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B RE VI O R A 



iVi HI s e 11 unn ol v^omnparaf ive /1/ooiogy 



us ISSN 0006-9698 



Cambridge, Mass. 



6 July 2011 



Number 525 



INTRASPECIFIC AND INTERSPECIFIC SPATIAL DISTRIBUTION OF THREE 

EASTERN NORTH PACIFIC CATSHARK SPECIES AND THEIR EGG CASES 

(CHONDRICHTHYES: SCYLIORHINIDAE) 

Brooke E. Flammang,' David A. Ebert, and Gregor M. Cailliet 

Abstract. Information on the distribution of three species of eastern North Pacific (ENP) catsharks (Apristurus 
brunneus, Apristurus kampae, and Parmaturus xaniurus) and their egg cases was previously unavailable despite being 
a species of interest for fisheries management evaluation and policy regulation. Data were generated from specimens 
collected by survey cruises from June 2001 through October 2004 between northern Washington to San Diego, 
California, U.S.A. and from known catch locations of specimens in museum collections. Longline catches consisted 
mainly of P. xaniurus, with occasional catch of gravid female A. brunneus. Conversely, trawl catches consisted mainly 
of Apristurus species. The three catshark species exhibited distinct differences in latitudinal and bathymetric range, 
albeit with partial overlap. Apristurus brunneus was typically found between 300 and 942 m along the entire area 
surveyed, while A. kampae always occurred >l,000-m depth and was not found north of 42°N. Parmaturus xaniurus 
was caught between 300- and 550-m depth between 40°N and 32°N. Egg cases of ^4. brunneus and P. xaniurus were 
collected in trawl surveys and observed in video footage taken by remotely operated vehicle. These egg cases were 
located in specific sites on areas of high vertical relief at 300- to 500-m depth. Nursery grounds, which were 
previously unknown for these catshark species, were described within the Monterey Bay Canyon and along the 
California coastline were identified on the basis of recurrence and specificity of oviposition. This paper describes the 
range of A. brunneus, A. kampae, and P. xaniurus in the ENP, detailing latitudinal, bathymetric, sexual, and 
ontogenetic intra- and interspecific segregation patterns. 

Key words: separation; nursery grounds; maturity; Apristurus brunneus; Apristurus kampae; Parmaturus xaniurus 



Pacific Shark Research Center, Moss Landing Marine 

Laboratories, 8272 Moss Landing Road, Moss Landing, 

California 95039, U.S.A. e-mail: bflammang@post.harvard. 

edu 

' Current address: Museum of Comparative Zoology, 

Harvard University, 26 Oxford Street, Cambridge, 

Massachusetts 02138. 



INTRODUCTION 

Three species of deep-sea catsharks (Chon- 
drichthyes: Scyliorhinidae) inhabit the upper 
continental slope habitats of the eastern 
North Pacific (ENP): brown catshark, Apris- 
turus brunneus (Gilbert 1892), white-edge 
catshark, Apristurus kampae Taylor 1972, 



The President and Fellows of Harvard College 201 1. 



BREVIORA 



No. 525 



and filetail catshark, Parmaturus xaniurus 
(Gilbert 1892). Although localized studies of 
these species have identified some areas 
where they are found (DeLacy and Chap- 
man, 1935; Roedel, 1951; Lee, 1969; Taylor, 
1972; Jones and Geen, 1977; Cross, 1988; 
Balart et ah, 2000; Ebert, 2003), the complete 
range of distribution for any of these three 
species is unknown. Understanding of the 
distribution of these catsharks is needed 
because they are often incidentally caught 
in commercial fishing (Rogers and Ellis, 
2000; Ebert, 2003; Flammang et al, 2008) 
and insufficient information is available to 
make evaluations for fisheries management. 
Also, distribution patterns of adults and 
juveniles, including patterns of sexual segre- 
gation, reveal important information about 
the Hfe history of sharks. Many species of 
sharks are known to segregate by size, sex, or 
species to reduce intra- and interspecific 
predation and competition (Springer, 1967; 
Carrasson et al, 1992; Morrissey and Gru- 
ber, 1993; Platell, 1998; Cortes, 2000). 

Encased catsharks are particularly vulner- 
able to interspecific predation because em- 
bryonic development may last up to 2 years 
in an egg case without parental input or care 
(Flammang et al, 2007). Predation on egg 
cases is not uncommon (Grover, 1972; Cox 
and Koob, 1993; Long, 1996; Barrull and 
Mate, 2001; Bor and Santos, 2003), and 
nursery grounds are a strategy by which the 
vulnerability of individual egg cases can be 
reduced by being part of an aggregate. Free- 
swimming juveniles utilize the midwater as a 
nursery away from larger conspecifics (Lee, 
1969; Cross, 1988), but there is no informa- 
tion on egg case nursery locations. This 
paucity of information is due primarily to the 
rarity of reports of viable egg cases being 
caught with fishing gear or by in situ 
observations. 

The objective of this research was to use 
fishery-independent surveys, designed to re- 



duce sampling bias and reporting error, to 
describe the distribution of A. brunneus, A. 
kampae, and P. xaniurus in the ENP, detailing 
latitudinal, bathymetric, sexual, and size 
intraspecific and interspecific segregation pat- 
terns. In addition, we report the distribution 
of egg cases of A. brunneus and P. xaniurus. 

MATERIALS AND METHODS 

Description of surveys 

The National Oceanographic and Atmo- 
spheric Administration (NOAA) Fisheries 
Service Northwest Fisheries Science Center 
(NWFSC) laboratories in Newport, Oregon 
and Seattle, Washington provided catshark 
samples from their annual slope and shelf 
Fisheries Resource Analysis and Monitoring 
(FRAM) cruise surveys. These fishery-inde- 
pendent bottom-trawl studies were conduct- 
ed from 2001 to 2004 during the months of 
June through October, between Cape Flat- 
tery, Washington (48 °N) and San Diego, 
California (32°N). To sample as many 
habitats as possible, the NWFSC designed 
a sampling protocol to cover three depth 
strata, shelf (24 to 183 m), shallow slope (184 
to 549 m), and deep slope (550 to 1,341 m). 
Each year, 600 sample locations are ran- 
domly chosen from a map of the survey area 
divided into grids of 2 nautical miles in width 
by 1.5 nautical miles in length. 

More localized continuous sampling be- 
tween Davenport, California (approximately 
37°N) and Monterey, California (approxi- 
mately 36°30'N) was conducted by the 
Federal Ecology Division (FED) of the 
NOAA Fisheries Service Southwest Fisheries 
Science Center (SWFSC) laboratory in Santa 
Cruz, California. The SWFSC provided 
samples obtained by fishery-independent 
boltom-lrawl and longline survey cruises 
targeting commercial groundfish species 
monthly from June 2002 to March 2004. 
No sampling was done in the month of May 



2011 



SPATIAL DISTRIBUTION PATTERNS OF CATSHARKS AND EGG CASES 



of any year because SWFSC/FED resources 
were focused toward the annual California 
Cooperative Oceanic Fisheries Investigations 
larval fish survey. Using a depth-stratified 
sampling method, five stations at arbitrarily 
designated depth gradients were surveyed 
monthly by bottom trawls (170- to 667-m 
depth) and longlines (750 to 7,250 hooks per 
haul, from 327 to 800 m). Observers for the 
Pacific States Marine Fisheries Commission 
(PSMFC) were able to opportunistically 
donate catsharks collected by bottom trawl 
in Monterey Bay (37°N to 36°30'N) and off 
Big Sur, California (approximately 36°30'N 
to 36°N) in 2001 and 2002. Addifionally, to 
augment field samples, specimens from the 
ENP kept in collections at the University of 
Washington (UW), California Academy of 
Sciences (CAS), Museum of Comparative 
Zoology, Scripps Institute of Oceanography 
(SIO), Los Angeles County Museum 
(LACM), Smithsonian National Museum 
of Natural History USNM), and the Com- 
monwealth Scientific and Industrial Re- 
search Organization (CSIRO), Hobart, Tas- 
mania were examined. Institutional codes are 
as designated in Leviton et al. (1985). 

For all specimens examined, date of 
collection, depth, latitude, longitude, sex, 
total length, weight, and maturity were 
recorded. Maturity for females was deter- 
mined as subadult (underdeveloped oviducal 
glands and oocytes <15-mm diameter, if 
present), adult (fully developed oviducal 
glands and oocytes), or gravid (having egg 
cases) and for males as subadult (noncalci- 
fied claspers) or adult (calcified claspers). 

Distributional data 

Fished and Museum Specimens. The latitu- 
dinal and bathymetric patterns of abun- 
dance, sex ratios, and maturity of A. 
brunneus, A. kampae, and P. xaniurus were 
investigated using catch records. Species 



were arbitrarily grouped into five geographic 
areas, Washington (48 °N to 46 °N), Oregon 
(46°N to 42°N), and Northern (42°N to 
38°N), Central (38°N to 34°N), and South- 
ern California (34°N to 32°N), and histo- 
grams detailing total body length (TL, cm) 
and sex of catsharks caught were plotted for 
each species by region. Bathymetric distribu- 
tion of each species at different reproductive 
maturity stages was analyzed using geo- 
graphic information system (GIS) mapping 
and graphical representation. A multivariate 
analysis of variance (MANOVA) was used to 
determine if there was any statistical effect of 
latitude or depth on difference in species, sex, 
or maturity of individuals caught. The null 
hypothesis for the MANOVA was that there 
would be no statistical difference among sex, 
maturity, or species distributions by latitude 
or depth. Additionally, sex ratio of speci- 
mens caught by latitudinal region was 
evaluated for A. brunneus and P. xaniurus 
using a chi-square test with Yates correction 
for continuity; sex ratios were tested to 
determine if they were significantly different 
from a 1:1 (female:male) ratio. 

Nursery Grounds. Egg case deposition sites 
were determined by catch records from 
NWFSC historic cruise data for which 
photographs were available for species iden- 
tification and from observations of remotely 
operated vehicle (ROV) video footage from 
the Monterey Bay Aquarium Research In- 
stitute (MBARI) digital library. Footage 
from exploratory ROV cruises of the Mon- 
terey Bay region off Central California that 
were conducted between November 1990 and 
February 2002 was examined for egg case 
location sites. Locations of known egg case 
deposition sites were identified as essential 
fish habitat (EFH) and interpreted to be 
nursery grounds on the basis of repeated 
utilization for egg case deposition, and were 
mapped using GIS. Essential fish habitat was 
defined by the United States Congress in the 



BREVIORA 



No. 525 



Table 1. Trawl and longline survey catches of Apristurus brunneus, A. kampae, and Parmaturus xanwrus 

FROM June 2001 through October 2004 (n = 1,044). Specimens obtained from commercial fishing operations or 

museum holdings (n = 142) are not included in this table. 





#of 


Depth 


Sets with 


A. 


Depth 


A. Depth 


P. 


Depth 


Source 


Sets 


(m) 


Catsharks 


brunneus 


(m) 


kampae (m) 


xaniurus 


(m) 


NWFSC Trawls 


647 


24^1,341 


108 


486 


177-1,209 


21 738-1,233 


50 


269-563 


SWFSC Trawls 


115 


170-667 


11 


81 


178-656 


211-564 


19 


178-564 


SWFSC 


















Longlines 


129 


327-800 


22 


83 


361-800 





302 


327-800 


Total 


891 




141 


650 




21 


371 





1996 amended Magnuson-Stevens Fishery 
Conservation and Management Act as 
"those waters and substrate necessary to fish 
for spawning, breeding, feeding, or growth to 
maturity." Egg-case deposition sites were 
described to detail the depth, temperature, 
and habitat characteristics of the locations 
utihzed as nursery grounds for these deep-sea 
catsharks. Egg cases were determined to 
species using morphological characteristics 
and measurements (Gomes and de Carvalho, 
1995; Flammang et al, 2007). 

RESULTS 

Latitudinal distribution 

A combined total of 1,042 A. brunneus, A. 
kampae, and P. xaniurus were caught on 
NWFSC and SWFSC surveys from June 
2001 through October 2004 (Table 1). An 
additional 140 specimens obtained from 
museums and commercial fishing operations 
were also studied. Six hundred forty seven 
trawls conducted by the NWFSC produced 
557 catshark specimens. In the central 
California region, the SWFSC provided 100 
catsharks from 1 15 trawls and 385 catsharks 
from 129 longlines. Trawl catches were 
composed primarily of Apristurus spp., 
whereas longline catches were almost exclu- 
sively P. xaniurus. Longline surveys were 
performed over untrawlable grounds. 

There were no statistical differences in 
laliludinal regions by sex within any species. 



but there was significant latitudinal variation 
among maturity groups within and among 
species {P < 0.0001; Table 2). Specifically, A. 
brunneus subadults were found at higher 
latitudes (40°52' ± 8'N) than adults (37°45' 
± 16'N) and gravid females (36°47' ± 24'N). 
No significant difference existed in the 
latitudinal distribution of maturity groups 
within or among A. kampae and P. xaniurus, 
which were found between 35°19'N and 
37°05'N. 

Apristurus brunneus. Of the 711 A. 
brunneus studied, 650 were caught by the 
NWFSC and SWFSC surveys between 
northern Washington (48 °N) and San Diego, 
California (32°N; Table 1). These specimens 
ranged in size from 122 to 693 mm TL. The 

Table 2. Multiple analysis of variance (MANOVA) 
OF the effect of sex maturity or species of Apristurus 

BRUNNEUS, A. KAMPAE, AND PaRMATURUS XANIURUS ON 
LATITUDINAL AND BATHYMETRIC distribution (N = 1,004). 

Specimens obtained from commercial fishing 

operations OR museum holdings {N = 142) ARE NOT 
included in this TABLE. 



Effect 


Latitude 


Depth 


Sex 


ns 


ns 


Maturity 


** 


* 


Species 


*** 


*** 


Sex X species 


ns 


ns 


Maturity X species 


*** 


*** 


Sex X maturity 


*** 


*** 


Sex X maturity X species 


*** 


*** 



***P < 0.001; **P < 0.01; */' < 0.05; n.s, not 
significant. 



2011 



SPATIAL DISTRIBUTION PATTERNS OF CATSHARKS AND EGG CASES 




Figure 1. Apris turns hnmneus collected by NWFSC trawl surveys from June 2001 through October 2004. 
Frequency abundance map of catch locations of adults (A), gravid females (B), and subadults (C) with bathymetric 
contours scaled at 500-m depths. 



remaining 61 specimens, which were com- 
mercially caught and museum specimens 
from this same latitudinal range, were not 
included in distributional analysis because 
location information could not be con- 
firmed. 

The NWFSC caught 486 A. bninneus by 
bottom trawl between northern Washington 
(48°N) and San Diego, California (32°N; 
Fig. 1). A normal distribution of body size of 
92 male {n = 39) and female {n = 53) 
specimens 300 to 550 mm TL was caught off 
Washington (48 °N to 46°N; Fig. 2A). One 
hundred forty one A. bninneus were caught 
off Oregon (46°N to 42°N); TL of males 
{n = 72) was normally distributed with a 



median of 375 mm TL and female median 
length {n = 69) was approximately 450 mm 
TL in this area (Fig. 2B). 

Off Northern California (42°N to 38 °N), 
136 of 148 specimens were caught between 
42°N and 40°N (Fig. 2C). The distribution of 
males in this area was bimodal {n = 61), with 
peaks at approximately 300 and 400 mm TL, 
and females were relatively evenly distributed 
between 200 and 600 mm TL {n = 87). Males 
{n = 24) and females {n = 28) both exhibited a 
bimodal distribution in frequency by TL in 
Central California (38°N to 34°N), where 
males peaked at 375 and 625 mm TL and 
females peaked at 400 and 575 mm TL 
(Fig. 2D). Catches of ^4. bninneus in Southern 



BREVIORA 



No. 525 




100 200 300 



500 600 700 



B 



n nini 



Ui 



ll 



100 200 300 400 500 600 700 




100 200 300 400 500 600 700 





D 








20- 

1 ''■ 
i. 10 


nifl^n 


„ 




5 



1 


fl 1 1 


llll 


1.. 



100 200 300 400 500 600 700 



1 



100 200 .'JOO 400 1,00 (,00 700 

Total Length (mm) 



California (34°N to 32°N) were scattered, and 
males {n = 35) and females {n = 36) ranged 
between 120 and 600 mm TL (Fig. 2E). 

In the Monterey Bay region of Central 
California (approximately 37°00'N to 
36°30'N), 164 A. brunneus were collected by 
the SWFSC, of which 83 were caught by 
longhne and 81 by trawls. The greatest 
number of females {n = 92) caught on 
longhne were approximately 450 mm TL, 
whereas females approximately 500 mm TL 
were the most common of those in the trawls. 
Fifty seven percent of A. brunneus caught on 
the longline were mature or gravid females. 
This species was commonly found at canyon 
heads in this region and at the outer 
continental shelf and upper slope. 

Apristurus kampae. A total of 97 A. 
kampae was studied; of these, 23 were caught 
in trawls during this study and the remainder 
were from museum collections (Table 1). 
The NWFSC, which fished at greater depths 
than the SWFSC, caught 21 of the 23 A. 
kampae. The SWFSC did not collect any A. 
kampae. Two specimens were caught inci- 
dentally during commercial sablefish fishing, 
and collected by PSMFC observers. Apris- 
turus kampae were never caught on longline. 

All of the A. kampae studied {n = 97) were 
included in distributional analysis to best 
represent what is known about the geo- 
graphic distribution of this catshark (Fig. 3). 
These specimens extended from the North- 
ern California border (42 °N) to the holotype 
in the Gulf of Cahfornia (28°N; Fig. 3A). 
Gravid female A. kampae were not found 



Figure 2. Histograms of frequency of occurrence of 
females (blacic) and males (wiiile) by total length of 
Api-isliiriis hniniwus collected by NWFSC trawl surveys 
off Washington (A; 48°N to 46°N; /; = 92), Oregon (B; 
46°N to 42°N; n = 141), Northern California (C; 42°N 
to 38°N; n = 148), Central California (D; 38°N to 34°N; 
n = 52), and Southern California (E; 34°N to 32''N; n = 
71) from June 2001 through October 2004. 



2011 



SPATIAL DISTRIBUTION PATTERNS OF CATSHARKS AND EGG CASES 




100 200 



300 400 500 

Total Length (mm) 



Figure 3. Apristurus kampae (n = 97) collected by all surveys in the ENP from June 2001 through October 2004, 
combined with catch locations of museum specimens. Frequency abundance map of catch locations of adults (A), 
gravid females (B), and subadults (C) with bathymetric contours scaled at 500-m depths. (D) Histograms of 
frequency of occurrence of females (black) and males (white) by total length. 



BREVIORA 



No. 525 



farther south than 33 °N (Fig. 3B). Twenty of 
the 23 specimens caught during this study 
were caught between 38 °N and 34 °N. 
Apristurus kampae studied ranged from 74 
to 647 mm TL, most of which were between 
500 and 600 mm TL (Fig. 3D). 

Parmaturus xaniurus. Eighty-one percent of 
the P. xaniurus caught from National Marine 
Fisheries Service (NMFS) surveys were caught 
on SWFSC longHnes; only 19% were caught in 
trawls (Table 1). An additional five specimens 
were obtained from commercial fishery ob- 
servers. All P. xaniurus were caught between 
40''N and 32°N (Fig. 4). The majority of P. 
xaniurus studied (321 of 371) were collected by 
the SWFSC from Monterey Bay (37°00'N to 
36°30'N). However, adult P. xaniurus, includ- 
ing gravid females, were not found farther 
south than 33°N (Fig. 4A-C). Both males (« 
= 117) and females (« = 204) were caught 
primarily on longline surveys. The smallest 
catshark caught on longlines was a P. xaniurus 
measuring 308 mm TL. These specimens were 
typically found along the outer continental 
shelf and upper slope. Size distribution of 
males {n = 28) was skewed to the left and most 
males were between 400 and 475 mm TL 
(Fig. 4d). Females {n = 37; Fig. 4D) were 
more normally distributed, with most between 
425 and 575 mm TL. Parmaturus xaniurus as 
small as 130 mm TL was caught in bottom 
trawls in Southern California. 

Bathymetric distribution 

The species {P < 0.0001), but not the 
sexes, differed in depth distributions (Ta- 
ble 2). Also, A. brunneus subadults were 
found significantly deeper (691 ±8 m) than 
adults (580 ± 17 m), which in turn were 
deeper than gravid females (440 ± 24 m; /* < 
0.001); however, no significant difference in 
the bathymetric location occurred among 
maturity stages for ^. /:am/>«t-'( 1,141 ± 27 m) 
or P. xaniurus (492 ± 15 m). 



All life stages of A. brunneus were found 
between 300- and 1,100-m depth (Fig. 5 A). 
However, 89% of subadults were > 600-m 
depth. Gravid females were caught between 
300- and 500-m depth. This species was 
typically caught over mud or silt bottom or 
rocky areas with high vertical relief. 

Apristurus kampae was typically found 
deeper than 1,005 m, to a maximum depth 
of 1,888 m (Fig. 5B), along the continental 
slope in areas with mud or silt bottom 
habitat. Subadult A. kampae were caught in 
bottom trawls from 400- to 1,800-m depth. 
Adults and gravid females were concentrated 
between 1,000- and 1,200-m depth. 

Parmaturus xaniurus usually was found over 
mud or silt bottom or areas of rocky vertical 
relief between 300- and 550-m depth (Fig. 5C). 
Subadults were typically caught between 300- 
and 600-m depth. Almost all P. xaniurus deeper 
than 600 m were mature. Gravid females were 
generally between 300- and 500-m depth. In 
October 2004, more than 200 subadult P. 
xaniurus 130 to 200 mm TL were caught in one 
bottom trawl just south of Santa Cruz Island 
(approximately 34°N) at 475-m depth. 

Sex ratios 

Although sex ratio did not vary by latitude 
or depth (Table 2), a greater proportion of 
females to males occurred in locations where 
the sex ratio was significantly different from a 
1:1 relationship (Table 3). The sex ratio for A 
brunneus was significantly different from a 1 : 1 
relationship only in Northern California {P < 
0.05) and Central California {P < 0.01). 

Apristurus kampae in Central California 
(38°N to 34°N) had a sex ratio that was not 
significantly different from 1:1 (Table 3). There 
were not enough specimens to determine 
male: female ratios for this species in other 
regions. 

The sex ratio for P. xaniurus was also 
significantly different from a 1:1 relationship 



2011 



SPATIAL DISTRIBUTION PATTERNS OF CATSHARKS AND EGG CASES 





300 400 

Total Length (mm) 

Figure 4. Frequency abundance map of total Parmatiirus xaniurus (n = 65) adults (A), gravid females (B), and 
subadults (C) collected by NWFSC trawl surveys in the ENP from June 2001 through October 2004. Bathymetric 
contours are scaled at 500-m depths. (D) Histograms of frequency of occurrence of females (black) and males (white) 
by total length. 



10 



BREVIORA 



No. 525 



0- 
200- 
400- 


A 


• 




♦ 


E. 600- 
1 800- 




• 


'lis 


EP^ n° 


1000- 






jjS 


•^Tti 


W'i 


1200- 
1400- 






• ▼ DO 





200 400 600 

Total Length (mm) 



200 

400 

600 

800 

■=- 1000 

(B 1200 
Q 

1400 
1600 
1800 

2000 



B 









ICO 200 300 400 500 600 700 

Total Length (mm) 



0- 


c 






200- 






a 


400- 




• • 


• • • D^ 


600- 


** ••'^^& 








T 1 III II 1 1 !♦! II 1 ♦ 


800- 






D ♦ D 
HI 


1000- 









100 200 300 400 500 600 

Total Length (mm) 

Figure 5. Depth distribution of all maturity stages 
(red circle = juvenile, green triangle = adolescent, 
yellow square = mature, blue diamond = gravid) of 
Apristurus hrunneus (A, n = 730), A. kainpae (B, /? = 97), 
and Parmaturus xaniurus (C, n = 376) collected by trawl 
and longline from 48°N to 32°N. 



in central California, with a greater propor- 
tion of females (P < 0.001; Table 3). 
Parmaturus xaniurus was rarely caught in 
other regions; therefore, it was not possible 
to determine sex ratios in other locations. 

Nursery grounds 

Historic NMFS trawl data showed that egg 
cases of A. brunneus were found from 1995 
through 2001 between 46°N and 34°N 
(Fig. 6). Egg cases were located between 
300- and 400-m depth (« = 131 locations, 
mean depth = 340 ± 65 m) in areas of rocky 
vertical relief, at an average water tempera- 
ture of approximately 5°C. Egg cases caught 
in trawls were either fully tanned bundles of 
several cases, or were single, untanned cases 
expelled from a gravid female during capture. 
Egg cases are originally translucent yellow 
(untanned) and turn a darker color after being 
in seawater for at least a month (tanned). 
Bundles of egg cases consisted of two or more 
cases attached together by entangled tendrils. 
On two occasions, 8 months apart, single 
bundles of approximately 475 A. brunneus egg 
cases were trawled from the same location off 
Northern California at 39°N (Fig. 6 A; desig- 
nated by arrow). 

Large bundles of ^. brunneus egg cases were 
also identified in Monterey Bay, California 
(Fig. 6B) using archived annotated ROV 
footage from MBARI cruises from 1989 
through 2003. Bundles of egg cases were 
species specific, with A. brunneus and P. 
xaniurus egg cases often observed within 12 
to 18 cm of each other but never attached to 
the same bundle. Translucent yellow, un- 
tanned egg cases, indicating recent oviposi- 
tion, were visible in video footage captured 
year round. Adult calsharks were never seen in 
the same video footage as egg cases (Fig. 6C). 

Apristurus brunneus and P. xaniurus egg 
cases were observed in situ by ROV camera 
and were associated with specific habitats in 



2011 



SPATIAL DISTRIBUTION PATTERNS OF CATSHARKS AND EGG CASES 



11 



Table 3. Sex ratios of male and female Apristurus brunneus, A. kampae, and Parmaturus xanwrus off 

Washington (48°N to 46°N), Oregon (46°N to 42°N), and Northern (42''N to 38°N), Central (38°N to 34°N), 

and Southern California (34°N to 32 °N). Museum specimens caught in the Central California region are 

included for a. kampae. Sex ratios determined to be significantly different from a 1:1 relationship using a 

CHI-SQUARE TEST WITH YaTES CORRECTION FOR CONTINUITY (X-0.05,1 = 3.841; ZaR, 1999) ARE INDICATED. 



Species 


Region 


Sex Ratio (F:M) 


Significance 


Apristurus brunneus 


Washington 


1:0.74 


ns 




Oregon 


1:1.04 


ns 




Northern California 


1:0.70 


* 




Central California 


1:0.68 


** 




Southern California 


1:0.97 


ns 


A. kampae 


Central CaHfornia 


1:1.20 


ns 


Parmaturus xaniurus 


Central CaHfornia 


1:0.59 


*** 



***P < 0.001; **P < 0.01; *P < 0.05; ns, not significant. 



areas of rocky vertical relief in the Monterey 
Bay region (Fig. 7A). Egg cases were typically 
found between 300- and 500-m depth 
(« = 124 locations, mean depth = 427 ± 
234 m). In Central California, average water 
temperature at this depth was approximately 
5°C. Egg cases were attached to the substrate 
by long, fibrous tendrils. Apristurus brunneus 
cases were observed attached to filter-feeding 
invertebrates such as sponges (e.g., Aphrocal- 
listes vastus), gorgonians (e.g., Euplexaura 
marki), and anemones (Fig. 7B). Parmaturus 
xaniurus egg cases were also attached by their 
long tendrils to substrates, such as corals (e.g., 
Antipathese sp.), hydroids, and compound 
ascideans, and other egg cases (Fig. 7C). In 
turn, egg cases provided substrate for the 
attachment of other sessile invertebrates, such 
as filter-feeding anemones (Fig. 7D). It was 
not possible to determine the substrate type to 
which all egg cases were attached in the video 
footage available. Therefore, it was also not 
possible to determine if the substrate or 
invertebrates associated with the different 
species of egg cases was species specific. 

DISCUSSION 

Distribution 

Apristurus brunneus (with the exception of 
gravid females) was more frequently encoun- 



tered in bottom trawls and P. xaniurus was 
primarily found on longlines. This could be 
due to the life histories of these species (Lee, 
1969; Bass et al, 1975; Cross, 1988; Rich- 
ardson et al, 2000); the uniform dark color 
of A. brunneus may be a camouflage 
adaptation indicative of association with 
deep water or rocky benthic substrate, 
whereas the dorsoventral countershading of 
P. xaniurus suggests more midwater habitat 
utilizafion (Lee, 1969; Cross, 1988). Gravid 
A. brunneus females may have been caught 
more on longlines than in bottom trawls 
because of their association with rocky 
vertical relief areas for oviposition or may 
have fed on baited hooks because of 
increased metabolic needs incurred through 
reproduction. Any of these factors may have 
influenced the latitudinal and bathymetric 
distribution results for the species in this 
study. 

As with all fishing surveys, distribution 
and frequency of abundance information 
here may be biased by coverage area and 
gear selectivity (Compagno et al, 1991). 
Both trawl and longline methods of fishing 
introduce additional biases: bottom trawls 
cannot be completed over rough bottom and 
longlines only reflect the distribution of 
fishes that fed on the baited hooks. Many 
demersal fishes may successfully evade a 



12 



BREVIORA 



No. 525 



127° 



122° 



117° 



47° ■ 



42° 



37° 



122''00' 




■ZTOQ' 






■36°30' 



37°00' 



36°30' 



127° 



122° 



117° 



Figure 6. (A) Locations of Apristurus brunneus and Parmaturus xaniurus egg cases captured by trawl. The arrow 
points to the location at which 953 A. brunneus egg cases were found (« = 478, 27 October 2000; n = 475, 29 June 
2001). Parmaturus xaniurus egg cases were found only in Monterey Bay (37°00'N to 36°30'N). (B) Locations oi A. 
brunneus (circles) and P. xaniurus (triangles) egg cases as captured by remote-operated vehicle (ROV) video footage. 
CYuises were conducted by the Monterey Bay Aquarium Research Institute (MBARI), 1989 through 2003. (C) Adult 
A. brunneus caught by trawl (« = 8 1 ) and longline (n = 83) and P. xaniurus caught by trawl (n = 20) and longline (« = 
301) in Monterey Bay Canyon by the SWFSC. Longline surveys were performed over untrawlable grounds. 
Bathymetric contours are scaled at 500-m depths. 



bottom trawl. Longlines, which were set over 
untrawlable grounds, may target larger fish 
and those fishes more closely associated with 
rugged topography. In the Central California 



region, where both bottom trawl and long- 
line fishing was conducted, there was a 
conspicuous difierence in species composi- 
tion by fishing gear type. 



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SPATIAL DISTRIBUTION PATTERNS OF CATSHARKS AND EGG CASES 



13 




Figure 7. Frame shots from underwater video footage collected by ROV. (A) Large mass of P. xaniurus egg 
cases. (B) Apristurus brunneus egg case on anemone. (C) Parmaturus xaniurus egg case cluster with orange brittle star. 
(D) Anemone adhered to P. xaniurus egg case. 



Latitudinal Distribution. The three cat- 
shark species were sympatric in latitudinal 
distribution for the Central California region 
but did not occur in exactly the same 
geographic areas. Apristurus brunneus was 
the most wide-ranging scyliorhinid collected, 
and the only species caught north of 42°N. It 
was abundant in all latitudinal regions 
sampled between 48°N and 32°N. Reported 
to 46°N (Ebert, 2003), A. kampae was only 
found as far as 42°N. However, A. kampae 



was rarely encountered and found only at 
great depths and an increased sample size 
may yield specimens outside of this range. 
Parmaturus xaniurus was found only as far 
north as 40 °N, although this species has 
previously been reported as far as 46 °N 
(Ebert, 2003). 

Historic NWFSC survey data from 1995 
through 2000 indicated that P. xaniurus was 
not found north of 40°N. Scyhorhinid 
distribution can be limited by oceanographic 



14 



BREVIORA 



No. 525 



features such as temperature, elevated ridges, 
and abyssal trenches that are difficult for some 
of them to traverse as benthic, sluggish 
swimmers (Nakaya and Shirai, 1992). The 
Mendocino Ridge and Gorda Escarpment, 
which lie at approximately 40.5°N, are also 
the site of diffuse cold seeps and elevated 
currents (Drazen et al, 2003). The tempera- 
ture change and geologic structure of this area 
may act as a barrier to habitat utilization for 
some catsharks. However, the presence of 
geologic obstacles does not adequately explain 
the limits of P. xaniurus distribution, as the 
subadults of this species inhabit the midwater 
(Lee, 1969), or why the range of ^4. brunneus is 
not limited at the same latitudes. 

Bathymetric Distribution. The bathymetric 
distributions of A. brunneus, A. kampae, and 
P. xaniurus differed by species but did have 
some overlap among species. Apristurus 
brunneus, which had the largest bathymetric 
range, had broad latitudinal overlap with, 
but bathymetric segregation from, A. kam- 
pae within the Central California region. 
Apristurus brunneus and P. xaniurus were 
commonly caught together in Central Cali- 
fornia. A similar situation of narrow bathy- 
metric and latitudinal range overlap is found 
in scyliorhinids off southern Africa (Com- 
pagno et al, 1991). However, P. xaniurus 
was never caught in the same haul as A. 
kampae, and the two may be considered 
bathymetrically disparate. Deep-sea benthic 
elasmobranchs may exhibit depth segrega- 
tion to reduce competition for resources 
(Carrasson et al, 1992). Apristurus brunneus, 
A. kampae, and P. xaniurus may be in 
competition for food sources, either inter- 
specifically or intraspecificaily, because their 
distributions overlap and they have similar 
diets among all size classes (Jones and Geen, 
1977; Cross, 1988; Ebert, 2003). The ecolog- 
ical consequences of bathymetric overlap of 
these three species, such as competition for 
food resources, are unknown at this time. 



Bathymetric distribution also revealed 
depth segregation within species. Subadult 
P. xaniurus are primarily mesopelagic, and 
utilize the midwater region as a nursery 
ground for young hatchlings (Lee, 1969; 
Jones and Geen, 1977; Cross, 1988; Nakaya 
and Shirai, 1992). Ebeling et al (1970) 
reported depth segregation of subadult and 
adult P. xaniurus in the Santa Barbara Basin 
in Southern California in their study using 
opening and closing Isaacs-Kidd midwater 
trawls. Cross (1988) determined that sub- 
adults of A. brunneus and P. xaniurus were 
conspicuously absent in Southern California 
when fishing by both bottom trawl and 
longline. Bottom trawls conducted in South- 
ern California were conducted in shallower 
waters and yielded a larger proportion of 
subadult P. xaniurus (34%) than the more 
northerly trawls. The subadults in this 
southern region were also smaller in size. 
Therefore, the paucity of newly hatched and 
young-of-the-year P. xaniurus (smaller than 
250 mm TL) in the north could be due to 
their inhabiting more shallow, midwater 
regions than the adults (Lee, 1969). 

Sex ratios 

Sex ratios of A. brunneus were approxi- 
mately 1:1 in Washington, Oregon, and 
Southern California, but the number of 
females was approximately 30% greater than 
that of males in Northern and Central 
California. Parmaturus xaniurus females 
were caught 41% more frequently than males 
in Central California. Greater frequencies of 
females to males have been observed in other 
scyliorhinid sharks, including the swellshark, 
Cephaloscyllium umbratile (Taniuchi, 1988), 
the redspotted catshark, Schroederichthyes 
chilensis (Farina and Ojeda, 1993), and the 
lesser spotted dogfish, Scyliorhinus canicula 
(Ellis and Shackley, 1997). Conversely, in 
some South African members of the genus 



2011 



SPATIAL DISTRIBUTION PATTERNS OF CATSHARKS AND EGG CASES 



15 



Apristurus, adult males were found in signif- 
icantly greater numbers (Ebert et al, 2006). 
Disparity in sex ratios in sharks may result 
from sexual segregation due to reproductive 
activity, bathymetric distribution, or sam- 
pling bias (Bullis, 1967; Compagno et al, 
1991). 

Nursery grounds 

Egg-case deposition sites identified by 
ROV video footage taken in the Monterey 
Bay area provided information on the precise 
locations used for nursery sites. Specific 
attributes of nursery grounds for A. brunneus 
and P. xaniurus egg cases include location at 
the shelf-slope break and upper continental 
slope, high vertical relief with rugose sub- 
strate, and circulating water currents. Egg 
cases were often seen moving in the current 
in ROV video footage. High vertical relief 
and increased water currents are important 
aspects of reproductive aggregation sites in 
Scyliorhinus retifer (Able and Flescher, 1991) 
and some deep-sea teleosts and cephalopods 
(Drazen et al, 2003). Water circulation may 
be especially important for providing ade- 
quate oxygenation for embryogenesis when 
egg cases are clumped together in large 
aggregates (Flammang et al, 2007). Egg 
cases are deposited on massive bundles of 
older cases that have long since hatched and 
started to degrade. Continued oviposition in 
specific locations characterizes these areas 
with high vertical relief and circulating 
currents as EFH. The continued return of 
these species of catsharks, year after year, to 
a specific area to deposit their egg cases 
classifies these areas as a nursery ground, 
which may be cause for inclusion in fisheries 
management considerations (Heupel et al, 
2007). 

Use of nursery grounds is common among 
elasmobranch species (Bullis, 1967; Branstet- 
ter, 1990; Simpfendorfer and Milward, 1993; 



Ellis and Shackly, 1997), enabling neonates 
to survive without risk of predation by larger 
conspecifics (Morrissey and Gruber, 1993). 
In Monterey Bay, adult A. brunneus and P. 
xaniurus were not caught in the same 
locations that egg cases were observed in 
ROV video. Conversely, egg cases were not 
caught in the Central California trawls where 
adults of these species were found. Subadult 
P. xaniurus exhibit a mesopelagic stage and 
utilize the midwater region as a nursery 
ground (Lee, 1969; Jones and Geen, 1977; 
Cross, 1988; Nakaya and Shirai, 1992). A 
similar situation was reported for the black- 
mouth {Galeus melastomus) and marbled 
(Galeus arae) catsharks, which exhibit depth 
segregation by size and maturity class, where 
juveniles inhabit shallower areas than mature 
adults (Bulhs, 1967; Tursi et al, 1993). 

Understanding bathymetric and latitudinal 
distribution ranges for a species is necessary 
for implementation of resource management 
policies. We have found that catsharks of a 
single species at different developmental 
stages inhabit different environments, and 
perhaps potentially different ecological nich- 
es. Also, different species of catsharks overlap 
in their habitat usage and their dietary niches 
should be studied in greater detail. All 
developmental stages of a species must be 
considered in regulating species of concern; 
spatial overlap and niche partitioning must be 
examined both within and among species in a 
given environment. Finally, locales used by 
catsharks as nursery grounds should be 
considered EFH and included in future 
fisheries management policies. 

Material examined 

Type specimens and catalogued reference 
samples, sex, and total length (in mm) 
indicated in parentheses. 

Apristurus brunneus. USNM 51708 (holo- 
type; female, 477), USNM 221292 (male, 



16 



BREVIORA 



No. 525 



458), USNM 221296 (male, 216), MCZ 
36239 (male, 435). 

Apristurus kampae. SIO 70-248 (holotype; 
female, 355), SIO, 85-70 (male, 553), SIO 88- 
98 (male, 582), SIO 88-99 (female, 575), SIO 
88-100 (male, 575), SIO 92-133 (female, 570), 
CAS 57935 (female, 365), CAS 58482 (fe- 
male, 540, male, 520), CAS 38288 (three 
females, 505, 520, 535, one male, 540), CAS 
58772 (female, 540, male, 535), CAS 58487 
(two females, 137, 435), CAS 58771 (two 
females, 565, 570, one male 573), LACM 
38584 (male, 500), LACM 37511 (female, 
535), LACM 37606 (female, 490), LACM 
44107 (male, 500), CSIRO 3998-02 (male, 
557), CSIRO 3999-01 (female, 500), UW 
046041 (eight females, 458, 484, 486, 486, 
472, 495, 513, 539; nine males, 415, 484, 486, 
521, 528, 536, 554, 555, 583), UW 45629 
(female, 590), UW 48615 (male, 530), UW 
45634 (six females, 424, 449, 526, 528, 550, 
579; eight males, 429, 531, 533, 534, 554, 561, 
589, 605). 

Parmaturus xaniurus. MCZ 1228 (male, 
490). 

ACKNOWLEDGMENTS 

All animals were handled ethically in 
accordance with Institutional Animal Care 
and Use Committee standards under San 
Jose State University (SJSU) protocols 801 
and 838. Funding for this research was 
provided by NOAA/NMFS to the National 
Shark Research Consortium and Pacific 
Shark Research Center, and in part by the 
National Sea Grant College Program of the 
U.S. Department of Commerce's NOAA 
under NOAA grant no. NA04OAR4 170038, 
project number R/r-i99, through the Cali- 
fornia Sea Grant College Program and in 
part by the California Slate Resources 
Agency, SJSU F-'oundation, American Elas- 
mobranch Society travel funds, Myers Trust, 
I';Kk;ir(l ioiiiKhit loii, Kim Pcppaicl Memo- 



rial Scholarship fund, and SJSU lottery 
funds. Underwater video footage was made 
available through J. Connor and S. von 
Thun (MBARI). The authors are indebted to 
the Moss Landing Marine Laboratories 
Ichthyology laboratory; M. Ezcurra, V. 
Franklin, S. Greenwald (Monterey Bay 
Aquarium); S. Todd (PSMFC); E. J. Dick, 
J. Field, A. McCall, D. Pearson (SWFSC); 
R. N. Lea (Cahfornia Department of Fish 
and Game); the NWFSC FRAM team, 
especially K. Bosely, E. Clarke, E. Fruh, E. 
Horness, D. Kamikawa, A. Keller, V. 
Simon, and T. Wick; and the crews of the 
B. J. Thomas, Miss Julie, Excalibur, Blue 
Horizon, and Captain Jack, for their contin- 
ued support and assistance in collecting and 
processing specimens. 

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