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Peete kN) CALIFORNIA ACADEMY OF SCIENCES

Number 3

BULLETIN

Volume 110

December 2011

BCAS-A110(3) 141-192 (2011)

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Bull. Southern California Acad. Sci.
110(3), 2011, pp. 141-151
© Southern California Academy of Sciences, 2011

Discordant Phylogeographic and Biogeographic Breaks in
California Halibut

Matthew T. Craig,'* F. Joel Fodrie,* Larry G. Allen,* Laura A. Chartier,* and
Robert J. Toonen*

‘University of Puerto Rico, Mayagtiez, P.O. Box 9000, Mayagtiez, PR 006851, USA
Institute of Marine Sciences and Department of Marine Sciences, University of North
Carolina at Chapel Hill, 3431 Arendell Street, Morehead City, NC 28557, USA
>California State University, Northridge, 18111 Nordhoff St., Northridge, CA 91330 USA
*Hawai‘i Institute of Marine Biology, School of Ocean & Earth Sciences &
Technology, P.O. 1346, Kdn‘eohe, HI 96744, USA

Abstract.—The range of the California Halibut, Paralichthys californicus, spans
three biogeographic provinces along the coastline of Alto (United States) and Baja
(Mexico) California. To assess population genetic structure of the California
Halibut, we analyzed mitochondrial cytochrome 5 sequences from 375 individuals
across a large portion of its native range. Nucleotide diversity was consistently low
among sampling sites (t = 0.0026 + 0.0017), while haplotype diversity was
consistently high (h = 0.77 + 0.024). We found that California Halibut were
genetically homogeneous across sampled sites with an overall ®,, = 0.0030 (p =
0.22). We saw no evidence of genetic discontinuities at two previously recognized
marine phylogeographic breaks in the Los Angeles region or across the California
Transition Zone at Point Conception. We conclude that California Halibut are
genetically homogeneous and experience substantial gene flow, at least over
evolutionary time scales.

INTRODUCTION

The nearshore marine environment of coastal California (USA) has long been a
playground for biogeographers owing to its dynamic composition of marine organisms
that has undergone dramatic shifts during the past five decades or so, particularly among
marine fishes (Horn, et al., 2006). While southern California’s marine ichthyofauna was
once thought to share many elements of the cool water ““Oregonian’”’ faunal assemblage, a
persistent warming trend since the early 1980s precipitated a change in southern
California’s marine ichthyofauna to a more temperate, sub-tropical fauna with estab-
lished communities whose biogeographic affinities lie with faunal assemblages further
south along the Pacific Coast (reviewed in Lea and Rosenblatt, 2000).

While the biogeographic history of southern California is dynamic, one geographic
feature has consistently stood out as a potential dividing point between two distinct
faunal provinces at Point Conception, a prominent headland that marks the beginning of
the “California Bight” and the California Transition Zone (CTZ; Figure | [Valentine.,
1966]). However, as detailed distributional data on California’s marine fishes emerged,
this biogeographic “‘break”’ appeared to be “leaky”, and is now regarded as more of a
gradual transition zone (Horn, et al, 2006).

* Corresponding author: matthewcraig4@gmail.com

141

142 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

%

Half Moon Bay 0}

[N=31] ‘é
¢

—

Santa Barbara ©
[N= 11]

Agua Hedionda [N = 14]
San Dieguito [N = 27]

Mission Bay|Nn = 38]

San Diego |N = 30]

San Diego Bay [N =35]

30° Tijuana Estuary [N = 34]

Oceanside Harbor |[N = a

Ensenada/Todos Santos
[N = 28]

Punta Bandao
[N = 35]

Fig. 1. Paralichthys californicus. Sampling locations and sample sizes for 375 individuals along the
California coastline.

With the advent of the phylogeographic revolution in the late 1990’s, many papers were
written discussing the theoretical expectation of concordance between biogeographic
boundaries and intra-specific, phylogeographical breaks (1.e., the concordance rule; see
examples in Avise, 2000)). It was recognized that the genetic structure of a population
may be influenced by a number of factors, including biogeographic barriers to dispersal
(Bernardi, 2000; Bernardi, 2005; Blanchette and Gaines, 2007; Burton, 1998; Dawson,
et al., 2001), yet one assumption of the concordance rule that was not immediately
recognized was that for a biogeographic boundary to function simultaneously as a

PHYLOGEOGRAPHY OF CALIFORNIA HALIBUT 143

phylogeographic boundary, the expectation would be that sister species would exist on
either side of the boundary due to the persistence of a common causal property of the
geographic area restricting gene flow over evolutionary time scales. At that time, data
from most studies highlighted the geographically similar locations of these phylogeo-
graphic and biogeographic breaks, particularly in the southeastern United States among
marine organisms (e.g., Cape Canaveral, Florida). In coastal California, however, a
pattern soon emerged in which geographical separations of marine faunal assemblages
did not correlate with the geographic locations of phylogeographic breaks within species,
and the generality of the “concordance rule”’ was challenged (e.g., Burton, 1998)

Further complicating the generality of California’s hypothesized barrier was the
realization that for some marine organisms, particularly those tied to aquatic inland
habitats (i.e., estuaries and marshes), or with low dispersal potential (e.g., live-bearing
fishes) a phylogeographic break was noted farther south in the Los Angeles region (LAR;
Bernardi, 2000; Dawson, 2001; Dawson, et a/., 2002). Few studies to date have tested the
functionality of either the LAR or CTZ in marine species with greater dispersal potential
or vagility as adults, but notable examples include studies of rockfishes of the fam
Scorpaenidae (e.g., Hyde and Vetter, 2007; Hyde and Vetter, 2009).

The California Halibut (Paralichthys californicus Ayers 1859) is an ecologically and
economically important flatfish species distributed from Washington State to southern
Baja California with unsubstantiated records from the Gulf of California (R. N. Lea and
R. Rosenblatt, pers. comm.). This range traverses the CTZ and the LAR. Contrary to
early predictions, the California Halibut is known to utilize both embayments/estuaries
and open coastal habitats for all stages of its life cycle (Fodrie, et al, 2009). It is also a
broadcast spawner with pelagic eggs and larvae. These characters provide an opportunity
to examine the efficacy of the LAR and CTZ “barriers” for a species that is not restricted
to aquatic inland habitats and that has higher dispersal potential than previous examples.
Herein, we use mtDNA sequence data from the cytochrome b gene to examine the genetic
architecture of California Halibut. We place these results within the context of recent and
past genetic studies and show that California halibut provide yet another vexing example
of the discordance between biogeographic and phylogeographic breaks in coastal
California.

MATERIALS AND METHODS

Tissue samples from P. californicus were collected from 14 sites along the coast of
California and Mexico throughout the entire effective range of the species (1.e.,
individuals are exceedingly rare North of San Francisco, California; Fig. 1). The
northernmost site sampled was Half Moon Bay, while the southernmost site was Bahia
Magdelena, Baja California Sur, Mexico. Samples were preserved in 100% ethyl alcohol
and stored at room temperature.

Total genomic DNA was extracted using the DNeasy kit (Qiagen, Inc.) following
manufacturer’s protocol. Polymerase chain reaction (PCR) was initially performed using
the primers (5’-GTGACTTGAAAAACCACCGTTG-3’) and (5’-AATAGGAAGTAT-
CATTCGGGTTTGATG-3’), designed by Song er al. (1998) and Taberlet er al. (1992),
respectively. Results were inconsistent with these primers, thus the species specific primers
Para-CBF2 (5'- CTG ATG AAA CTT TGG CTC CCT -3’) and Para-CBR2 (5'- TAT
GGG TGG AAG GGG ACT TTG TC - 3’) were designed which consistently amplified
approximately 700 base pairs of the mitochondrial cytochrome b region. Twenty-five ul
PCR reactions were prepared using BioMixRed (Bioline, USA) following manufacturer’s

144 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

rs Half Moon Bay
Ese Santa Barbara
(aie Los Angeles
(es Oceanside Harbor
____| Agua Hedionda
aaa) San Dieguito
er Mission Bay
eo | San Diego
©) GE San Diego Bay
et Tijuana Estuary
(eel Ensenada/Todos Santos
ears) Punta Banda
GM Bahia Asuncion

(sl Bahia Magdelena

Fig. 2. Paralichthys californicus. Statistical parsimony network for 375 cytochrome b sequences. Small
squares specify missing haplotypes; colors signify collection location. Circles are proportional to the
number of individuals containing the haplotype with the smallest circles representing one individual.

protocols with the addition of 0.2 uM of each primer, and 10-100 ng DNA template.
PCR amplifications were performed using the following cycling protocol: preliminary
denaturing step for 2 min at 94°C, followed by 35 cycles of 30s at 94°C, 45 s at 53°C, 45 s
at 72°C, and a final continuous hold at 15 °C. Exonuclease I and shrimp alkaline
phosphatase (ExoSAP) were used to eliminate non-incorporated oligonucleotide primers
and excess dNTPs in successful amplification products. Direct sequencing of
amplification products was performed in both directions using the PCR primers at the
Hawa11 Institute of Marine Biology EPSCOR Sequencing Core Facility on an ABI3130
genetic analyzer.

Sequences were trimmed to a common length and collapsed to single stranded
sequences using SEQUENCHER V. 4.1 (Sequencher® sequence analysis software, Gene Codes
Corporation, Ann Arbor, MI USA), and aligned using CLusTaL X (Larkin, et al., 2007)
with default settings. A statistical parsimony network of mtDNA haplotypes was created
for P. californicus using the program tcs (Clement, et a/., 2000) under default settings
(Fig. 2.). Hierarchical population structure was evaluated based on estimates of O, for
both the entire dataset and in a pairwise manner using ARLEQUIN (v. 3.11; Excoffier and
Lisher, 2010). Values of haplotype and nucleotide diversity were obtained through
ARLEQUIN. Departure from equilibrium conditions was assessed using Tajima’s D and
Fu’s F, (Table 2) as well as with mismatch distributions as calculated in ARLEQUIN. When

PHYLOGEOGRAPHY OF CALIFORNIA HALIBUT 145

a unimodal distribution was found, we followed Li (1977) and Rogers and Harpending
(1992), and fitted estimates of s, hg and h; to observed mismatch distributions to
determine effective population sizes and time to coalescence. Coalescence analysis
requires an estimate of generation time and rate of DNA evolution. Empirical values are
not available for California halibut, so a range of values were used that bracket rates used
in previous studies (Bowen, ef a/., 2001). Mutation rates of 0.1-10% per million years
within lineages and generation times of 1.5—10 yr were used.

A coalescence-based analysis of historical migration rates was performed using the
program MiaratE v. 3.1.6 (Beerli, 2009) to assess relative migration rates across the two
hypothesized “‘barriers’” (CTZ and LAR). The data were grouped into three pseudo-
populations: North of Pt. Conception, Santa Barbara to the Tiyuana Estuary, and Todos
Santos to Bahia Magdalena. The Maximum Likelihood method was used under Markov
Chain Monte Carlo (MCMC) search strategy of MIGRATE using default settings to
estimate starting parameters for subsequent runs. A second MIGRATE analysis was
performed using the estimates of © (N,. y) and M (m/n) from the first “run” as starting
parameters. Estimates of © and M were within one order of magnitude and were thus
accepted as good values following program documentation. Geographic distance between
these pseudo-populations was not included in the analysis given the broad distances
between individual sampling localities of the constituent members.

RESULTS

Overall, 681 base pair sequences of mtDNA cytochrome b were resolved for 375
individuals of P. californicus. Unique haplotypes were deposited in GenBank (JQ182307—
JQ182398). Overall, there were 92 unique haplotypes found throughout all samples. San
Diego Bay exhibited the highest number of unique haplotypes (N = 9) while Oceanside
Harbor exhibited the least (N = 2). Overall nucleotide diversity was m = 0.0026 + 0.0017
and overall haplotype diversity was h = 0.77 + 0.024 (Table 1).

The statistical parsimony network showed a pattern consistent with the eee that
California Halibut represent a single, genetically homogeneous population with evenly
dispersed haplotypes throughout the sampled range (Fig. 2). The fixation index (®,,) for
the entire dataset was ®,, = 0.0030 (p = 0.22). In pairwise comparisons of the population,
5 out of 13 comparisons were statistically significant; however this significance was not
apparent following Bonferroni correction for multiple comparisons (Table 2). Significant
paiwise comparisons consistently included the open coast San Diego site. Tajima’s D and
Fu’s F, were negative and significant for nearly all sample locations and for the entire
dataset (Table 1). Harpending’s Ragedness index was R = 0.01 (P = 0.98; Fig 3).

Estimates of T, Op and ©, are presented in Table 3. Estimated coalescence times did
not vary depending on generation time (1.5—l0yr) or mutation rate (0.1-10% per my).
Coalescence times did vary, however, based on the mean, lower and upper limits of the
estimated value of T (Table 3). The MiGraTe analysis indicated substantial effective
migration among the three regions in a general North to South direction but not from
South to North (Table 4).

DISCUSSION AND CONLCUSIONS

Point Conception has been a well-studied area due to its physical attributes and their
implications for dispersal of marine organisms. Waters north of this region are
characterized by strong, consistent upwelling and generally cooler surface waters, while
those south of this region have weak, seasonal upwelling with relatively warmer surface

146 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 1. Paralichthys californicus. Molecular diversity indices for 375 cytochrome b haplotypes. A
single asterisk (*) indicates statistical significance at <0.05, double asterisk (**) indicates significance
at <0.01.

No. of
No. of Unique Haplotype Nucleotide Tajima’s
Site N Haplotypes Haplotypes Diversity Diversity D Fu’s F,
California
Half Moon Bay _17 1] 5 0.8824 +/— 0.002894 +/— PAV Hy 2
0.0718 0.001925
Santa Barbara 11 7 3 0.8182 +/— 0.002563 +/— = || 498M ee —3:523"=
0.1191 0.001816
Los Angeles 26 1] 4 0:7785 +/—-~ 0.002548 4/— | —i Sissi 563352
0.0792 0.001707
Oceanside 31 1] 2 0.7269 +/— 0.002078+/— —1.713* —6.167**
Harbor 0.0832 0.001453
Agua 14 10 5 0.9231 +/— 0.003566+/— —1.174 —5.610**
Hedionda 0.0604 0.002307
San Dieguito 27 12 3 0.7350 +/— 0.001991+/— —=1.884* —8.713**
0.0920 0.001415
Mission Bay 38 19 8 0.8193 +/— 0.003116+/— —2.251* —14.838**
0.0621 0.001972
San Diego 30 12 3 0.6805 +/— 0.002093+/— —=—210* —7.805**
0.0951 0.001463
San Diego Bay 35) 18 9 0.8185 +/— 0.002833+/— —2.115* —14.841**
0.0667 0.001833
Mexico
Tijuana 34 18 5 0.8093 +/— 0.002947+/— —1.922* —14.662**
Estuary 0.0703 0.001893
Ensenada/ 28 15 4 0.8201 +/— . 0.002785+/— —2.06* —11.162**
Todos 0.0736 0.001823
Santos
Punta Banda 35 16 6 0.7109 +/— 0.002739+/— —2.287* —11.403**
0.0869 0.001786
Bahia 23 9 3 0.5850 +/— 0.001648 +/-— = —2.269* —5.574**
Asuncion 0.1222 0.001242
Bahia 26 12 4 0.7538 +/— 0.002282 +/— - =2:099* > —7-916-+
Magdelena 0.0900 0.001569
All Samples 375 92 - —1.942* —8.918**

waters (Blanchette and Gaines, 2007; Diehl, et a/., 2007). Both the temperature difference
and circulation patterns, along with discontinuities in hydrography, salinity, dissolved
oxygen, and topography, suggest that marine organisms may experience restricted larval
dispersal and thus increased potential for a decrease in gene flow Briggs, 1974; Seapy and
Littler, 1980; Diehl, et al, 2007). We found no evidence for a genetic break at Point
Conception. Thus, it appears that none of the physical differences of this biogeographic
boundary have affected the larval dispersal or gene flow of the California Halibut;
instead they are best regarded as a single, genetically homogeneous population, at least
over evolutionary time scales. These findings agree with numerous other studies
examining the role of Point Conception in shaping the evolutionary history of marine
organisms (Bernardi, 2000; Burton, 1998; Dawson, et al., 2001; Lee and Boulding, 2007).

The California Halibut population was also continuous across the Los Angeles region
(LAR). According to Dawson (2001), the LAR was fully or partially submerged before

147

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148 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

16000 —
14000 —
12000

10000 —
8000 —
6000 —
4000 —
2000 —

0 a | |
0 Z

Fig. 3. Mismatch distribution for cytochrome 6 sequences of Paralichthys californicus. Harpending’s
(to = 0L01e(P— 10198):

Ly Observed
—e— Simulated

3 4 5 6 if 8 9 10

Number of Pairwise Differences

the Late Pleistocene. Similar to the present day conditions, with a substantially-sized area
submerged, there was an increase in shallow, coastal habitat available for marine
organisms, particularly those that inhabit estuaries and bays. During the last ice age, the
LAR subsequently emerged, leading to a significant loss of shallow coastal habitat.
However given the complete loss of shallow coastal habitats elsewhere, the LAR may
have provided glacial refuge given what little habitat remained in the LAR. This
emergence most likely wiped out some coastal populations and created phylogeographic
breaks in certain lineages (Ahnelt, et al, 2004; Bernardi, 2005; Dawson, et al, 2001;
Dawson et al., 2002), suggesting that historical fluctuations in sea level were likely key
factors that contributed to these breaks (McGovern, et al., 2010; Marko and Hart, 2011).
Although populations of California Halibut may have been affected by this alteration in
habitat across the LAR, we do not see evidence of a genetic break in the halibut
population supporting this hypothesis. In addition, the estimated coalescence time for
California Halibut of approximately 160,000 yr before present does not correlate with the
last glacial cycle, an event that would have been recognized if populations were severely
affected by the loss in habitat with the emergence of the LAR.

Table 3. Estimates of Tau (T), Theta naught (80), Theta one (81), and Coalescence Times (CT; yr).

Lower Bound Mean Upper Bound
IL 0 ANTS 5.262
Do 0 feSull3 0.045
0] 1.129 41215 Infinity

Cr 13,656 159,691 330,837

PHYLOGEOGRAPHY OF CALIFORNIA HALIBUT 149

Table 4. MuGRATE estimates of migrants (M) per generation, ©, and likelihood scores (L). Top row
indicates population from which migrants leave while left columns are recipient localities.

Lc oO North Middle South
North 1.993 0.0081 s ~0 31
Middle 1.993 0.0298 2920 = ~0
South 1.993 0.1154 2050 503 *

The MIGRATE analysis indicated that the three pseudopopulations were highly
connected in a general North to South direction. This could represent longer-term gene
flow over several thousand generations being affected by the general motion of the
California Current. However, nearshore current fields, which may be those most expected
to influence California halibut during their larval stage, are chaotic and generally do not
echo the constant flow of the California current (Mitarai, et a/., 2009: White et a/., 2010).

Our results showed statistical pairwise differences of California Halibut in only the San
Diego location. However, there are no obvious reasons for this phenomenon. For
example, there are no differences in sizes or ages from the samples at San Diego which
could suggest sampling a single cohort which may skew population signals and there are
no geographic features which might be acting as a physical barrier.

The marine taxa that demonstrate phylogeographic structure in the LAR, mainly
species of the family Gobiidae, share certain qualities that are susceptible to population
bottlenecks during these periods, and these species tend to show deeper phylogeographic
structure (e.g., they are egg layers, have low adult vagility and inhabit patchy supra-tidal
or estuarine habitats, which presumably limits their dispersal capabilities). Halibut,
however, have planktonic eggs and larvae, are more mobile as adults, and they also reside
in continuous, sub-tidal habitats, factors that would suggest a refuge may not have been
necessary or advantageous during Pleistocene sea level fluctuations and concomitant
changes in habitat (Dawson, et a/., 2002). These differences in life history characteristics
may explain why certain taxa show phylogeographic structure at LAR while others do
not, including the California Halibut. In addition, other factors, including ecological
parameters (e.g., kelp habitat and ocean circulation) may influence subtle genetic
“patchiness” in California’s marine species (Selkoe, et al., 2010). The physical and
biological factors mentioned above may thus work in concert with biological
characteristics to design the genetic architecture of marine species in California.

Acknowledgements

DNA was sequenced at the HIMB EPSCoR Core Facility, with special thanks to
Rajesh Shrestha. The study was funded by the National Science Foundation (Bio-OCE
+()6-23678). the California Department of Boating and Waterways Agreement (03-106-
104), California Sea Grant Rapid-Response Funds (R/F-117PD) and a UCMEXUS
Fellowship to FJF. MTC was supported by the HIMB-NWHI Coral Reef Research
Partnership (NMSP MOA 2005-008/6682) during the course of this research.

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Bull. Southern California Acad. Sci.
110(3), 2011, pp. 152-164
© Southern California Academy of Sciences, 2011

Abundance of the long-beaked common dolphin (Delphinus
capensis) in California and western Baja California waters
estimated from a 2009 ship-based line-transect survey

James V. Carretta, Susan J. Chivers, and Wayne L. Perryman

NOAA Fisheries, Southwest Fisheries Science Center, 3333 North Torrey Pines Court,
ia Jolla sCA 92037.

Abstract.—The abundance of the long-beaked common dolphin (Delphinus capensis)
is estimated from data collected during a 2009 ship-based line-transect survey. The
survey was designed to provide fine-scale coverage of the known range of D. capensis
along the California and west Baja California coasts. Estimates of D. capensis
abundance presented are the highest to date for California waters and may reflect a
combination of improved survey design for this species and increasing numbers of
D. capensis in state waters. Estimates of D. capensis abundance within California
waters are 183,396 (CV=0.41, 95% CI 78,149 — 379,325) animals. An additional
95,786 (CV=0.47, 95% CI 36,881 — 209,507) D. capensis were estimated in Baja
California waters from the U.S./Mexico border south to the tip of Baja California.
Total estimated abundance of D. capensis in California and Baja California west
coast waters is 279,182 (CV=0.31, 95% CI 148,753 — 487,323) animals.

Introduction

In 2009, the Southwest Fisheries Science Center (SWFSC), a branch of the National
Oceanic and Atmospheric Administration (NOAA), conducted a ship-based line-transect
survey to estimate the abundance of long-beaked common dolphin (De/phinus capensis) in
California waters and along the west coast of Baja California (Chivers et al. 2010). This
was part of a larger mandate under the U.S. Marine Mammal Protection Act to collect
data on marine mammal populations used to prepare marine mammal stock assessments
published annually (Carretta et al. 2011). Surveys are conducted periodically to provide
updates on marine mammal abundance and trends. Between 1991 and 2008, six coarse-
scale vessel line-transect surveys were conducted along the U.S. west coast out to 300 nmi
(Barlow 1995, Barlow 2003, Forney 2007, Barlow and Forney 2007, Barlow 2010). These
surveys provided comprehensive estimates of abundance for short-beaked common
dolphin (Delphinus delphis) in the California Current. However, transect coverage was
not optimal for coastal species, such as D. capensis. Abundance estimates of D. capensis
from previous coarse-scale surveys have been highly variable and characterized by small
numbers of sightings and low statistical precision (Table 1). Part of this variability is
because California waters represent the northern extent of the range of a D. capensis
population which extends into Mexico. Gillnet bycatch of the California population of
D. capensis has sometimes exceeded sustainable levels (“potential biological removal” or
PBR) as defined under the Marine Mammal Protection Act (Wade and Angliss 1997). A
lack of precise abundance estimates, in combination with human-caused mortality levels
of this stock, prompted a more intensive, fine-scale survey of D. capensis coastal habitat
in 2009 to provide improved estimates of abundance. Although this species also occurs in
the Gulf of California, it was not practical to survey their entire range in 2009. Since

S52

ABUNDANCE OF LONG-BEAKED COMMON DOLPHIN 153

Table 1. Historic. estimates of D. capensis abundance within California waters, from ship-based line-
transect surveys. Multiple estimates in a given year reflect incorporation of new analysis methods to
existing datasets, such as the use of covariates in line-transect analysis (Barlow and Forney 2007).

Estimated abundance

Survey year Reference D. capensis sightings (n) (CV)
199] (Barlow 1995) 5 9,472 (0.68)
199] (Barlow & Forney 2007) 5 16,714 (n/a)
1993 (Barlow & Forney 2007) 0 0
1996 (Barlow & Forney 2007) 6 49,431 (n/a)
2001 (Barlow 2003) ] 306 (1.02)
2001 (Barlow & Forney 2007) 2 20.076 (n/a)
2005 (Barlow & Forney 2007) 6 11,191 (n/a)
1991-2005 pooled (Barlow & Forney 2007) 19 21,902 (0.50)
2005 (Forney 2007) 6 11,714 (0.99)
2008 (Barlow 2010) 7 62.447 (0.80)

management of the population is based only on abundance in U.S. waters and animals
occur throughout their range year-round, the area surveyed in 2009 was adequate to
assess the status of the U.S. population.

Field Methods

A ship-based line-transect survey was conducted in 2009 on the 62 m NOAA vessel
McArthur IT from September to December (Chivers et a/. 2010). Transect coverage of the
study area was designed to encompass the known range of D. capensis in California
waters and along the west coast of Baja California, based on examination of historic
(SWFSC) sightings (Figure 1A).

The survey design included approximately 4,800 km of transect lines, with different
coverage goals for each of three 25-day sea legs (Figure 1B). Leg | effort targeted inshore

00H

124°0°0°W 120°0'OW i600 W 12°00'W 124°00°W 120°00'W 116°0 0"W 12°00°W

Fig. 1. (A) SWFSC ship survey line-transect effort and Delphinus capensis sightings prior to 2009.
Solid black lines represent survey strata used to design transect coverage for the 2009 survey and dashed
line represents a portion of the U.S. Exclusive Economic Zone (EEZ). Thin gray lines represent historic
ship survey line-transect effort. (B) Planned transect coverage and geographic strata for the 2009 survey.

154 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

waters from Monterey Bay south to the U.S./Mexico border, with a series of 26 transects
ranging from 40 to 170 km in length, up to 150 km offshore of the mainland. Leg 2
transects covered the waters of western Baja California, with a series of 15 transects in a
saw-tooth pattern offshore to the shelf break, ranging from 85 to 195 km in length. Leg 3
transects included southern California transects from Leg 1, with additional offshore
extensions of up to 250 km from the mainland. These additional offshore transects were
not used to estimate abundance but were utilized to obtain additional data on stock
structure of D. delphis in southern California offshore waters and to determine if the
range of D. capensis was limited to inshore waters where it had been historically seen.
Abundance and density were estimated for three strata: “Central California’, ‘Southern
California’, and ‘Baja California’ (Figure 1). Areas for all strata were determined using
ArcGIS 9.3 software, with a ‘World Equal Area’ map projection.

Line-transect methods were similar to previous SWFSC surveys described by Kinzey
(2000) and Barlow and Forney (2007). The basic line-transect survey mode consisted of
three experienced marine mammal observers searching from the flying bridge of the
NOAA ship McArthur IT at a height of 15.2 m above the water. Two observers searched
port and starboard of the transect line using pedestal-mounted 25X binoculars, and a
third observer acted as data recorder, searching the transect line primarily with naked eye
and 7X binoculars. Surveys were conducted in ‘closing mode’ (Barlow and Forney 2007),
whereby the ship diverts from the transect line to allow observers to better identify and
count dolphin groups. Exceptions to closing mode occurred where navigational
constraints prevented this or where closing mode made estimation of group size more
difficult. For example, several dolphin groups (see Results) were too large and/or diffuse
to effectively estimate group size in closing mode and therefore, passing mode was used.
In passing mode, the ship maintains its course after animals are sighted and observers
count animals as they pass on either side of the ship. Dolphin groups too large or diffuse
to estimate group size in closing mode were known as ‘mega-schools’ and observers
divided the task of estimating group size between the left and right sides of the ship as the
ship passed through the school. Resulting group size estimates of ‘mega-schools’
represent the sum of estimates of two or more observers. Observers typically made three
estimates of group size: a ‘best’, a ‘high, and a ‘low’. Only the observers’ ‘best’ estimates
were used in this study.

Observers aboard research vessels tend to underestimate dolphin group sizes because
animals are diving and not available to be seen and because counting large groups of
dolphins is a difficult task (Barlow et al. 1998, Gerrodette et al. 2002). Thus, estimates of
group size require correction factors to address these biases. A NOAA Twin Otter
aircraft was utilized during the 2009 survey to coordinate with the NOAA ship McArthur
IT to obtain digital aerial photographs of dolphin groups to calibrate observer estimates
of group size. Photographs were taken using three Canon EOS-1 DS Mark III digital
cameras mounted in the belly of the aircraft (Chivers et al. 2010). Digital aerial images of
sufficient quality were obtained for 12 calibration groups (10 D. capensis and 2 D. delphis)
where all six marine mammal observers aboard the McArthur IT also obtained estimates
of group size. Observer group size calibration coefficients were developed as described in
the Analytical Methods section.

Analytical Methods

Standard line-transect methods were used to estimate the density and abundance of
D. capensis and D. delphis (Buckland et al. 2001), using the program Distance 6.0

ABUNDANCE OF LONG-BEAKED COMMON DOLPHIN 155

(Thomas eft al. 2009). Only ‘standard effort’ transect data (effort on planned transect
lines, excluding ‘deadhead’ effort between lines) where Beaufort sea state was between
zero and 4, visibility was at least 3.5 nmi, and no fog or rain were recorded were used to
estimate density and abundance. Dolphin density (D) within a stratum was calculated as:

2

a ty Mine O)eaSi;
gee 2.1; . g(0); )

where

n;; = number of dolphin groups of size j detected in stratum /,

f(0) = probability density function (km ') evaluated at zero perpendicular
distance

S;; = mean group size of dolphin groups of size category / in stratum /,
L; = length of transect line (in km) surveyed in stratum /,

g(0); = probability of detecting a dolphin group of size j on the transect
line.

Values for g(0) used in this analysis are based on those reported by Barlow and Forney
(2007) for delphinid group sizes of = 20 animals (0.856, CV=0.056) and > 20 animals
(0.970, CV=0.017), respectively. Half-normal and uniform models with simple
polynomial adjustment terms were fit to the perpendicular sighting distance data to
estimate f(0) and the effective strip width (ESW) for all geographic and group size strata
pooled. The ESW is defined as that perpendicular distance from the transect line at which
the number of objects detected beyond this distance equals the number missed within the
same distance. Perpendicular sighting distances were right-truncated at 4.0 km (excluding
510% of the largest distances) to avoid fitting extreme values near the tail of the
distribution. The model fit with the lowest Akaike’s Information Criterion (AIC) was
selected by the program Distance to estimate dolphin density. Because observers are less
likely to detect small groups of dolphins at greater distances, this may introduce a positive
bias into overall mean group size. The program Distance includes the option of correcting
mean group size based on regressing the logarithm of observed group size versus
perpendicular sighting distance. If the regression is significant at an alpha-level of 0.15,
then the ‘expected group size’ based on the regression is used in place of the observed
group size (Thomas ef al. 2009). We implemented this Distance program option in our
analysis. It should be noted that regression-based corrections to mean group size address
the bias that observers are more likely to miss small groups. This is independent of
observer calibrations from aerial photographs used to correct the bias of undercounting
of detected groups, which we discuss below.

Total abundance was estimated as the sum for all three geographic strata (Central
California, Southern California, and Baja California) as:

3
Ni= Sy Ds A; (2)

where N; is estimated abundance in stratum i and 4, is the area of the stratum. Encounter
rate (n/L) variance was estimated empirically within the program Distance from the
individual survey effort segments. We tested a range of effort segment lengths as sampling
units (5 km to 100 km), to see if resulting coefficients of variation (CV) in abundance

—
Nn
oO

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

estimates were significantly affected by segment length choice. An initial sensitivity
analysis suggested that segment lengths of 20 km provided the greatest precision for this
particular dataset (in exploratory analyses, CVs for all strata combined ranged from
0.43 to 0.51 using segment lengths of 5 to 100 km). Within a stratum 7, the CV of the
abundance estimate for groups of size 7 was calculated as the square root of the sum of
the squared CVs of the parameters group size, encounter rate, detection function, and
trackline sighting probability:

CV Nj) = | CV(Sig) + CV( 2) + CVF 0) + CV>((0)) (3)

The variance and CV of the combined abundance (across all group size categories j within
stratum 7) was calculated as:

Var( Nj) = ». (CV(Niy)-Nij)” (4)

JF"

at 4 / Var(N;)
( ae Ae alee (5)

I

and

Variances for combined estimates of abundance (multiple strata) were also calculated as
shown in Equation 5. Ninety-five percent confidence intervals for abundance estimates
were estimated by simulating a log-normal distribution from each point estimate and
associated CV and taking the 2.5'" and 97.5" percentiles respectively, as the lower and
upper limits of the confidence interval.

Group size calibration

Group size calibration coefficients were developed from digital aerial photographs
of 12 dolphin groups (10 Delphinus capensis and 2 Delphinus delphis) and correspond-
ing observer ‘best’ estimates of group size from the research vessel. Three counters
independently counted dolphin numbers from aerial photographs of the 12 calibration
groups and the ‘true group size’ for each sighting was calculated as the mean of the three
photo counts (Table 2). We calculated individual observer calibration coefficients by fitting
a log-transformed, linear regression (intercept = 0) to the 12 photo calibration groups and
‘best’ estimates of group size. The calibration coefficient, Bp, for a given observer 1s:

In Sa = Bo: In S photo (4)
where
Shest= the observer’s best estimate of group size
and
Siiiore = mean ‘true group size’ determined from aerial photographs.
Estimates of group size for individual observers were corrected as follows:

In Sorrecied = || Sbest/ Bo (5)

In cases where multiple observers estimated separate portions of a mega-school, a single

ABUNDANCE OF LONG-BEAKED COMMON DOLPHIN 157

Table 2. Dolphin counts from digital aerial photographs of 12 Delphinus groups obtained in 2009 and
used for group size calibration. Uncorrected field estimates of mean group size and corrected estimates of
group size, based on 2009 and ETP calibration coefficients are shown.

Uncorrected Corrected Mean Corrected Mean
Sighting Mean Photo Mean Best Best Estimate (2009 Estimate (ETP
Number Species Count Estimate coefficients) correction factor)
161 D. capensis 569 310 590 360
290 D. delphis BYP 155) 269 180
291 D. capensis 634 353 681 411
292 D. capensis 1394 396 778 461
293 D. capensis 776 283 530 329
320 D. capensis 48 33 46 3)
3 D. capensis 35) 20 Di, D3
SZ D. capensis 475 613 1166 AS
514 D. capensis 284 289 561 336
526 D. capensis 1281 404 795 470
528 D. capensis 574 303 555 3)
705 D. delphis 122 ISD 278 185

calibration coefficient was used and calculated as the mean of all individual observer
calibration coefficients. For comparison, we also report estimates of abundance obtained
using uncorrected group sizes (calibration coefficients = 1.00) and those obtained by
applying a mean group size correction factor for 52 observers calibrated during line-
transect surveys in the Eastern Tropical Pacific (ETP) (Gerrodette et al. 2002, Gerrodette
and Forcada 2005). The ETP correction factor is based on the mean ratio of observer best
estimates to photo counts (0.860), with a mean of 38 calibration groups per observer
(Gerrodette et al. 2002, Gerrodette and Forcada 2005). Estimates of dolphin density and
abundance presented in the Results section utilize the calibration coefficients developed
from 12 calibration schools photographed in 2009.

Results

Over 5,000 km of standard line-transect effort was conducted during the 2009 survey in
Beaufort sea states 0 through 5 (Table 3; Figure 2). The length of completed transects
slightly exceeds the length of the designed transect grid because Southern California
stratum transects were surveyed on both Legs | and 3. Standard effort sightings included
88 groups of D. capensis (Figure 3). The observed distribution of D. capensis sightings in
2009 did not differ appreciably from historic sighting distributions (Figures | and 3). No
sightings of D. capensis were made in the Offshore stratum, though some groups were
sighted near the boundary of the Offshore and Southern California strata. Observers
underestimated group size for the 12 calibration schools, as evidenced by the mean ratio
of observer best estimates to aerial photo counts (=0.669, Table 2). Four out of six
observers had group size correction coefficients of less than one and the degree of
underestimation increased with group size (Tables 2 and 4; Figure 4). After correcting
observer best estimates with linear regression, the mean ratio of corrected counts to aerial
photo counts was 1.20 (Table 2). A half-normal model provided the best fit to the
perpendicular distance data over competing uniform models, based on the lowest AIC
values (Figure 5). The mean ESW for D. capensis was 2.81 km (CV=0.13), which is
similar to previous estimates reported by Barlow and Forney (2007) and Barlow (2010),
who reported values of 2.85 km and 2.62 km, respectively.

158 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 3. Stratum sizes and length of transect lines surveyed during standard survey effort. Estimates
of density and abundance in this report do not include survey effort and sightings within the
‘Offshore’ stratum.

Length of transects surveyed (km)

Study Area Beaufort Total

Stratum (km?) 0-3 Beaufort 4 Beaufort 5 (Beaufort 0—5)
Central California 23,259 D233 82 68 383
Southern California 42,263 1,059 740 340 MN 3S)
Offshore 32,094 291 292 180 763
Baja California 175,493 580 1,016 142 1,738
TOTAL 273,109 2,163 DBO) 730 5,023

Mean group size of D. capensis (corrected for undercounting bias) was 454 animals
(Table 5). This is larger than that reported by Barlow and Forney (2007), who reported a
mean group size of 315 animals, but smaller than the mean of 535 animals recently
reported by Barlow (2010) from a 2008 survey. Approximately 279,000 D. capensis were
estimated for all geographic strata combined, with approximately 180,000 animals in U.S.

38°0'0"N
=
ss
CALIFORNIA oN o3)
E: by \
SN 2 Pt. Cancentio
° oT fi "é = : . =
34°00°N Pr27 1 AIF UNITED/STATES

5

30°00"N

Nautical Miles

124°0 0"W 120°0 0"W 116°0'0"W 112°0 0"W

Fig. 2. All standard survey effort completed during Legs 1-3 (07 September — 09 December 2009).

ABUNDANCE OF LONG-BEAKED COMMON DOLPHIN 159

38°0'0"N

a ™
CALIFORNIA a

x =

e

@ Ft. Conception

x,
aor" NFER UNITED 9 sares
rs
= 47.
< e

30°0'0"N
26°0'0"N

22°0'0"N : ;
280 Nautical Miles

1240 D"W 120 OD" 116 OD" 112 D"W

Fig. 3. Sighting locations of long-beaked common dolphin (D. capensis, n=88) during standard survey
effort (gray lines).

west coast waters (Table 6). These estimates are based on using observer calibration
coefficients calculated from 12 Delphinus groups photographed in 2009. Corrected
estimates were on average, nearly double that of estimates not corrected for
underestimation of group size (Figure 6). Estimates of density and abundance for D.
capensis are provided in Table 6.

Discussion

Estimated abundance of D. capensis in California waters in 2009 (~ 180,000 animals) is
the highest of any ship line-transect survey to date. Nearly 40% of the estimate (~ 70,000)
comes from the Central California stratum, where relative survey effort was low, group
sizes were large, and precision of the estimate was poor (CV=0.79). The ratio of D.
capensis to D. delphis sightings during standard transect effort was nearly 1:1 (88 and 90
sightings, respectively) within our strata. Previous SWFSC line-transect surveys from
1986-2008 within the same strata had a ratio of 1:3.6 (73 and 262 standard-effort

160 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 4. Individual group size correction coefficients based on ‘best’ estimates of group size for 12
calibration groups photographed in 2009.

Observer Group size correction coefficient (2009)

0.859
0.943
0.874
0.909
0.880
0.931
Mega-school aggregate 0.900

au) (ea! fol @) les)

sightings, respectively) D. capensis to D. delphis sightings (SWFSC unpublished data).
The difference in relative sighting numbers of each species may reflect differences between
fine-scale and coarse-scale transect coverage between previous surveys and ours, but it
may also reflect increasing trends in abundance of D. capensis.

3
2 :
9 Cc
5 Q
0 E
E =
=
0 500 1000 1500 3 4 5 6 i
mean photo log(mean_ photo}
oO
0
Ww
9 6 5
Te N
dy .
of 2
o if 2
2
Oo
0 500 1000 1500 3 4 5 6 7
mean. photo logimean. photo}

Fig. 4. Top Row: Mean photo counts and mean observer estimates (mean of six ‘best’ observer
estimates) for 12 calibration groups of common dolphin photographed during 2009. Both raw (A) and log-
transformed values (B) are shown. Bottom row: Corrected observer estimates based on the linear
relationship between observer estimates and ‘true group size’ from aerial photographs. Both raw (C) and
log-transformed (D) values are shown. Diagonal lines represent a 1:1 relationship between uncorrected/
corrected observer estimates and counts from aerial photographs. In the absence of estimation error, all
points would fall on the diagonal line.

ABUNDANCE OF LONG-BEAKED COMMON DOLPHIN 161

Half normal model fit to perpendicular distance
data

— Sa
= fh f§

SS
5
s
° 08
o.

c 0.6
= 0.4
oO

O2
®
OQ

>)

2

Perpendicular Distance in km

Fig. 5. Half normal model fit to D. capensis perpendicular sighting distances (n=56) for Beaufort sea
states 0 to 4 and visibility = 3.5 nmi. Model fit statistics are f(0)=0.356 km ', CV=0.13, chi-square
p=0.445, and the effective strip width (ESW) is 2.81 km. Truncation distance is 4.0 km.

The ratio of D. capensis to D. delphis strandings in southern California increased
following a strong 1982-83 El Nino (Heyning and Perrin 1994). Within San Diego
County, dramatic increases in the ratio of D. capensis to D. delphis strandings were
observed from 2006-2008 (Danil et al. 2010) and these have persisted through 2010
(SWESC unpublished stranding data). Trends in D. capensis abundance are not apparent
from a series of six line-transect cruises conducted by SWFSC between 1991 and 2008,
but it is notable that the most recent survey in the series (2008) yielded the highest
estimate of abundance (~ 62,000 animals, Barlow (2010), Table 1). An abundance trend
analysis for D. capensis would be difficult to perform, as the line-transect estimates are
based on few sightings and inter-annual oceanographic variability likely influences the
distribution of this trans-boundary population. Discerning a trend is also confounded by
the fairly recent recognition of D. capensis as a separate species (Heyning and Perrin
1994) and the related issue that marine mammal observers may have experienced a
‘learning curve’ in their ability differentiate D. capensis from D. delphis since that time.
The relatively high estimate of D. capensis abundance in 2009 may be related to a

Table 5. Number of standard-effort sightings (n) of D. capensis and mean group sizes (based on 2009
photographic calibration coefficients) for three geographic strata where density and abundance were
estimated. Only groups used for density and abundance estimation are included in this table. Mean group
size for all strata is calculated as the weighted mean (by number of sightings in each strata) for all
three strata.

Central California Southern California Baja California All Strata

Mean Mean Mean Mean
Species n group size n group size n group size n group size

Delphinus capensis 6 716.0 36 481.3 14 274.3 56 45

Nn

162 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 6. Total number of sightings (7), estimated abundance (JN), coefficients of variation (CV), lower
and upper 95% confidence intervals by strata for long-beaked common dolphins. Estimates are based on
group size calibration coefficients estimated from aerial photographs obtained in 2009 (see text). Stratum
estimates for ‘Southern CA’ represent pooled estimates of Leg 1 and Leg 3 survey data. U.S. EEZ stratum
values represent combined Central CA and Southern CA estimates, but do not include sightings and effort
data from the ‘Offshore’ stratum in Figure 1. No sightings of long-beaked common dolphin were recorded
in the Offshore stratum.

Delphinus Density per

capensis Stratum n N (CV) Lower 957. Cle" Uppems57on@l 1000 km?
Central CA 6 71,658 (0.79) 14,650 224,313 3,080
Southern CA 36 111,738 (0.44) 44,618 229,417 2,643
Baja CA 14 95,786 (0.47) 36,150 205,078 545
U.S. Strata 42 183,396 (0.41) 78,149 3793325 2,798
All strata 56 ZISESZN(OS i) 148,753 487,323 1,158

moderate El Nino event that began in mid-2009 (NOAA Climate Prediction Center),
which may have shifted D. capensis distribution northward into U.S. waters. Differences
in abundance estimates between this and previous surveys may also be due to analytical
differences. We did not use Beaufort 5 data in our analysis, which has been necessary to
include in previous survey analyses that suffered from poor weather. Nor did we use
covariate modeling in our line-transect approach (Marques and Buckland 2003, Barlow
and Forney 2007), but instead utilized simple stratification to select good weather
conditions for inclusion (which was only possible because of the inshore nature of our
transect coverage).

Our estimates are also influenced by the group size correction factors derived from the
aerial photographs, though it should be noted that even our uncorrected estimates of
abundance are higher than any previous estimates in this region (Table 1, Figure 6.).

ro)

oO

S CO Central CA
2 6 HB Southern CA
2 Re [ BajaCA
5 C4 = §CA Strata
Ww Co At Strata
®
oO

fen)
E09
aS
<— =

oO

oO

oO

oO

wm

oO

No.Correction Correct.ETP Coef.2009

Group Size Corrections

Fig. 6. Estimates of abundance by stratum for long-beaked common dolphin (Delphinus capensis).
Estimates shown are based on uncorrected group sizes, group size corrections based on coefficients
developed from 2009 aerial photographs, and a global correction factor for 52 observers, based on the
ratio of observer best estimates to photo counts in the Eastern Tropical Pacific (Gerrodette et al. 2002).

ABUNDANCE OF LONG-BEAKED COMMON DOLPHIN 163

Abundance estimates obtained with group size calibration coefficients based on 2009
aerial photographs were nearly double that of abundance estimates obtained with
uncorrected group sizes (Figure 6). This is similar to the ratio of mean photo counts
divided by mean observer counts (1.87) for the 12 calibration groups in Table 2. This
highlights the challenges of accurately estimating dolphin numbers from a research vessel.
The 2009 coefficients also provided estimates that are considerably higher than estimates that
would be obtained if one applied the inverse of the mean ratio of observer best estimates to
aerial photo counts (=0.860) for 52 calibrated observers in the ETP (Gerrodette et al. 2002)
(Figure 6). The ETP correction factor is based primarily on spotted (Stenel/la attenuata) and
spinner (Stenella longirostris) dolphin schools, where the mean number of dolphins per
school was approximately 230 (based on photo counts). In contrast, our calibration
coefficients are derived from 10 schools of long-beaked common dolphin and 2 schools of
short-beaked common, with a mean of 539 animals per school (Table 2). Long-beaked
common dolphin schools are typically characterized by the largest group sizes of any
cetacean encountered in the California Current (Barlow and Forney 2007). Barlow and
Forney (2007) noted that in their calibration of observers’ estimates of group size, it was
apparent that proportionately larger corrections were applied to larger groups. Thus, the
large increases in group size (and abundance) resulting from our calibrations are not
extraordinary, considering the relatively large mean group sizes observed in 2009.

Acknowledgments

We would like to thank Bill Perrin, Jeff Laake, Tim Gerrodette and Jay Barlow for
advice on survey design and comments on the manuscript. The manuscript was also
improved by the comments of two anonymous reviewers. Thanks to marine mammal
observers Jim Cotton, Rich Pagen, Richard Rowlett, Juan Carlos Salinas, Ernesto
Vasquez, and Suzanne Yin. Cruise leaders were Eric Archer (and JVC and SJC). The
aerial survey team included Morgan Lynn, Jim Gilpatrick, Fionna Matheson (and WLP).
This work could not have been completed without the dedication of the crew and
command of the R/V NOAA ship McArthur II and our international collaborators:
Lorenzo Rojas-Bracho and Jorge Urban. All work was authorized and conducted under
permits 774-1714-10, MULTI-2008-003-A2 and 05599 issued by the U.S. National
Marine Fisheries Service and National Marine Sanctuary, and Mexico’s Secretaria de
Relaciones Exteriores, respectively.

Literature Cited

Barlow, J. 1995. The abundance of cetaceans in California coastal waters: I. Ship surveys in summer/fall

1991. Fish. Bull., 93:1-14.

, T. Gerrodette, and W. Perryman. 1998. Calibrating group size estimates for cetaceans seen on ship

surveys. Southwest Fisheries Science Center Administrative Report, LJ-98-11. 39 pp.

. 2003. Preliminary estimates of the abundance of cetaceans along the U.S. west coast: 1991—2001.

Southwest Fisheries Science Center Administrative Report LJ-03-13. 31 pp.

and K.A. Forney. 2007. Abundance and population density of cetaceans in the California Current

ecosystem. Fish. Bull., 105:509-526.

. 2010. Cetacean abundance in the California Current estimated from a 2008 ship-based line-

transect survey. U.S. Department of Commerce, NOAA Technical Memorandum, NOAA-TM-

NMEFS-SWESC-456. 19 pp.

Buckland, S.T., D.R. Anderson, K.P. Burnham, J.L. Laake, D.L. Borchers, and L. Thomas. 2001.
Introduction to Distance Sampling: Estimating abundance of biological populations. Oxford
University Press, Oxford. 432 pp.

164 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Carretta, J.V., K.A. Forney, E. Oleson, K. Martien, M.M. Muto, M.S. Lowry, J. Barlow, J. Baker,
B. Hanson, D. Lynch, L. Carswell, R.L. Brownell, Jr., J. Robbins, D.K. Mattila, K. Ralls, and
M.C. Hill. 2011. U.S. Pacific Marine Mammal Stock Assessments: 2010. U.S. Department of
Commerce, NOAA Technical Memorandum, NMFS-SWFSC-476. 352 pp.

Chivers, S.J., W.L. Perryman, N.M. Kellar, J.V. Carretta, F.I. Archer, J.V. Redfern, A.E. Henry, M.S.
Lynn, C. Hall, A. Jackson, G. Serra-Valente, T.J. Moore, C. Surrey-Marsden, and L.T. Ballance.
2010. Ecosystem Survey of Delphinus species cruise report. U.S. Department of Commerce, NOAA
Technical Memorandum, NOAA-TM-NMFS-SWESC-464. 53 pp.

Danil, K., S.J. Chivers, M.D. Henshaw, J.L. Thieleking, R. Daniels, and J.A. St. Leger. 2010. Cetacean
strandings in San Diego County, California, USA: 1851-2008. Journal of Cetacean Research and
Management, 11(2): 163-184.

Forney, K.A. 2007. Preliminary estimates of cetacean abundance along the U.S. west coast and within
four National Marine Sanctuaries during 2005. U.S. Department of Commerce, NOAA Technical
Memorandum, NOAA-TM-NMEFS-SWESC-406. 27 pp.

Gerrodette, T., W. Perryman, and J. Barlow. 2002. Calibrating group size estimates of dolphins in the

Eastern Tropical Pacific Ocean. Southwest Fisheries Science Center Administrative Report, LJ-02-

08. 26 pp.

and J. Forcada. 2005. Non-recovery of two spotted and spinner dolphin populations in the eastern

tropical Pacific Ocean. Marine Ecology Progress Series, 291:1—21.

Heyning, J.E. and W.F. Perrin. 1994. Evidence for two species of common dolphins (Genus Delphinus)
from the eastern North Pacific. Contr. Nat. Hist. Mus. L.A. County, No. 442.

Kinzey, D., P. Olson, and T. Gerrodette. 2000. Marine mammal data collection procedures on research
ship line-transect surveys by the Southwest Fisheries Science Center. Southwest Fisheries Science
Center Administrative Report LJ-00-08. 32 pp.

Marques, F.F.C. and S.T. Buckland. 2003. Incorporating covariates into standard line transect analyses.
Biometrics, 59:924-935.

NOAA Climate Prediction Center. Tabular E] Nino index data: (15 June, 2011; http://www.cpe.ncep.noaa.
gov/products/analysis_monitoring/ensostuff/ensoyears.shtml).

Thomas, L., Laake, J.L., Rexstad, E., Strindberg, S., Marques, F.F.C., Buckland, S.T., Borchers, D.L.,
Anderson, D.R., Burnham, K.P., Burt, M.L., Hedley, S.L., Pollard, J.H., Bishop, J.R.B., and
Marques, T.A. 2009. Distance 6.0. Release 2. Research Unit for Wildlife Population Assessment,
University of St. Andrews, UK. (10 April, 2011; http://www.ruwpa.st-and.ac.uk/distance/).

Wade, P.R. and R. Angliss. 1997. Guidelines for assessing marine mammal stocks: report of the GAMMS
workshop April 3—5, 1996, Seattle, Washington. U.S. Dep. Commer., NOAA Tech. Memo.
NMEFS-OPR-12. 93 pp.

Bull. Southern California Acad. Sci.
110(3), 2011, pp. 165-176
© Southern California Academy of Sciences, 2011

Commercial fishery effort for California spiny lobster (Panulirus
interruptus) off Orange County, California before State Marine
Reserve implementation

Eric F. Miller,'* David G. Vilas,’ Jennifer L. Rankin,’ and David Pryor?

'MBC Applied Environmental Sciences, 3000 Red Hill Ave., Costa Mesa, CA 92626,
phone: 714-850-4830, fax: 714-850-4840, email: emiller@mbcnet.net
°Orange Coast District, California State Parks, 8471 N. Coast Highway,
Laguna Beach CA 92651, 949 497-1421

Abstract.—The California spiny lobster (Panulirus interruptus) commercial fishing
effort along the southern Orange County, California coastline was examined using
fishery-independent counts of trap marker buoys and fishery-dependent information
submitted to the California Department of Fish and Game in the required
commercial logbooks. Buoy counts were conducted in spatially-discrete subsections
of the coastline inshore of the 30-m isobath to determine the density of fishing effort
at a scale finer than is afforded by the standard fishing blocks used by the
Department of Fish and Game. Both the buoy densities and fisherman-reported trap
pull counts recorded declining effort across the area as the season progressed. Effort
was more diffuse at the beginning of the season, but increasingly focused on areas
covered by giant kelp canopy, including the boundary of a previously existing, small
no-take marine reserve located in the study area. General effort declined as the
frequency of capturing a harvestable California spiny lobster declined. The catch per
unit effort of harvestable and sublegal individuals was found to decline at highly
correlated rates with no effect on the following season. Fishing regulations in
portions of this study area will be increased through the implementation of a
network of no-take marine reserves. Data presented herein provides a baseline to
compare future fishing effort in the Laguna Beach area after two of the three most
intensively fished sites are closed due to their inclusion in the Laguna Beach State
Marine Reserve and adjoining State Marine Conservation Area.

Introduction

The Orange County coastline between Huntington Beach and Doheny State Beach,
California is characterized by cliff-backed sandy beaches interspersed between numerous
headlands, where rocky intertidal substrate extends offshore as subtidal reefs. As a result
of the extensive rocky habitat, the area is targeted by the commercial California spiny
lobster (lobster; Panulirus interruptus) trap fishery except in the no-take Heisler Park
State Marine Reserve (HPSMR) located off the Laguna coast (McArdle 1997;
OCMPAC!). In the Orange County area, lobster traps are typically deployed from
small boats around shallow reefs and hard structure with holes and crevices where
lobsters conceal themselves during the day (Mitchell et al. 1969). California Department

*Corresponding Author: emiller@mbcnet-net
' Orange County Marine Protected Areas Committee. 2009. MPA sites and regulations. http://www.
ocmarineprotection.org/mpa_sites_and_regulations.php. Accessed 17 April 2009.

165

166 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

of Fish and Game designated October to March each year as the commercial lobster
fishing season (Barsky 2001), with most landings historically recorded during the first
month of the season (Parnell et al. 2007; CDFG 2008). California commercial fishery
regulations require each trap be attached individually to a buoy marked with the owner’s
commercial fishing license number, followed by a “P” for commercial lobster pot to make
their identification easier (CDFG 2011). After the first Tuesday in October, or nearly one
week after the season opens on first October Wednesday, buoys may be submerged by a
timed release device called a pop-up.

Harvest effort has been routinely recorded for the commercial fishery through
logbooks (CDFG 2011). The commercial logbooks record the number of traps retrieved
(pulled) and the number of lobsters taken, but they do not provide fine-scale spatial
information on the location of the trap set. Rather, harvest sites are designated within
California Department of Fish and Game fishing blocks, which are predesignated 10 min
latitude < 10 min longitude areas, although blocks along the coastline are often not
square and therefore of smaller and variying size. At this spatial resolution, the fishing
effort along gradients inside and outside a marine protected area (MPA) cannot be fully
evaluated. Therefore, we attempted to evaluate the level of fishing effort along the
Orange County coastline, including the area surrounding the HPSMR, which will be
subsumed into future lobster no-take marine reserves; a complex including the adjoining
Laguna Beach State Marine Reserve and State Marine Conservation Area*. Basic
information at a spatial scale finer than the California Department of Fish and Game
fishing blocks will be needed to evaluate the impacts of the newly designated MPA
complex. Of specific interest is the responses in the lobster aggregations that will be
released from harvest pressure within the new MPA complex. We expect areas open to
fishing effort would likely receive pressures proportional to their production of
havestable (>83 mm carapace length) individuals. The presence of a no-take reserve
within the area during the survey may provide insights into what future effort can be
expected once the new no-take marine reserves have been implemented. We attempt to
address this by first describing the present baseline effort under existing spatial
management regulations prior to the implementation of the MPA complex.

Materials and Methods

Fishing pressure was estimated by counting commercial lobster fishing trap buoys as a
proxy for each individual trap during the 2008-2009 commercial fishing season (1
October 2008 to 18 March 2009). Counts were conducted monthly (except February
2009) from a small vessel between 3 October 2008 and 6 March 2009 by two observers
under clear skies and calm seas between (600 and 1100 h. Final counts represent the mean
of the two counts. The use of pop-ups on buoys could not be quantified, but we assumed
its impact on the counts would likely be most pronounced between the first survey,
completed before pop-ups were allowed, and the second survey after pop-ups were
allowed. In either case, these buoy counts represent a conservative estimate of fishing
effort as the number of submerged buoys could not be verified.

Surveys were completed within three California Department of Fish and Game fishing
blocks (737, 738, and 757; Figure 1). These fishing blocks (block) encompassed

* California Fish and Game Commission gives final approval for south coast marine protected areas.
http://www.dfg.ca.gov/news/news10/2010121501-Commission-Approves-SCMPA.html. Accessed, July 15,
2011.

ORANGE COUNTY COMMERCIAL LOBSTER FISHERY EFFORT 167

Newport Bay

Dana Point

—— 30-m isobath

ma 2008 Kelp

Gs Heisler Park

Laguna Beach MPA Complex
{__] DFG Catch Block

L__, Lobster Count Area
<—Lobster Count Subdivision

Fig. 1. Map of the study area including all three catch blocks (757, 738, and 737) and the subsections
delineated for the current study, Heisler Park no-take marine reserve (lla), and the Laguna Beach MPA
complex that includes the Laguna Beach State Marine Reserve and the Laguna Beach State Marine
Conservation Area. The occurrence and spatial distribution of the giant kelp canopy mapped during aerial
surveys in 2008 are also depicted.

approximately 62 km of linear coastline. Each block was further subdivided into
subsections designated by landmarks easily recognized from the deck of the survey vessel
with an offshore extent bounded by the 30-m isobath (Figure 1). The HPSMR is within
block 737 designated subsection lla. Areas (km7) of each subsection were calculated

168 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

using ArcMAP®. The trap density (count/km*) was calculated for each subsection from
the monthly counts. Similar density estimates were calculated by block to better
summarize the surveys at a more comparable spatial scale to the commercial fishery
records. It should be noted, however, that only a subset of the area of each block was
surveyed as the blocks extended offshore beyond the 30-m isobaths. No information was
collected on buoys, if present, located offshore of the 30-m isobaths. The rate of declining
effort was measured as the percent of the October buoy density observed each subsequent
month of the season.

Habitat information was described using giant kelp (Macrocystis pyrifera) maximum
annual canopy area as a proxy of hard substrate within each subsection. Giant kelp
canopy areas surveyed in December 2008 were compiled from MBC (2009*) with the
subsection areas calculated in ArcMAP. Confirmation of the co-occurrence of giant kelp
canopy and hard substrate was done by reviewing habitat maps in Marinemap?.
Spearman rank correlation was used to compare the giant kelp canopy area by subsection
with survey-specific buoy densities.

The CDFG provided commercial lobster fishery logbook data (2000-2009) summa-
rized by month and fishing block on the number of traps pulled, legal individuals retained
and sublegal individuals returned. Due to fishermen confidentiality requirements,
data were only provided for blocks where at least three fishermen set traps that month
(K. Barsky, pers. comm®.). We examined these data for long-term trends in effort.
Despite the spatial scale differences, the commercial landing data were used as an
independent verification of the buoy density estimates. Linear regression was used to
compare the monthly buoy count densities by block (737, 738, and 757) against the
corresponding trap pull records for the 2008 commercial season. The mean catch rate (+
standard error), or catch per unit effort (CPUE; count/trap) was calculated for the entire
survey area, after combing blocks, for each of the 2000 to 2009 commercial seasons. A
one-way ANOVA with SNK multiple comparison test was used to compare the October
CPUEs for each commercial season for legal-sized individuals to test for changes in
harvest success. Fisherman response to declining catches was evaluated by regressing the
legal-sized CPUE against the number of traps pulled for each month in the 2008 season
when concurrent buoy counts were completed. Linear regression was used to compare the
legal and sublegal CPUEs for each block by season, 2000-2009, to examine for
similarities in their trends over the season. All statistical analyses were completed using
Sigmaplot 11 (SYSTAT’).

Results

Five monthly (minus February) counts of commercial lobster trap buoys were made
during the 2008-2009 California lobster fishery season. A total of 8676 buoys were
counted during the five surveys in each of the three fishing blocks. Total buoy density

°ESRI 2010. ArcMap Geographic Information System software version 10. ESRI, Redlands,
California.

*MBC Applied Environmental Sciences. 2009. Status of the Kelp Beds 2008 San Diego and Orange
Counties. Prepared for the Region Nine Kelp Consortium.

> Marinemap. 2011. Southcoast Marine Protected Area Habitat Mapping. http://southcoast.marinemap.
org/marinemap/. Accessed, July 28, 2011.

°K. Barsky, Senior Invertebrate Specialist, California Department of Fish and Game, Ventura,
California

’SigmaPlot version 11. Systat Software, Inc. San Jose, California.

ORANGE COUNTY COMMERCIAL LOBSTER FISHERY EFFORT 169

80
70 a
60
50
40
30

Buoy density (count/km*)

Oct Nov Dec Jan Feb Mar Apr
Date

Fig. 2. a) California spiny lobster trap marker buoy density (+ standard error) summed across all
three fishing blocks by survey date during the 2008-2009 commercial fishing season and the best fit linear
regression (R* = 0.94) describing the general trend, b) total buoy density in each fishing block depicted in
Figure | by survey date.

linearly (R* = 0.94, p = 0.006) declined each month of the season (Figure 2a). Effort was
greatest in block 737 where 51% of the total buoy density was observed, after
standardizing for the area surveyed. This was followed by block 757 with 36% and block
738 with 13%. Effort in block 757 was initially the most consistent registering the smallest
change between the first and second survey while the remaining block-specific densities
declined each month (Figure 2b). Block 757 densities registered the largest month-month
decline with 48% fewer buoys observed between the December and January surveys, as
compared to the October baseline.

The subsection densities revealed distinct variations in effort within each block
(Figure 3). Subsections 3, 9, and 11b were among the most intensively fished subsections.
These include relatively unique areas, in comparison to the rest of the survey area,
including the headlands of Dana Point (subsection 3) and an area located adjacent to the
HPSMR (subsection 11b). Effort in subsections 3 and 14b was the greatest during the
first survey near the season opening while subsection 11b surrounding the HPSMR

170 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

250 738 737 757
200 ¥ 10/3/2008

200 4 11/14/08

400 § 12/19/08

Buoy density (count/km’)

400 ¥ 1/29/09

500 1000000

3/6/09
Bd 100000

10000

ow
oO
jo)
(,W) ease Adoueo djey

100 / 1000
PP DO LVN SNCIN ANAS A O91@ & > YN

North Area South

Fig. 3. California spiny lobster trap marker buoy density in each subsection of the three fishing blocks
depicted in Figure | by survey date during the 2008-2009 commercial fishing season. The Heisler Park no-
take marine reserve is subsection 1la. Maximum annual giant kelp canopy (m7) observed during 2008 in
each subsection is represented. Note the log scale for kelp canopy.

received the greatest effort during the next two surveys. Subsections 3, 9, and I1b
remained the most productive throughout the season but each declined as the season
progressed. Some buoys were recorded within the no-take reserve. Whether these
represented traps set within the boundaries or simply a case of the buoy drifting into the
reserve while the trap was set outside of the boundary could not be verified.

ORANGE COUNTY COMMERCIAL LOBSTER FISHERY EFFORT 17]

14000
12000
10000
8000
6000
4000
2000
0

Trap pull

Sd eelopeZ0 2a 50 35-40 45

Buoy density (count/km*)

Fig. 4. Scatterplot of the number of commercial California spiny lobster traps pulled, as reported via
the California Department of Fish and Game-required commercial fishing logbook, versus the buoy
density (count/km7) summed across the three fishing blocks depicted in Figure 1 and monitored during the
2008-2009 commercial fishing season. The best-fit regression is drawn (R? = 0.93).

Thirteen of the 24 subsections contained reef habitat as suggested by the presence of a
giant kelp canopy (Figure 1). All five subsections in block 757 were within the boundary
of the Dana Point-Salt Creek kelp forest as represented by the presence of a canopy. The
overall maximum canopy area was in subsection 4 with 0.743 km’, although this area lies
outside of the soon-to-be implemented MPA complex which will primarily encompass
block 737. Subsection 3, however, had the greatest proportion of its area covered by giant
kelp canopy (Figure 3). The HPSMR (subsection lla) had no kelp canopy while the
adjacent offshore and southeast area (subsection 11b) had a small area of kelp canopy
(Figures | and 3). No surface canopy was observed to the northwest of the HPSMR
within block 737 until the North Laguna kelp bed which covers subsections 14a (block
737) through subsection 17 in block 738. Spearman rank correlation analysis found a
significant correlation (p < 0.05, n = 24) between each survey-specific buoy density by
subsection and the associated kelp canopy. With the exception of the January 2009
survey, correlation coefficients (r) steadily increased from 0.53 for the October 2008
survey through 0.72 for the March 2009 survey.

A significant relationship (R? = 0.92, F = 32.349, df = 1,3, p = 0.011) was detected
between the number of traps pulled reported by commercial fisherman and the buoy
densities in all three surveyed blocks, combined, during the 2008 season (Figure 4). The
degree of agreement between the two effort measures ranged from block 737 (R* = 0.97,
p = 0.002) to block 738 (R” = 0.86, p = 0.025). Total effort was highest in block 757 in
during the 2008 fishing season (Figure 2a), which likely related to the differences in size
between the three blocks (Figure 1). Effort significantly responded to the legal-sized
CPUE with the greatest effort occurring when legal-sized individuals were commonly
taken, but declined linearly when the legal-sized CPUE declined (Figure 5; R* = 0.23,
F = 9.995, df = 1,34, p = 0.003).

The fishery-dependent data was not standardized to area. Logbook records for the
Laguna Beach area indicated CPUE for both legal-sized and sublegal-sized individuals

172 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Ln legal-sized CPUE

5 6 i 8 9 10 ld
Ln trap pulls

Fig. 5. Scatterplot of the number of commercial California spiny lobster traps pulled, as reported via
the California Department of Fish and Game-required commercial fishing logbook, versus the legal-sized
catch per unit effort (CPUE; count/trap) for the three fishing blocks depicted in Figure | for the 2007—
2008 and 2008-2009 commercial fishing seasons, after Ln-transformation. The best-fit regression is drawn
(Re 1023)

declined each year as the season progressed (Figure 6); often in similar significantly
correlation fashion (R* = 0.65, p < 0.001; Figure 7). The effect of this simultaneous
decline on the subsequent season was examined. Each season began with similar CPUEs
for legal-sized (~ 0.7 individuals/trap) lobsters, with the exception of 2004. The October
2004 CPUE was significantly higher (ANOVA, F = 9.731, df = 9,20, p < 0.001) than the
remaining years, but no differences were detected between any other combination of
years.

Discussion

Despite the potential use of pop-up devices to minimize buoy visibility, the significant
relationship between buoy densities and the number of traps pulled reported by the
commercial fleet (Figure 4) validate the use of buoy counts as a fishery-independent
monitoring technique. Using the combination of this and fishery-dependent logbook
information, the Orange County lobster fishery was reviewed to determine the spatial
distribution of effort. Although catch has been reported and fishing practice is known
anecdotally, the density and location of traps set at any time during the season off Orange
County, California has not been well documented. Observations of commercial lobster
fishing in Orange County suggested that fishing effort was most intense at the beginning
of the season, with effort declining as the season progressed. Because of minimum size
requirements for the legal take of lobster, harvestable individuals should be most
abundant early in the season as a result of growth during the seasonal closure. Observed
fishing effort (Figure 2a) and commercial logbook information (Figure 6) concur with
this hypothesis. All available measures of effort suggest that as the catch declines, fishing
effort correspondingly declines (Figure 5).

More important than the sheer number of traps is their distribution throughout the
area. Adult California spiny lobsters prefer high-relief rocky habitat (Barsky 2001). While

ORANGE COUNTY COMMERCIAL LOBSTER FISHERY EFFORT

=== Legal —e— Sublegal
= —-
2000 2001

Legal CPUE
N

=e

Balen |

4
Es 2003

Legal CPUE
(e)

Legal CPUE

2006 2007

Legal CPUE
NO

| Lat

Legal CPUE
N

3 Ne t t
a |
Boon! Peelen

Oct Nov Dec Jan Feb Mar Oct Nov Dec

Month of season

Jan Feb Mar

8

6

4

2

ANd9 le6e|qNS 3Ndd je6e\qng ANdd le6sjqns 4Ndd je6e\qng

ANd9d jebejqns

173

Fig. 6. The legal-sized and sublegal-size California spiny lobster catch per unit effort (CPUE: count/
trap) as reported via the California Department of Fish and Game-required commercial fishing logbook

during each of the 2000-2009 commercial fishing seasons.

174 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Sublegal CPUE

0.0 02°04 06 08 1,00 mp2zaee
Legal CPUE

Fig. 7. Scatterplot and linear regression comparing the sublegal and legal lobster CPUEs recorded in
fishing blocks 737, 738, and 757 off the Laguna Beach area, 2000-2009. The best-fit regression is drawn
(R? = 0.65).

no subtidal habitat assessments were conducted during this study, the spatial distribution
of giant kelp canopy can act as a proxy for hard substrate given giant kelp’s general
ecological need for hard substrate to anchor its holdfast (Dayton 1985). Furthermore, the
significant correlations observed during each survey between the spatial distribution of
buoys and kelp canopy in light of the aforementioned substrate preferences of both giant
kelp and lobster was consistent with Parnell et al. (2007) who found lobsters, and fishing
effort, more commonly on rocky reefs offshore of La Jolla, California.

As noted previously, the commercial fleet in the area reduced effort when the CPUE
declined and therefore likely focused remaining effort on the most productive areas which
were often associated with above average kelp canopies. These patterns were evident in
the subsection buoy densities (Figure 2) and the significant correlations between these
densities and kelp canopy area. This is consistent with Parnell et al. (2007) and Parnell
et al. (2010) who found the most heavily fished areas were likely highly productive and
areas of preferred habitat. As the season progressed, with the exception of January 2009,
fishermen progressively abandoned the areas devoid of kelp canopy and increasingly
focused their efforts to areas covered to a varying extent by kelp canopy likely due to the
presence of submerged hard habitat. The comparatively elevated effort recorded near the
southeastern edge of the HPSMR, especially after the first month, suggests that once the
abundance of legal-sized individuals was greatly diminished in the areas available to
harvest effort, fishermen targeted the edge of the HPSMR where suitable habitat was
present as effort in subsection 11b consistently exceeded that in subsection 12 which
adjoins the northwest border of the HPSMR. Given lobsters execute nocturnal
migrations of up to 1500 m (Hovel and Lowe 2007), it is likely that these migrations
potentially exposed them to fishery resources deployed near the reserve boundary similar
to that reported by Goni et al. (2006). This is consistent with fishing effort patterns in
similar studies of lobster commercial effort near no-take reserves in southern California,
specifically focused effort at reserve boundaries (Parnell et al. 2007; Parnell et al. 2010).

ORANGE COUNTY COMMERCIAL LOBSTER FISHERY EFFORT 175

This documented commercial effort in relation to existing no-take marine reserves will
likely become more relevant as new MPAs, some of which are no-take reserves, are
implemented in southern California*. The pending MPA complex in our study area will
encompass two of the three most productive sites currently exploited by the commercial
fishery, specifically subsections 9 and 11b. This new MPA complex will likely be of
sufficient size to allow some individual lobster movement within its borders without being
exposed to fishing at the boundary. It will not, however, include the areas of greatest kelp
canopy coverage, which will remain open to fishing. Based on the observations near the
HPSMR and near the La Jolla Ecological Reserve (Parnell et al. 2007), we anticipate a
significant effort along the MPA complex edge. If legal-sized lobster from within the
MPA complex are exported out of the no-take area (via migration, density-dependent
factors, etc.) as has been described for other spiny lobster species receiving MPA
protection (Goni et al. 2006), then these adjacent areas may become the most productive
assuming suitable habitat is present.

Over the 10 commercial seasons studied, the lobster fishery along the southern Orange
County coastline began with generally steady catches, excluding 2004, but quickly
declined with time likely due to a lack of harvestable individuals as time passed.
Surprisingly, sublegal-sized individuals declined at a rate similar to that of the harvestable
stock in the Laguna area (Figures 6 and 7). Reasons for this decline are outside the scope
of this study, and warrant further examination, but did not appreciably impact the next
season's fishery as no significant differences were detected between the October CPUEs in
9 out of 10 seasons. These simultaneous declines and apparent non-impact on the
following season superficially resembles what would be expected given the documented
behavior of other spiny lobster species (Panulirus, Jasus). Specifically, a potential
explanation includes a mass migration wherein all lobster size classes were observed to
move from shallow spawning habitat into deeper waters (Kanciruk and Herrnkind 1978
and references therein; MacDiarmid 1991). Data reported by Parnell et al. (2007) was
consistent with this as they documented a shift in effort to deeper waters during the
middle of the season off La Jolla, although the total number of traps set was greatly
reduced. This spatial shift in effort, small as it was, may be a fishermen adaptation to the
offshore migration and consistent with that described by Kanciruk and Herrnkind (1978).
Work by Hovel and Lowe (2007) confirmed movement by individual animals, but further
research on the seasonal movements is needed to verify the potential similarities between
the California spiny lobster and those from the Atlantic and Southern Pacific.
Interestingly, Kanciruk and Herrnkind (1978) also reported that the migrating lobsters
were typically smaller in size and more frequently sexually-inactive in comparison to
those found at shallower depths prior to the migration beginning. Overall, these data
suggest that the commercial California spiny lobster fishery in the vicinity of Laguna
Beach, California is likely sustainable at this time under the present level of effort.

Acknowledgements

This work was supported by the County of Orange through the Orange County Marine
Protected Area Council. We would like to thank the Council members for their
comments on earlier drafts. This work greatly benefitted from discussions with and
comments by K. Barsky, D.S. Beck, and C.T. Mitchell. We would also like to thank K.
Barsky and the California Department of Fish and Game for supplying the commercial
catch data. Discussions with E. Parnell greatly improved this manuscript. Comments by
two anonymous reviewers significantly improved this manuscript.

176 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Literature Cited

Barsky, K.C. 2001. California spiny lobster. In California’s Living Marine Resources: A Status Report,
(W.S. Leet, C.M. Dewees, R. Klingbeil, and E.J. Larson, eds.), 98-100. UC Agri. Nat. Res. Publ.
SGOI-11.

California Department of Fish and Game (CDFG). 2008. Review of Some California Fisheries for 2007:

Coastal Pelagic Finfish, Market Squid, Dungeness Crab, California Spiny Lobster, Highly

Migratory Species, Ocean Salmon, Groundfish, California Halibut, Hagfish, Pacific Herring, and

Recreational. CalCOFI Rep., 49:15—38.

. 201 1a. Digest of California Commercial Fishing Laws & License Requirements, 2011-2012. Calif.

Dept. Fish Game, Pp. 55-56.

Dayton, P.K. 1985. Ecology of kelp communities. Ann. Rev. Ecol. Syst., 16:215—245.

Goni, R., A. Quetglas, and O. Refiones. 2006. Spillover of spiny lobsters Palinurus elephas from a marine
reserve to an adjoining fishery. Mar. Ecol. Progr. Ser., 308:207-219.

Hovel, K.H. and C. Lowe. 2007. Shelter use, movement, and home range of spiny lobsters in San Diego
County. Calif. Sea Grant Tech. Rep. — R/MLPA-04.

Kanciruk, P. and W. Herrkind. 1978. Mass migration of spiny lobster, Panulirus argus (Crustacea:
Palinuridae): behavior and environmental correlates. Bull. Mar. Sci., 28:601—623.

MacDiarmid, A.B. 1991. Seasonal changes in depth distribution, sex ratio and size frequency of spiny
lobster Jasus edwardsi on a coastal reef in northern New Zealand. Mar. Ecol. Progr. Ser., 70:
129-141.

McArdle, D. 1997. California Marine Protected Areas. Sea Grant Publ. T-039., Pp. 204-231.

Mitchell, C.T., C.H. Turner, and A.R. Strachan. 1969. Observations on the biology and behavior of the
California spiny lobster, Panulirus interruptus (Randall). Calif. Fish Game, 55:121—131.

Parnell, P.E., P-.K. Dayton, R.A. Fisher, C.C. Loarie, and R.D. Darrow. 2010. Spatial patterns of fishing
effort off San Diego: implications for zonal management and ecosystem function. Ecol. Appl., 20:
2203-2222.

, and F. Margiotta. 2007. Spatial and temporal patterns of lobster trap fishing: a survey of

fishing eflent and habitat structure. Bull. South. Calif. Acad. Sci., 106:27—37.

Bull. Southern California Acad. Sci.
110(3), 2011, pp. 177-183
© Southern California Academy of Sciences, 2011

A New Species Of Late Cretaceous (Gampanian) Cypraeid
Gastropod, Santa Ana Mountains, Southern California and New
Records of California Cretaceous Cypraeids

Lindsey T. Groves,' Harry F. Filkorn,* and John M. Alderson’

‘Natural History Museum of Los Angeles County, Malacology Section, 900 Exposition
Boulevard, Los Angeles, CA 90007, lgroves@nhm. org
*Los Angeles Pierce College, Physics and Planetary Sciences Department, 6201
Winnetka Avenue, Woodland Hills, CA 91371, filkornh@piercecollege. edu
>Natural History Museum of Los Angeles County, Invertebrate Paleontology Section,
900 Exposition Boulevard, Los Angeles, CA 90007, jjalderson@live.com

Abstract.—A new species of Cypraeidae is described from the middle Campanian
(Late Cretaceous) portion of the Schulz Ranch Member of the Williams Formation,
Santa Ana Mountains, Orange County, southern California. This is the first
cypraeid described from the Williams Formation and only the second cypraeid
species described from the Santa Ana Mountains. New paleogeographic and
chronologic records of previously described and indeterminate Cretaceous cypraeid
species are also listed.

Introduction

Cretaceous cypraeids are uncommon in North American strata and comprise 17
previously described species (Groves, 1990; 1994; 2004). Of these 17 species, seven are in
the genus Palaeocypraea, four are in the genus Bernaya s.s., and six are in the genus/
subgenus Bernaya (Protocypraea). A new species of Bernaya (Protocypraea) 1s
described from the Upper Cretaceous (middle Campanian) Schulz Ranch Member of
the Williams Formation, Santa Ana Mountains, Orange County, southern California.
This is the first cypraeid species described from the Williams Formation, which brings
the North American total to 18. Of these 18 species 12 are from western North America
(Table 1).

Stratigraphy and Geologic Age

Popenoe (1937) informally introduced the Schulz member of the Williams Formation
as part of a “generalized section of formations in the Santa Ana Mountains,
California.” The Schulz Member of the Williams Formation of Popenoe (1942) was
formally described for outcrops of Late Cretaceous age approximately 0.402 km
(0.25 mile) upstream from the mouth of Williams Canyon, near the western boundary of
the Schulz Ranch, Santa Ana Mountains, Orange County, California. The member was
composed predominantly of coarse-grained, light-colored, cross-bedded arkosic
sandstone and minor boulder beds. To eliminate confusion with the Schulz Member
of the Talpa Formation of Permian age in Coleman County, Texas, Woodring and
Popenoe (1945) revised the name to the Schulz Ranch Member of the Williams
Formation.

The new species was collected from a conglomeratic sandstone bed from the basal 4.5—
6.0 m (15-20 ft.) of the Schulz Ranch Member above a disconformable contact with the

7

178 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 1. Updated list of Cretaceous cypraeid species from North America and their generalized
localities (formation is included for the new species).

PALAEOCYPRAEA

Early Cretaceous
Palaeocypraea fontana (Anderson, 1958) [Shasta Co. California]

Late Cretaceous

Palaeocypraea corsicana (Stephenson, 1948) [Navarro Co., Texas]

. grooti (Richards and Shapiro, 1963) [New Castle Co., Delaware]
. nuciformis (Stephenson, 1941) [Navarro Co., Texas]

. squyeri (Campbell, 1893) [Dawson Co., Montana]

. suciensis (Whiteaves, 1895) [San Juan Co., Washington]

. wilfredi Groves, 2004 [Butte Co., California]

ash as) Ss) ach 2s

BERNAYA s.s and BERNAYA (PROTOCYPRAEA)

Late Cretaceous

Bernaya ( Bernaya) beardi Groves, 2004 [Vancouver Id., British Columbia]
. (B.) burlingtonensis (Schilder, 1932) [Burlington Co., New Jersey]
(B.) crawfordcatei Groves, 1990 [San Diego Co., California]

(B.) jeanae Groves, 2004 [Butte Co., California]

(Protocypraea) argonautica (Anderson, 1958) [Jackson Co., Oregon]
(P.) berryessae (Anderson, 1958) [Yolo Co., California]

(P.) gualalaensis (Anderson, 1958) [Mendocino Co, California]

(P.) louellasaulae new species [Williams Fm., Orange Co., California]
(P.) mississippiensis Groves, 1990 [Lee Co., Mississippi]

. (P.) popenoei Groves, 2004 [Orange Co., California]

. (P.) rineyi Groves, 1990 [San Diego Co., California]

mt th bh

underlying Holz Shale Member of the Ladd Formation. Filkorn (2005) reported the first
occurrence of the hippuritid rudist bivalve Barrettia sparcilirata Whitfield, 1897 from the
Upper Cretaceous of the North American west coast along with the more widely
distributed caprinid rudist Coralliochama orcutti White, 1885, from the locality. He
further reported in 2007 that the fauna also included fragments of an undetermined
species of radiolitid rudist. Additional bivalve genera and species at the locality include
Calva, Crassatella, Cucullaea, Glycymerita veatchii (Gabb, 1864), Indogrammatodon, Opis
rosarioensis Anderson and Hanna, 1935, Pterotrigonia, and Spondylus. Gastropod genera
and species include Ampullina?, Bernaya (Protocypraea) sp., cf. B. (P.) popenoei Groves,
2004, Biplica, Pentzia, Volutoderma santana Packard, 1922, and an undetermined
cerithiid. One paratype of Prisconatica hesperia Squires and Saul, 2004, LACMIP 8128, is
from LACMIP locality 27199, which is equivalent to the new cypraeid locality LACMIP
17761. It was thought that the specimen represents reworked material from the
underlying upper part of the lower Campanian Holz Shale Member of the Ladd
Formation (Squires and Saul, 2004). Non-molluscan biota includes several species of
colonial scleractinian corals and the calcareous alga Archaeolithothamnium sp. Despite
containing rip-up clasts from the underlying Holz Shale Member of the Ladd Formation,
fossils in the conglomeratic sandstone were mostly unabraded and well-preserved with
original shell material. This unabraded condition indicated that they were not reworked
and likely only transported a short distance, possibly by a storm surge. Squires and Saul
(2009) indicated the stratigraphical range of the bivalve Opis rosarioensis Anderson and
Hanna, 1935, found here and elsewhere in the Schulz Ranch Member of the Williams
Formation, to be lower middle Campanian.

NEW CRETACEOUS CYPRAEID 179

Abbreviations

Abbreviations used for institutional specimen and locality numbers are: CAS, California
Academy of Sciences, San Francisco; LACMIP, Natural History Museum of Los Angeles
County, Invertebrate Paleontology Section; SC, Sierra College, Rocklin, California; SU,
Stanford University, Palo Alto, California [collections now housed at CAS]; UCLA,
University of California, Los Angeles [collections now housed at LACMIP].

Measurement parameters were defined as: length = greatest distance between anterior
and posterior ends; width = greatest distance between lateral margins; and height =
greatest distance between base and dorsum.

Systematic Paleontology

The classification used here follows that of Schilder and Schilder (1971).

Superfamily Cypraeoidea Rafinesque, 1815
Family Cypraeidae Rafinesque, 1815
Subfamily Bernayinae Schilder, 1927

Tribe Bernayini Schilder, 1927
Genus Bernaya Jousseaume, 1884

Type Species: Cypraea media Deshayes, 1835, by original designation. Upper middle
Eocene (Bartonian Stage), Auvers-sur-Oise, Val-d’Oise (northwest of Paris), France.

Diagnosis: Shell small to large size; anterior end weakly carinate; dorsum smooth; spire
of medium height and partially exposed; aperture wide, sides rounded; anterior and
posterior canals deep; fossula smooth, concave, wide.

Remarks: Schilder and Schilder (1971) recognized five species and two subspecies of
worldwide Cretaceous Bernaya s. s., and all seven were recognized as full species by
Groves (1994). Subsequent to Schilder and Schilder (1971), Yu and Zhu (1983) described
a single new species, and Groves (1990, 2004) described three additional species.
Although these studies raised the present total to 11 species, only three of the species are
from western North America. Groves (2004) documented a poorly preserved specimen of
B. (B.) crawfordcatei Groves, 1990, from the Campanian Pleasants Sandstone Member
of the Williams Formation, the only known Bernaya s. s. from the Santa Ana Mountains.

Subgenus Protocypraea Schilder, 1927

Type Species: Eocypraea orbignyana Vredenburg, 1920, by original designation. Upper
Cretaceous (Turonian through Santonian), Trichinopoly Group, Kullygoody, southern
India.

Diagnosis: Shell small to large size; moderately pyriform shape, constricted anteriorly;
fossula smooth, concave, wide.

Remarks: Schilder and Schilder (1971) recognized eight species and seven subspecies of
Cretaceous Bernaya (Protocypraea) and all of their subspecies were elevated to specific
level by Groves (1994). Subsequent to Schilder and Schilder (1971), three species were
described by Groves (1990 and 2004), and another new species is described here. This
raises the present tutal to 19 species, five of which are from western North America.
Groves (2004) described Bernaya (Protocypraea) popenoei from the lower Campanian
Holz Shale Member of the Ladd Formation, the only species of Bernaya ( Protocypraea)
previously known from the Santa Ana Mountains.

180 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Explanation of Figures 1-4. Cretaceous cypraeids from the Santa Ana Mountains: Fig. 1 - Bernaya
(Protocypraea) louellasaulae new species, holotype LACMIP 13720, from LACMIP loc. 17761, dorsal view
(< 3.7). Fig. 2 — ventral view of same specimen. Fig. 3 - Bernaya ( Protocypraea) sp., cf. B. (P.) popenoei
Groves, 2004, hypotype LACMIP 13893, from LACMIP loc. 17761, dorsal view (X 3.6). Fig. 4 — ventral
view of same specimen.

Bernaya (Protocypraea) louellasaulae new species
(Figs. 1-2)

Diagnosis: Bernaya of medium size, anterior and posterior canals deep, spire of
medium height, fossula concave, and smooth posterior terminal ridges extend to margins.

Description: Shell of small to medium size, constricted anteriorly; maximum height of
shell nearly centered; maximum width of shell slightly posterior of center; dentition
coarse to medium with smooth interstices; columellar lip with 11 teeth, labral lip with 15
teeth: aperture fairly wide and straight, curved posteriorly toward columella, widens
anteriorly; terminal canals deep; columella slightly inflated; prominent anterior terminal
ridges form a slight marginal callus; posterior terminal ridge extended from base of spire
to form a slight marginal callus; spire of medium height and partially exposed due to shell
loss.

NEW CRETACEOUS CYPRAEID 181

Comparison: The new species resembles Bernaya ( Protocypraea) veraghoorensis (Stoliczka,
1867) from the Upper Cretaceous (Campanian) Arrialoor Group, near Veraghoor,
Tamilnadu District, India, particularly the specimen figured by Stoliczka (1868: pl. 4,
fig. 4) [as Cypraea (Luponia) carnatica]. In contrast, the new species is less inflated,
more constricted anteriorly, and has a narrower and less sinuous aperture than B. (P.)
veraghoorensis.

Discussion: Generic and subgeneric assignment are based on the wide aperture, deep
anterior and posterior canals, and medium-height spire. Bernaya (Protocypraea)
louellasaulae represents the first cypraeid described from the Williams Formation.

Type Material: Holotype, LACMIP 13720. A single fairly well-preserved specimen
with minor amounts of apparent original shell material on the base and lateral margins.
The specimen measures 17.2 mm in length, 10.8 mm in width, and 9.3 mm in height.

Type Locality: LACMIP loc. 17761, Schulz Ranch Member of Williams Formation,
near 533 m (1750 ft.) elevation at bottom of eastern tributary to Fremont Canyon, Santa
Ana Mountains, Orange County, California. Collectors: John M. Alderson and Harry F.
Filkorn, 4 April, 2004.

Etymology: This species is named for LouElla R. Saul (LACMIP, Research Associate)
for her numerous important contributions to the paleontology of the western United
States.

Additional Records of California Cretaceous Cypraeids
Bernaya (Protocypraea) sp., cf. B. (P.) popenoei Groves, 2004
(Figs. 3-4)

New Record: Hypotype, LACMIP 13893, LACMIP loc. 17761 (see locality description
above), Upper Cretaceous Schulz Ranch Member, Williams Formation, collected by
John M. Alderson and Harry F. Filkorn, 4 April, 2004. This record is based on a single
fairly well-preserved internal mold, that is 25.5 mm in length, 17.7 mm in width, and
13.2 mm in height.

Distribution: This species was formerly restricted to the lower Campanian part of the

Holz Shale Member of the Ladd Formation and is here extended upward to the lower
middle Campanian part of the Schulz Ranch Member of the Williams Formation.

Bernaya? sp.
New Record: SC MG153, Granite Bay, Treelake Village Estate, northeast of Sacramento,
Placer County, California. Upper Cretaceous (Campanian), Chico Formation. Poorly

preserved internal mold. Collected by Richard P. Hilton (SC) during paleontological
monitoring for land development in 1999.

Cypraeidae, undetermined genus and species

New Record: CAS 69097.03 (ex SU 30286), Dip Creek, San Luis Obispo County,
California. Uppermost Cretaceous/lowermost Paleocene Dip Creek Formation. A single
poorly preserved internal mold. Collected by Nicolas L. Taliaferro, date unknown.

Acknowledgments

We thank Richard L. Squires (California State University, Northridge, Department
of Geological Sciences) who critically reviewed an early draft of the manuscript and
made helpful suggestions. LouElla R. Saul (LACMIP) generously assisted with the

182 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

identifications of specimens from LACMIP loc. 17761. Cathy L. Groves (LACM, Echino-
derms Section) and Brian Koehler (formerly LACM, Entomology Section) are thanked
for their input in composing the figures. The critiques of LouElla Saul (LACMIP)
and Steffen Kiel (University of Gottingen, Paleobiology Group, Germany) are greatly
appreciated.

Literature Cited

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Campbell, J.H. 1893. Description of a new fossil Cypraea. The Nautilus, 7(5):52.

Filkorn, H.F. 2005. First report of Praebarettia sparcilirata (Whitfield, 1897) from the Late Cretaceous

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Scott, eds.), Society for Sedimentary Geology (SEPM) volume, 30-31.

. 2007. Relict of a lost Pacific Coast: Late Cretaceous (Campanian) reef fauna from the Black Star

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Schilder, F.A. 1927. Revision der Cypraeacea (Moll., Gastr.). Arch. Naturges., 91A(10): 1-171.

. 1932. Cypraeacea. In: W. Quenstedt (ed.), Fossilium Catalogus, I Animalia, pt. 55. W. Junk:

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Appendix 1.

Localities Cited

CAS 69097. Dip Creek, NE % sec. 30, T25N, RIOE, U.S. Geological Survey Adelaida 7.5’ quadrangle,
San Luis Obispo Co.. California. Uppermost Cretaceous/lowermost Paleocene. Dip Creek Formation (?).
Collector: Nicolas L. Taliaferro, date unknown.

LACMIP loc. 17761. Float blocks of conglomeratic sandstone from basal 4.5—-6.0 m (15-20 ft) of
member, near 533 m (1750 ft.) elevation at bottom of eastern tributary to Fremont Canyon, center of SW
Ys SW 4 sec. 7, T4S, R7TW, U.S. Geological Survey Black Star Canyon 7.5’quadrangle (1967 [PR 1973)).
eastern Santa Ana Mountains, Orange County, California. Upper Cretaceous (lower middle Campanian).
Schulz Ranch Member, Williams Formation. Collectors: John M. Alderson and Harry F. Filkorn, 4 April.
2004 and 4 April, 2005. This locality is equivalent to LACMIP loc. 27199 (= UCLA 7199) collected by
Willis P. Popenoe and J.E. Schoellhammer in 1951.

SC MGI153. Granite Bay, Treelake Village Estate, NE % sec. 16, TION, R7E. U.S. Geological Survey

7.5’ Folsom quadrangle (1967 [PR1975]), northeast of Sacramento, Placer Co., California. Upper
Cretaceous (Campanian), Chico Formation. Collector: Richard P. Hilton, 1999.

Bull. Southern California Acad. Sci.
110(3), 2011, pp. 184-188
© Southern California Academy of Sciences, 2011

Southern occurrence of the sand sole (Psettichthys melanostictus).

Robert H. Moore,’ Eric F. Miller,'* and Milton Love?

'MBC Applied Environmental Sciences, 3000 Red Hill Ave., Costa Mesa, CA 92626
°Marine Science Institute, University of California, Santa Barbara, CA 93106

The geographic and depth ranges of marine fishes commonly reflect their physiological
preferences (Portner et al., 2010). Given the wide availability of habitats along the
California coastline, biogeographic range extensions of many species have been observed
to occur periodically, most frequently during periods of short-term oceanographic
temperature fluctuation. Over the last 30 years, these range extensions in California have
mostly been poleward expansions as ocean temperatures have warmed or through large-
scale oceanographic anomalies such as Californian-El Nino conditions (Lea and
Rosenblatt, 2000). Many of the recently documented range extensions in southern
California have been associated with thermal power plant cooling water intakes or
discharges, often due to the increased sampling and/or the presence of greater-than-
ambient water temperatures near the discharges (Pondella, 1997; Lea and Rosenblatt,
2000; Miller and Curtis, 2008). In addition to the thermal discharge, the cooling water
system entrains material, including fishes, with the cooling water drawn into the system.
The cooling water is filtered through traveling screens with a nominal square mesh of
10-mm to prevent debris from passing farther into the system and potentially clogging
downstream condensers. Fish impingement upon these traveling screens is routinely
monitored to provide a representative accounting of the fishes taken in by the cooling
water system, and an opportunity to collect random tourist species.

Sand sole (Psettichthys melanostictus) reportedly ranges from the Southeastern Bering
Sea, Alaska to Newport Beach, California in depths ranging from the intertidal zone out
to 325 m (Love et al., 2005). Museum records contain numerous specimens taken in
northern California with only three lots collected offshore of Ventura County, California
at the southernmost extent (Fishnet2 2011). Surprisingly, no records were found for
collections in the Santa Barbara, California area despite substantial areas of suitable
habitat. Reviews of the Santa Barbara Natural History Museum (SBNHM 2011)
ichthyology records found no sand soles in the collection. Fitch and Schultz (1978)
detailed two fish taken in the southern Santa Monica Bay in the mid-1970s during
impingement sampling at Scattergood Generating Station in El Segundo, California and
the Redondo Beach Generating Station in Redondo Beach, California. The Redondo
Beach sample had set the southern range limit for this species at the time. Slightly farther
southwards, several sand sole were caught by recreational anglers fishing off the Balboa
Pier during the 1980s (M. Love, unpubl. data), which had served as the impetus for the
current southern range endpoint. One collection that has gone largely unreported is
recorded in the Museum of Comparative Zoology (MCZ 2011) as collected in San Diego
County, California during the mid-1800s (Lot 25988) and has not been previously
included in the biogeographic distribution of the sand sole (Love et al., 2005; Horn et al.,
2006). This sample, however, has limited information regarding its collection. Careful

*Corresponding author: emiller@mbcnet.net

184

SAND SOLE SOUTHERN OCCURRENCE 185

Fig. 1. Photo of a sand sole collected at the San Onofre Nuclear Generating Station near San
Clemente, California on March 22, 2011. The specimen measured 235 mm SL and weighed 212 g.

review of the available record indicates the sample is now missing and was originally
held in a jar with other lots collected near San Francisco, California (Lots 11197
and 11559) that each contain extensive collection information. The status of this San
Diego record raises concerns as to its validity given the lack of collection information,
unknown present status of the specimen, and its historic storage with San Francisco
collections.

While these records hardly represent its population size in the area, it does signify the
rarity of its occurrence in the Southern California Bight. A demersal species, it has yet to
be taken in either of the four completed summer regional otter trawl surveys conducted
by the Southern California Coastal Water Research Project (E. F. Miller, pers. obs.) or in
various otter trawl monitoring surveys conducted on a near annual basis since 1972
throughout portions of the Southern California Bight in support of regulated discharge
monitoring (Stull and Tang, 1996).

The San Onofre Nuclear Generating Station Unit 2 withdraws seawater through an
open-water intake located 950 m offshore along the 10-m isobath at 33° 21.633’N, 117°
33.743’W. On March 22, 2011, R.H. Moore collected a 235-mm SL sand sole that
weighed 212 g (Figure 1) during an impingement survey. The identification was made
based on the occurrence of five free dorsal rays, consistent with the diagnostic features
described by Miller and Lea (1976) and confirmed with local taxonomic experts (H.J.
Walker, pers. comm.”; R.N. Lea, pers. comm.?; M.L. Love). This specimen has been
deposited with the Scripps Institution of Oceanography Marine Vertebrate Collection
with catalog number SIO 11-74.

We note that the San Onofre fish represents the most southerly physical collection
of this species. However, on 3 September 2009, a specimen was photographed in situ in
the La Jolla Shores area (at about 32° 51.3’N, 117° 15.2'W) at a depth of about 20 m
by David Andrews (Figure 2). The identity of this specimen was confirmed by M.L.
Love based on the dorsal fin ray separation. Thus the documented range of the sand

°H.J. Walker, Jr. Collection Manager, Scripps Institution of Oceanography Marine Vertebrates
Collection
>R.N. Lea, California Department of Fish and Game, Retired.

186 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Fig. 2. Image of sand sole observed in the La Jolla Shores, California area at a depth of ~ 20 m taken
on September 3, 2009 by D. Andrews with the identity confirmed by M. L. Love.

sole has been extended/reconfirmed southwards approximately 105 km from Newport
Beach to La Jolla Shores, California. This may represent the second record from the
San Diego County, California area separated by over 100 years if the aforementioned
mid-1800s specimen catalogued in the Museum of Comparative Zoology is considered,
but, again, the earlier sample is unconfirmed and questionable given the caveats
detailed above.

Recent southern extensions or occurrences have been noted less frequently given the
recent poleward trend in biogeographic shifts (Lea and Rosenblatt, 2000; Perry et al.,
2005; Harley et al., 2006), but the recent decline in seawater temperatures (Figure 3) may
have made southern extensions, such as this, physiologically possible. Mean annual
sea surface temperatures (SST) recorded at the San Clemente Pier in San Clemente,
California, approximately 8 km northwest of the San Onofre Nuclear Generating Station,
through September 30, 2010 were the third coolest since 1990 and the 16" coolest since
1966 (UCSD 2011). With the exception of 2004 and 2009, the mean annual SST since
2000 at San Clemente has remained below 17.5°C after generally exceeding this for the
prior 17 years. If oceanographic conditions continue as they have persisted for the recent
five years, it is expected that additional southern range extensions will be recorded.

Acknowledgements

We would like to thank Southern California Edison and the San Onofre Nuclear
Generating Station for their support of the impingement monitoring program.

SAND SOLE SOUTHERN OCCURRENCE 187

18.5

18.0

AS

17.0

SST °C

16.5
16.0
3s

15.0

1970 1980 1990 2000 2010

Year

Fig. 3. Mean daily sea surface temperature (°C) recorded at the San Clemente Pier, San Clemente,
California, approximately 8 km northwest of the San Onofre Nuclear Generating Station, January 1, 1966
— September 30, 2010.

Additional gratitude is extended to H.J. Walker, Jr. and R.N. Lea for their assistance
with confirming the identification. R. Feeney provided invaluable assistance in our search
for museum collections. The comments of two anonymous reviewers and extensive
discussion with R.N. Lea substantially improved this manuscript.

Literature Cited

FishNet2. 201 lhttp://www.fishnet2.net/ accessed July 7, 2011.

Fitch, J. and S. Schultz. 1978. Some rare and unusual occurrences of fishes off California and Baja
California. Calif. Fish Game, 64:74-92.

Harley, C.D.G., A. Randall Hughes, K.M. Hultgren, B.G. Miner, C.J.B. Sorte, C.S. Thornber, L.F.
Rodriguez, L. Tomanek, and S.L. Williams. 2006. The impacts of climate change in coastal marine
systems. Ecol. Letters, 9:228—241.

Horn, M., L. Allen, R. Lea, and D. Pondella. 2006. Biogeography, in: (Allen, L.G., Pondella, I1.D., and
Horn, M.H.., eds.). The Ecology of Marine Fishes: California and Adjacent Waters. UC Press, Los
Angeles, CA. Pp. 3—25.

Lea, R.N. and R.H. Rosenblatt. 2000. Observations on fishes associated with the 1997-98 El Nino off
California. CalCOFI Rep., 41:117-129.

Love, M., C. Mecklenburg, T. Mecklenburg, and L. Thorsteinson. 2005. Fishes of the West Coast and
Alaska: a checklist of North Pacific and Artic Ocena species from Baja California to the Alaska-
Yukon border., US Dep. Interior. US Geological Survey, Biol. Res. Div. 288 pp.

Miller, E.F. and M.D. Curtis. 2008. First Occurrence of a Pacific Crevalle Jack, Caranx caninus, north of
San Diego, California. Bull. South. Calif. Acad. Sci., 107:41-43.

Museum of Comparative Zoology (MCZ). 2011. Online ichthyological collection database. http://
mezbase.mez.harvard.edu/SpecimenSearch.cfm. Accessed, September 15, 2011.

Perry, A.L., P.J. Low, J.R. Ellis, and J.D. Reynolds. 2005. Climate change and distribution shifts in
marine fishes. Science, 308:1912.

188 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Pondella, D. 1997. The first occurrence of the Panamic Sergeant Major, Abudefduf troschelii
(Pomacentridae), in California. Calif. Fish and Game, 83:84-86.

Portner, H., P. Schulte, C. Wood, and F. Schiemer. 2010. Niche dimensions in fishes: an integrative view.
Physiol. Biochem. Zool., 83:808—826.

Santa Barbara Natural History Museum (SBNHM). 2011. http://www.sbcollections.org/vz/search_simple.
php#sr. Accessed, September 21, 2011.

Stull, J.K. and C. Tang. 1996. Demersal fish trawls off Palos Verdes, southern California 1973-1993.
CalCOFI Rep., 37:211-240.

University of California, San Diego (UCSD). 2011. Shore station program. http://shorestation.ucsd.edu/
active/index_active.html. Accessed, July 7, 2011.

Bull. Southern California Acad. Sci.
110(3), 2011, pp. 189-192
© Southern California Academy of Sciences, 2011

Reproduction in the Great Basin Collared Lizard, Crotaphytus
bicinctores (Squamata: Crotaphytidae)

Stephen R. Goldberg! and Clark R. Mahrdt?

‘Whittier College, Department of Biology, Whittier, California 90608
°Department of Herpetology, San Diego Natural History Museum, San Diego,
California 92112

Abstract.—The reproductive cycle of the Great Basin Collared lizard, Crotaphytus
bicinctores was studied by a histological examination of museum specimens. Mean
clutch size (n = 13) was 3.46 + 1.1 SD, range: 2—6. Histological evidence indicates that
two clutches may be produced in the same year. The reproductive season includes
spring and early summer. There was a significant positive correlation between female
body size (SVL) and clutch size (P = 0.03). The smallest reproductively active male
and female C. bicinctores measured 81 mm and 78 mm SVL, respectively.

Crotaphytus bicinctores frequents xeric rocky habitat in southeastern and extreme
northeastern California, much of Nevada, western and northern Arizona, western and
central Utah, southeastern Oregon and western Idaho (McGuire 1996). Information on
its reproduction is limited and consists of reports of juveniles, gravid females and adult
males from southeastern California on 2 May (McGuire 1996): neonates observed in
eastern Oregon in August (Brooking 1934); mean clutch size of 5.38, (range: 3—7), egg
deposition in June in Millard County, Utah (Andre and MacMahon 1980). Ryan (2009)
reported clutch sizes of 3—7, the possibility of 2 clutches and hatchlings appearing in
August (Ryan 2009). The purpose of this paper is to examine the reproductive cycle of C.
bicinctores in the southern portion of this species range. Information on the reproductive
life history including period of sperm production, timing of yolk deposition and number
and sizes of clutches produced, provides critical information for formulating conservation
policies of lizard species populations. Due to the difficulty in justifying collections of
monthly lizard samples, utilization of museum collections for obtaining reproductive data
has become increasingly important.

A sample of 135 C. bicinctores consisting of 57 adult males (mean snout-vent length
[SVL] = 94.5 mm = 7.7 SD, range: 81-117 mm; 47 adult females (mean SVL = 88.5 mm
+ 5.9 SD, range: 78-98 mm); 31 subadults consisting of 15 males (mean SVL = 67.8 mm
+ 6.5 SD, range: 58-78 mm SVL) and16 females (mean SVL = 67.1 mm = 6.5 SD, range:
56-75 mm SVL) from Arizona (n = 5), California (n = 114), Nevada (n = 14) and Utah
(n = 2) was examined from the herpetology collection of the Natural History Museum of
Los Angeles County (LACM: Appendix 1). Lizards were collected from 1929-1980.

The left testis was removed from males and the left ovary was removed from females
for histological examination (Presnell and Schreibman 1997). Enlarged ovarian follicles
(> 5 mm) and/or oviductal eggs were counted. Tissues were embedded in paraffin,
sectioned at 5 um and stained with hematoxylin followed by eosin counterstain. Slides of
testes were examined to ascertain the stage of the testicular cycle. Slides of ovaries were

Cover Page Footnote: We thank Christine Thacker (LACM) for permission to examine specimens.

189

190 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 1. Monthly stages in the testicular cycle of 57 Crotaphytus bicinctores.

Month n Regression Recrudescence Spermiogenesis

March 5 1 D, 2)
April 18 1 5) 12
May 157, 1 4 12
June 9 l 0 8
July 4 1 1 D
August + - 0 0

examined to ascertain the stage of the ovarian cycle. Histology slides were deposited in
the herpetology collection of LACM. Mean SVL of male and female C. bicinctores were
compared using an unpaired f-test and the relationship between female SVL and clutch
size was examined using linear regression analysis (Instat vers. 3.0b, Graphpad Software,
San Diego, CA).

The mean SVL of males of C. bicinctores significantly exceeded that of females
(unpaired ¢ test, t = 4.4, df = 102, P < 0.0001). Monthly changes in the testicular cycle of
C. bicinctores are shown in Table 1. Three stages were present: (1) Regression, the
germinal epithelium is reduced to 1-3 cell layers in thickness and consists of
spermatogonia and Sertoli cells; (2) Recrudescence, a proliferation of germ cells for the
next period of sperm formation is underway. In early recrudescence, primary
spermatocytes predominate, whereas in late recrudescence, secondary spermatocytes
and spermatids are most abundant; (3) Spermiogenesis, lumina of the seminiferous
tubules are lined by clusters of sperm or metamorphosing spermatids. The period of
sperm production encompassed March to July. The smallest reproductively active
(spermiogenic) male of C. bicinctores (LACM 16870) measured 81 mm SVL, and was
collected May 1954 from Los Angeles County. Males < 81 mm SVL had not attained
reproductive maturity.

Monthly changes in the ovarian cycle of C. bicinctores are presented in Table 2. Four
stages were present in the ovarian cycle of C. bicinctores: (1) No yolk deposition
(quiescent); (2) Early yolk deposition with basophilic granules present in the ooplasm; (3)
Enlarged preovulatory follicles (> 4 mm); (4) Oviductal eggs. Gravid females were noted
April to June. Mean clutch size (n = 13) was 3.46 + 1.1 SD, range: 2-6. Linear regression
analysis revealed a significant positive correlation between female SVL (n = 13) and
clutch size (Y = —4.95 + 0.095X, r = 0.57, P = 0.04). A significant positive correlation
between female SVL and clutch size was also reported for C. bicinctores from Millard

Table 2. Monthly stages in the ovarian cycle of 47 Crotaphytus bicinctores, * = one female with
oviductal eggs and concurrent early yolk deposition for a second egg clutch; ** = some enlarged follicles in
one female were crushed not allowing clutch determination.

n Quiescent Early yolk deposition Enlarged follicles > 5mm _Oviductal eggs
April 8 6 | 0 1
May 23 9 8 4 2
June 6 0 0 hee ik
July a 3 0 0 0
August 6 5 l 0 0
October 1 | 0 0 0

REPRODUCTION CROTAPHAYTUS BICINCTORES 19]

County, Utah (Andre and MacMahon 1980). The smallest reproductively active female
(LACM 26840) measured 78 mm SVL, contained three oviductal eggs and was collected
June 1958 in Churchill County, Nevada. Females < 78 mm SVL had not attained
reproductive maturity. One female (LACM 16865) from Los Angeles County collected 14
June (SVL 93 mm) contained three oviductal eggs and concurrent early yolk deposition
for a subsequent clutch indicating select females may produce two clutches in the same
reproductive season. A single female collected in August exhibited early yolk deposition
(Table 2), but it is not known if she would have produced a clutch or if the follicles would
have undergone atresia. Follicular atresia is commonly observed near the close of the
reproductive season when follicles that did not complete vitellogenesis degenerate
(Goldberg 1973).

Andre and MacMahon (1980) reported a mean clutch size of 5.38, (range 3-7) for six
females from northern populations from Idaho and Utah. Fitch (1985) reported a mean
value of 5.0, range 3-8 for six northern C. bicinctores females from southern Idaho and
Millard and Tooele counties, Utah. Both values for northern C. bicinctores females were
greater than those of Fitch (1985) for seven females from southern populations in
California, Nevada and Utah (3.9, range 2-5), suggesting larger clutch sizes at higher
latitudes. The value provided by Fitch (1985) for southern populations approximates our
value (n = 13, 3.46 + 1.1 SD, range 2-6) reported herein. Whether the larger clutch sizes
in C. bicinctores from northern populations reflect a shorter activity season with fewer
females producing two clutches, warrants further study.

Other species of Crotaphytus exhibit similar reproductive life histories. Crotaphytus
vestigium exhibited a spring to early summer period of sperm production and ovarian
activity (Goldberg and Mahrdt 2010) as did Crotaphytus collaris (Fitch 1956, Trauth
1978, 1979). Two clutches were produced by C. collaris in Arkansas (Trauth 1978). Based
on anecdotal information such as time of egg deposition and appearance of hatchlings,
other species of Crotaphytus also appear to exhibit similar timing of events in their
breeding cycle, even though their reproduction has not been studied in detail. The report
of a gravid female of Crotraphytus grismeri from September (McGuire 1996) merits
further investigation. Detailed studies of the breeding cycles of C. antiquus, C. dickersonae,
C. grismeri, C. insularis and C. nebrius (see McGuire 1996, Grismer 2002, Babb 2009) are
needed to ascertain similarities in the timing of the reproductive cycles, and also to
determine if significant geographic variation in their clutch sizes exists.

Literature Cited

Andre, J.B. and J.A. MacMahon. 1980. Reproduction in three sympatric lizard species from west-central
Utah. Great Basin Naturalist, 40:68—72.

Babb, R.D. 2009. Sonoran collared lizard Crotaphytus nebrius Axtell and Montanucci, 1977. Pp. 108-111
In: (L.L.C. Jones and R.E. Lovich, eds.). Lizards of the American Southwest. A Photographic
Field Guide. Rio Nuevo Publ., Tucson, Arizona. 567 pp.

Brooking, W.J. 1934. Some reptiles and amphibians from Malheur County, in eastern Oregon. Copeia,
1934:93-95.

Fitch, H.S. 1956. An ecological study of the collared lizard (Crotaphytus collaris). Univ. Kansas, Mus.
Nat. Hist. Pub., 8:213-274.

. 1985. Variation in clutch and litter size in New World reptiles. Mus. Nat. Hist. Univ. Kansas,

Misc. Publ., 76:1—76.

Goldberg, S.R. 1973. Ovarian cycle of the western fence lizard, Sceloporus occidentalis. Herpetologica, 29:

284-289.

and C.R. Mahrdt. 2010. Reproduction in the Baja California collared lizard, Crotaphytus vestigium

(Squamata: Crotaphytidae). Bull. So. Calif. Acad. Sci., 109:153—156.

192 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Grismer, L.L. 2002. Amphibians and reptiles of Baja California including its Pacific Islands and the
islands in the Sea of Cortés. Univ. Calif. Press, Berkeley. 399 pp.

McGuire, J.A. 1996. Phylogenetic systematics of crotaphytid lizards (Reptilia: Iguania: Crotaphytidae).
Bull. Carnegie Mus. Nat. Hist., 32:1-143.

Presnell, J.K. and M.P. Schreibman. 1997. Humason’s Animal Tissue Techniques, 5" Ed.. The Johns
Hopkins University Press, Baltimore. 572 pp.

Ryan, M.J. 2009. Great Basin Collared Lizard Crotaphytus bicinctores Smith and Tanner, 1972. Pp.
100-103 In: (L.L.C. Jones and R.E. Lovich, eds.). Lizards of the American Southwest. A
Photographic Field Guide. Rio Nuevo Publ., Tucson, Arizona. 567 pp.

Trauth, S.E. 1978. Ovarian cycle of Crotaphytus collaris (Reptilia, Lacertilia, Iguanidae) from Arkansas

with emphasis on corpora albicantia, follicular atresia, and reproductive potential. J. Herpetol., 12:

461-470.

. 1979. Testicular cycle and timing of reproduction in the collared lizard (Crotaphytus collaris) in

Arkansas. Herpetologica, 35:184-192.

Appendix I

Crotaphytus bicinctores examined from the Natural History Museum of Los Angeles County (LACM)
by state and county: Arizona: Coconino 134075; Yuma 16892, 16893, 26835, 26836; California: Inyo
26824-26832, 36666, 36667, 36670, 52887, 122468, 123321—123325; Kern 63829-63835, 63837, 63838; Los
Angeles 3994-3996, 3998, 3999, 16865, 16867, 16870, 16872, 26811, 26812, 26814, 26815, 63188-63190,
94595-94600, 132436, 132437; Riverside 16876, 16885, 16888, 16889, 26820, 26822, 62448, 94601-94624,
94626; San Bernardino 16877, 16882, 16883, 21651, 23245, 26816-26819, 63179, 63180, 63184-63186,
64007, 94633-94638, 94641-94643, 94645-94648, 137887, 137890; Nevada: Churchill 26840-26843; Clark
76458, 107189 Lyon 26837, 26838; Mineral 126915; Nye 61454, 94658, 94659, 133205; Pershing 112790;
Utah: Washington 94678, 147476.

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CONTENTS

Discordant Phylogeographic and Biogeographic Breaks in California Halibut. Mat-
thew T. Craig, F. Joel Fodrie, Larry G. Allen, Laura A. Chartier, and Robert J.
Te na IPR EE cL INES 141

Abundance of the long-beaked common dolphin (Delphinus capensis) in California
and western Baja California waters estimated from a 2009 ship-based line-
transect survey. James V. Carretta, Susan J. Chivers, and Wayne L. Perryman. 152

Commercial fishery effort for California spiny lobster (Panulirus interruptus) off
Orange County, California before State Marine Reserve implementation. Eric
F. Miller, David G. Vilas, Jennifer L. Rankin, and David Pryor. 165

A new species of Late Cretaceous (Campanian) cypraeid gastropod, Santa Ana
Mountains, Southern California and new records of California Cretaceous cy-
praeids. Lindsey T. Groves, Harry F. Filkorn and John M. Alderson. ah

Southern occurrence of the sand sole (Psettichthys melanostictus). Robert H. Moore,
Eric F. Miller, and Milton Love 2220 184

Reproduction in the Great Basin Collared Lizard, Crotaphytus bicinctores (Squa-
mata: Crotaphytidae). Stephen R. Goldberg and Clark R. Mahrdt 189

Cover: Cretaceous cypraeids from the Santa Ana Mountains. Photo by L.T. Groves, reproduced by
permission.