based on their immediate surroundings as a form of crypsis. This strategy has already been shown successful in flatfishes, which have the ability to change color and pattern in response to the sediment to avoid detection

(Sumner 1911). The few in captivity they have been observed changing colors over time. On one occasion an orange morph collected from the wild actually retreated to this brownish reddish color, which was much darker than when it was collected. It should be noted that the environment that it was kept near (i.e. the algae species) was much darker than the M. pyrifera found in the wild. This ability to camouflage with their surroundings has potentially increased the successful recruitment of GSB in these areas. Especially since they can be quite difficult to locate in these low visibility sandy bottom environments.

The soft sandy benthos that surrounds these underwater canyon areas might be an successful nursery grounds for GSB since they are highly abundant in food (Dalh 1952), and relatively devoid of predators (McLachlan 1990), especially when compared to the crowded kelp forests and rocky reefs nearby. This soft benthos may also aid in their predator avoidance behaviors. On one occasion, an individual S. gigas was startled by a diver, turned sideways,

18 undulated like a flatfish and buried itself completely under the sediment (Couffer & Benseman

2015). Burying is a common behavior in many teleost species, but not in quite the same manner.

Senoritas, Oxyjulis californica, also bury themselves to avoid predation, but typically only at night and not indirect response to an approaching predator (Hobson 1968). Flatfish will also bury themselves to ambush their unsuspecting prey, but usually the head and/or opercula remains unburied (Gibson & Robb 1991), however this GSB was completely submerged under the sediment and only a small section of scales could be seen (Figure 15). This unique combination of adaptations could allow for them to hide in plain sight, but when necessary to take refuge in the sediments and wait for the predator to abandon their pursuit.

Figure 9 shows us the distribution along the southern Californian coast and the patchy distribution corresponds strongly with the presence of underwater canyons. This leads us to believe that it is the presence of the underwater canyon that, for some reason, yields an increased successful recruitment. The underwater canyon areas typically have an abundance of organisms present due to the deep sea internal waves causing upwelling from the canyon, providing cold nutrient rich waters increasing the primary productivity, leading to a higher abundance of organisms (Shea & Broenkow 1982, Pai et al. 2016). Since the nutrient rich waters can increase the mean biomass of the algal primary producers, primary consumers --the mysids-- and secondary consumers—which would include the GSB, at least at this young stage of their life.

Those deep sea internal waves that bring nutrients, also could be facilitating the recruitment of the young as the move from the plankton down to the ocean floor. This might cause a channeling effect that moves the GSB through and to the head of the canyon and the surrounding shallow sandy beach areas. This pattern of distribution near the underwater canyons is strengthened by

19 the fact that there have been thousands of divers and photographers who have dove countless sites along the California coast, yet, after all that time the obvious majority of the sightings occur at the underwater canyon locations. This could be due to the fact that the underwater canyons probably draw more divers than other beach sites, however there is little evidence to date to suggest large populations exists outside these underwater canyon areas. The strong correlation between the depth and body size of the GSB found in Figure 13, could be explained by the fact that the smaller individuals, who are more at risk for predation, utilize the shallower more turbulent areas as protection. And once they reach a certain size the larger morphs switch from the shallower areas to the kelping behavior possibly to reserve energy and allow for faster growth.

Another unknown factor of the early life history of the YOY of GSB is where they go when they leave the sandy beach areas, in which they inhabit following recruitment, and temporally when this occurs. The black morphs were observed as early as mid-July continuing until the first week of December, the brown morph from August through December, and the orange morphs from August until early February. Since none of the fish we observed during my study was larger than 80 mm, it would seem that they leave these areas, possibly to seek shelter from predators. The largest one donated from SCMI was collected on the R/V Yellowfin in an otter trawl off near a sandy beach area off Palos Verdes, CA. This 178 mm individual was collected in 28 meter waters, which could elude to the fact that these juveniles move deeper after they leave these recruitment areas. Further research should be done to help establish their distribution after these first few months.

The SCUBA transects I conducted also allowed me to get a unique opportunity to observe the YOY GSB in the wild and describe some of their natural ecology. The behaviors described in this paper are the most abundant seen in the wild during the field surveys. When we quantified each of the behaviors into table and the relative number of each of the major behavioral category based on the color morph of each individual (Figure 14). Based on my finding I determined that there were approximately 4 main behaviors that the YOY GSB exhibited: kelping, cruising, eating, and sitting. However, we only quantified the three most distinct behaviors, as the GSB were observed eating during all three of the other behaviors so we did not record the instances. The three behaviors including kelping, where the individual mimics kelp, cruising where the individual is just slowly moving just above the sand, and finally sitting where the individual would remain in one place usually a small divet or sand pocket.

Predation pressure can affect where individuals are found (Walters & Martell 2004), or select for predator avoidance behaviors (Seghers 1974, Magurran 1990, Pitcher & Parrish 1993).

The kelping behavior the GSB exhibit is probably a predator avoidance adaptation to the bare environment. The fact that kelping behavior was the most frequent behavior we came across, especially in the larger orange morphs which makes sense since they are the largest and most conspicuous of the three morphs. This allows the YOY of GSB to basically hide in plain sight and avoid predation during these vulnerable early developmental periods. Many fish species undergo similar examples of behavioral camoflauge in which they mimic algal species including kelpfish, seahorses, and pipefishes (Russell 1976, Sewell 2010). The color of the drift kelp found in these areas varies from browns to oranges, just like the YOY of GSB. This helps them blend into the bare sandy bottom surroundings and avoid predation. In fact, they are so successful at

2021 this strategy that on numerous occasions’ divers preforming surveys were almost on top of one these YOY and they did not see them right away. These nursery areas offer little physical protection from visual predators so the mimicry along with utilization of an available structure would provide the most protection.

The cruising behavior is when they appeared to be feeding the most although this was anecdotal observations and not quantified. They were observed on many occasions darting their head to one side and gape their mouth open, appearing to suck in the mysids in their blooms as they drifted along. After which they would continue swimming in a slow cruising manner, usually with the current and not appearing to exhibit much energy. They would extend both their dorsal and the enlarged pelvic fins in and out with the oncoming surge. I believe that this was the individual stabilizing themselves against the turbid waters, similar to a sail and a keel on a sailboat. This action, coupled with the gentle dragging of that enlarged pelvic fin against the substrate while cruising which could be to establish the distance between the fish and the benthos, could be beneficial since these areas experience such variable surge conditions.

Establishing where the bottoms is would prevent injury to the individual. Alternatively, the dragging of the pelvic fin might be used to maintain position by increasing friction with the sand substrate slowing movement in the surge. Sculpins have been known to exhibit this type of behavior in the intertidal to maintain their position with the incoming surge (Kane & Higham

2012). Further research needs to be conducted to explain why the pelvic fin is so greatly enlarged at this stage in their life, and not when once the GSB has grown into adult form.

Age and growth studies are just a part of the life history needed for proper management and conservation of a target fish species (Calliet et al. 1996). However no study to date has

22 looked at the growth rates in the first year of life in the wild. The use of daily growth rings on

YOY have been shown to be an accurate estimation of fish age (Itoh & Tsuji 1996, Szedlmayer

1998, Itoh et al. 2000, Neuman et al. 2001), but has been shown to have it disadvantages as it can be time consuming, expensive and can have a great deal of inconsistencies based on the readers experience (Cardinale et al. 2000). Therefore we used the grayscale plots in ImageJ instead of counting each one using only the human eye (Figure 19). The use of this technology is a newer way of reading otoliths that may yield accurate counts without the tediousness and repetition of multiple counters. These counts can be used to estimate growth rates and used to confirm the length-to-age relationship (von Bertalanffy 1938). This information can help us finally provide daily growth, planktonic larval duration, and spawning periods for S. gigas. This study was able to analyze these early life growth rates in more detail and provide a daily growth curve (Figure

20). A completed early life growth curve could also allow us to estimate the approximate age of a fish, without collecting, or harming the individual. Accurate conformation of these growth rates finally completes the missing piece of life history of this stunning organism.

Based on the planktonic larval duration estimation, we can infer about the temporal scale of their spawning periods based on the age of the fish and the date of collection. Since the GSB are very elusive little is known about their reproductive activities including if they are actually pair spawners (Clark unpublished data), and the actual temporal scale of spawning. Based on the age of the fish collected, we can back calculate the days after spawning, and then estimate the temporal scale of the spawning period. This is the first study to attempt to determine the PLD for this species, and the first to have actual quantifiable evidence of the duration of the spawning periods rather than previous anecdotal observations.

Our findings on the planktonic larval duration showed the population spawning from July through November, which disputes the information in Crooke 1992. It should be noted that this study was done during the 2014-2015 El Niño periods, which yielded unseasonably warm weather and water surface temperatures. An increase in the surface temperature would cause an increase in the metabolic rate, directly increasing the growth rate (Mosegaard et al. 1988). This might have been the reason that we saw recruitment well into November, since the waters remained warmer, and spawning might have occurred later in the year. If reproduction continued to occur later in the year, the temporal scale of the spawning period could exhibit a longer duration during an El Niño year, and might increase the year class strengths. Some of the size classes present in the aggregations are estimated to coincide with the historic cycles of El Niño.

This could be further evidence of the increased recruitment success of the individuals from those

El Niño years, which has already been anecdotally described as showing a strong recruitment success in El Niño years (Love 2011). This warmer temperature theory is a possible explanation for the increase success in the recruitment of the YOY, however warmer temperature are also usually negatively correlated with the abundance of food (Wellington & Victor 1992), which is another important factor in the length of the larval duration (Riley 1966, Houde 1977, Houde &

Schekter 1980, Hovenkamp 1990). Future studies need to be conducted to further investigate the factors affecting the duration and variability of the PLD for S. gigas. The possibility of a longer spawning season was supported recently with evidence from captive Giant Sea Bass in the Long

Beach Aquarium of the Pacific by head aquarist Nicky Leier, who collected samples of larval

Giant Sea Bass from the main tank into December 2016 (pers. comm.). Leier also successfully raised a larva into a fully transformed juvenile in approximately 21 days under laboratory

24 conditions. This rearing period corresponds well with my findings of for the PLD, as well as the extended spawning periods. Comparing growth rates seen in the field to ones seen in the lab can enhance our overall knowledge and understanding of these species, allowing us to more successfully manage their fishery.

The discovery of the temporal scale of the PLD is vital for inferences on their spawning periods, without having to be present in the water to actually confirm mating, since this can be ineffective, inefficient, and time consuming. Based on the age of these individuals we can estimate the duration of the mating periods, which until now have only been speculated on through aggregation sightings. Clark et al. (unpublished data), discovered the mating happens mostly in the summer months, but based on the otolith reads I can determine that there is some degree of spawning happening later that previously believed. Further studies should be conducted on the effects of El Niño on spawning periods.

Besides population estimates, other early life history information such as spawning periods and distribution, management agencies need to have detailed information to properly assess current and future regulations. These estimates can help inform policy makers about the predicted populations and therefore if the current by catch allowance is sustainable. Direct effects of fishing can alter community compositions that can be detected but the indirect effects of fishing on marine communities can take decades to determine (Daan et al. 2005, Babcock

2010, Estes et al. 2011). One successful tool in fisheries management is the implementation of

Marine Protected Reserves (MPA), or no take zones. These MPAs can increase the fish stock of target species and allow populations to recover. However, these MPAs usually focus on the kelp forest or rocky reef species to maximize the number of species protected, however they do not

2425 typically target species that rely on sandy bottom areas as nursery grounds such as the GSB. If nursery areas are limited, or endangered by development, regeneration of future populations may suffer greater than a species that has a very broad recruitment pattern. Since the GSB YOY rely on these sandy beach areas adjacent to underwater canyons, then we may need to reassess our influence on these areas. Specifically, human influences must be minimized in these areas. For example, in Redondo Beach sediment from the head of the canyon head has been scooped up to replenish the beaches in these areas (Mike Couffer pers. comm.). These re-sanding events may have deleterious effects on the recruitment success of the YOY of GSB, and should be investigated. The relatively low numbers in these areas might also be an insight into future populations since counts even at the peak season show that there may only be hundreds of GSB successfully recruiting to these areas each year, instead of millions or even thousands like other broadcast spawners. Now that the nursery grounds are identified, protecting these areas may a key component to aid in the replenishment of future GSB populations.

Early developmental processes and recruitment patterns are crucial for completing the life history for any species, allowing us to make increasingly intelligent decisions about current fisheries management policies as well as future conservation efforts. T his study is the first of its kind to examine the YOY of this endangered species making it a key component to their life history. For the first time, this study was able to determine habitat & distribution, recorded & categorized behaviors, confirmed diet, calculated a PLD, inferred spawning periods, created a growth curve of the young-of-the-year of giant sea bass, Stereolepis gigas, off southern

California waters finally creating a baseline of information for a critically endangered & understudied species.

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Appendix: Figures

Figure 1. Pictures shows an adult giant sea bass, (Stereolepis gigas). Photo credit: Mike Couffer.

Figure 2. This picture shows the commercial catch rates of Stereolepis gigas from 1928 to 2006. The arrows represent the Moratorium in 1982, and Prop 132 Gill net Ban of 1994. (Allen 2017).

Figure 3. Graph represents the number of Stereolepis gigas seen during quarterly surveys off Palos Verdes from 1974-2014 (taken from Pondella and Allen 2008). The arrows represent the Moratorium in 1982, and Prop 132 Gill net Ban of 1994.

Figure 4. Picture showing a juvenile Giant Sea Bass over a sandy bottom off the southern California coast. Photo Credit: Mike Couffer.

Figure 5. Picture shows a standard transect off Redondo Beach, CA, with a young-of-the-year of Stereolepis gigas in the foreground. The S. gigas is approximately 50 mm, at 8.2 meters depth. Photo credit: Mike Couffer.

Figure 6. Photograph of a young-of-the-year of giant sea bass, Stereolepis gigas, in the black morph. The second dorsal, pectoral, caudal, and anal fins are all transparent. The body is all black with only the white blotches shown, which occur in a haphazard pattern, which varies between individuals. Black morphs total length ranged from 10-21 mm. Photo credit: Mike Couffer.

Figure 7. Photograph of a young-of-the-year of giant sea bass, Stereolepis gigas, showing the brown morph. The second dorsal, caudal, and anal fins are all transparent, and the enlarged pelvic fin remains a solid black (shown in a tucked position). The body is a dark brown color, the white blotches remain, and black spots begin to appear also in a haphazard pattern down their body. The brown morphs ranged in size from 23-33 mm. Photo credit: Mike Couffer.

Figure 8. Photograph of a young-of-the-year of giant sea bass, Stereolepis gigas, showing the orange morph. The body is round and now a bright orange/red color, and the white blotches and black spots remain. The enlarged pelvic fin remains a solid black. The pigmentation of the transparent fins begins to slowly fill in during this stage. The orange morphs ranged in size from 41-186 mm.

Figure 9. Distribution map of young-of-the-year GSB observed off southern California. The bars represent the densities of individuals seen (# per/hectare). Circles represents sites surveyed which had zero sightings. The line represents the depth contour line where deep water canyons meet shallow sandy beach areas, which corresponds to the highest GSB abundances.

Figure 10. Histogram representing the average abundance of young-of-the-year of Stereolepis gigas found in surveys conducted form 2013-2015. The obvious majority of the distribution occurring in the late summer- fall months of August through November.

H = 31.3 df = 19, 350 p = 0.037*

2 Figure 11. The mean density (number of individuals/m + 1 std) by location of the GSB from north to south in the southern California Bight.

Figure 12. Histogram representing the total abundances of individual GSB seen, and their estimated distance from the canyon head.

6 Depth (m)

4 y = 0.0389x + 4.9524 R² = 0.1565 p < 0.001 2

0 0 10 20 30 40 50 60 70 80 90 Total Length (mm)

Figure 13. Plot of the total length (in mm) of the individuals observed by depth (m). There is a strong correlations between the size of the individual and depth, with smaller individuals found shallower and larger individuals deeper (p<0.001).

Frequencies

Figure 14. Histogram representing the total abundances of individual young-of-the-year of Stereolepis gigas seen, and the behavior at the time of sighting. Black bars represents the smaller black morphs, the brown bar represent the medium brown morphs, and the orange bars represent the larger orange juveniles. The three behaviors including kelping, where the individual mimics kelp, cruising where the individual is just slowly moving just above the sand, and finally resting where the individual would remain relatively stationary. The kelping behavior was significantly more common in the larger orange morphs from a contingency table analysis with three sizes by three behaviors (X2 = 10.24, p<0.05).

Figure 15. Photograph showing a young-of-the-year of Stereolepis gigas who buried itself in Redondo Beach, CA. Taken from Couffer & Benseman (2015).

Figure 16. Picture shows a young-of-the-year of Stereolepis gigas feeding on a mysid. The mouth in extended for feeding typical of gape and suck predator.

Herb

(A)

(B) (C

Figure 17. Picture of the gut content analysis of one of a young-of-the-year of Stereolepis gigas (A). The gut contained both a Crangonid shrimp (B), and a Hisyeotuethis squid (C) weighing 2.64 grams.

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Individual Stomach Contents Content Stomach weight # weights (empty) 1 1 Crangonid Shrimp (1.3 cm) + digested 0.831 g 0.67 g material 2 2 copepods 0.131 g 0.145 g 3 N/A N/A N/A 4 Empty N/A 0.045 g 5 1 Annelid worm, 2 mysids 0.015 g 0.021 g 6 1 Copepod 0.011 g 0.016 g 7 Empty N/A 0.036 g 8 N/A N/A N/A 9 Empty N/A 0.271 g 10 12 Mysids 0.056 g 0.060 g 11 1 mysid + digested material 0.262 g 0.278 g 12 1 Isopod 0.037 g 0.04 g 13 Empty N/A 0.047 g 14 Empty N/A 0.039 g 15 Digested material 0.010 g 0.053 g 16 Empty N/A 0.111 g 17 1 mysid + digested material 0.241 g 0.28 g 18 Empty N/A 0.009 g 19 1 mysid 0.019 g 0.022 g 20 Empty N/A 0.012 g 21 Empty N/A 0.019 g 22 Empty N/A 0.029 g 23 Empty N/A 0.011 g 24 Empty N/A 0.048 g 25 Empty N/A 0.029 g 26 1 Hisyeotuethus squid, and 1 Crangonid 2.640 g 1.98 g shrimp 27 2 Mysids + Digested material 0.055 g 0.06 g 28 1 Copepod + Digested material 0.041 g 0.039 g 29 Empty N/A 0.001 g 30 Empty N/A 0.007 g 31 Empty N/A 0.009 g 32 Empty N/A 0.005 g 33 6 Copepods 0.019 g 0.027 g 34 Empty N/A 0.008 g 35 1 mysid 0.011 g 0.014 g

Table 1. Table representing the gut contents of 35 individuals obtained including contents, dry weights, and empty stomach weighs (in grams).

A. B. Figure 18 (A & B). Picture of the rings of the otolith of a young-of-the-year of Stereolepis gigas, taken from a compound scope at a magnification of 100X.

Figure 19. A grayscale plot of an otolith removed from a young-of-the-year of Stereolepis gigas in ImageJ software. The peaks and valleys represent the color change of the ring of the otolith.

Growth Curve of YOY of S. gigas 100 90 y = 20.834e0.0161x R² = 0.7921 80 70 60 50 40

Total Length TotalLength (mm) 30 20 10 0 0 10 20 30 40 50 60 70 80 90 Age (Days)

Figure 20. Observed total length (TL) at age for Stereolepis gigas (N=28) taken from Southern California. Line is exponential curve best fit line.

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