Age, Growth, and Reproduction of the Aleutian Skate
AGE, GROWTH, AND REPRODUCTION OF THE ALEUTIAN SKATE,
BATHYRAJA ALEUTICA, FROM ALASKAN WATERS
______
A Thesis
Presented to the Faculty of
Moss Landing Marine Laboratories and the
Division of Science and Environmental Policy
California State University Monterey Bay
______
In Partial Fulfillment of the
Requirements for the Degree
Master of Science
in Marine Science
______
by
Diane Lee Haas
August 2011
© 2011
Diane Lee Haas
ALL RIGHTS RESERVED
ABSTRACT
Age, Growth, and Reproduction of the Aleutian Skate, Bathyraja aleutica, from Alaskan Waters
by Diane Lee Haas Master of Science in Marine Science California State University Monterey Bay, 2011
The Aleutian skate (Bathyraja aleutica) is a large deep-water species that commonly occurs in bycatch of Alaskan trawl and longline fisheries. Although prominent in the skate biomass of the eastern Bering Sea (EBS) and Gulf of Alaska (GOA) ecosystems, minimal biological information exists. To increase our understanding of this potentially vulnerable species, and address the possibility for two separate populations in Alaskan waters, the age, growth, and reproduction of B. aleutica was studied. Vertebrae and caudal thorns were examined for age determination, and multiple growth models were evaluated to determine growth characteristics. Skates from the EBS attained maximum ages of 17 years for females and 16 years for males, and the two-parameter -1 von Bertalanffy growth functions generated estimates of k = 0.13 yr and L∞ = 162.1 cm for females, with similar results for males. Skates from the GOA reached 19 years in females and 18 years in males. Growth parameters of female skates from the GOA were -1 estimated as k = 0.11 yr and L∞ = 160.0 cm, whereas males grew faster, with estimates -1 of k = 0.15 yr and L∞ = 138.2 cm.
In evaluating reproduction, maturity stages were determined using external morphology and histological analyses. Size at maturity was similar among sexes and regions, however, age at maturity was ~3.5 years greater for skates from the GOA (13.7 yrs) than the EBS (10.4 yrs). Ovarian fecundity reached 60 ova from skates from the EBS skates, and 36 ova for skates from the GOA skates. Both fecundity and ovum diameter increased weakly with size, but not age. The presence of males with mature spermatocysts and gravid females signified reproductive capability during all months sampled. These data indicate B. aleutica is a moderately slow-growing and late-maturing species. Although skates had relatively similar life history characteristics, skates from the GOA had greater longevity, later age at maturity, and lower potential fecundity than skates from the EBS, and may indicate increased vulnerability to fishing pressures.
ACKNOWLEDGEMENTS
Funding for this project was provided by the North Pacific Research Board
(NPRB) under project #510 and by the National Oceanographic and Atmospheric
Administration/ National Marine Fisheries Service (NOAA/NMFS) to the National Shark
Research Consortium and Pacific Shark Research Center (PSRC). This study also was supported by funds from the David and Lucille Packard Foundation, San José State
University, Earl and Ethel Meyers Oceanographic Trust, American Fisheries Society,
American Elasmobranch Society, and Western Groundfish Conference. Animal care approval was obtained from the Institutional Animal Care and Use Committee (IACUC
#801) at San José State University.
Many people provided advice and assistance with skate collections – this study would not have been possible without collaborative efforts such as these. With the
National Marine Fisheries Service-Alaska Fisheries Science Center (NMFS-AFSC), I thank Jerry Berger, Eric Brown, Sarah Gaichas, Christopher Gburski, Jerry Hoff, Dan
Kimura, Ned Laman, Bob Lauth, Beth Matta, Jay Orr, Frank Shaw, Jim Stark, and Duane
Stevenson for letting us participate on survey cruises throughout the eastern North
Pacific. I thank Rob Swanson (NMFS-AFSC) for providing valuable support with sampling efforts in Kodiak, and for taking me out catch my first Pacific halibut. With the
Alaska Department of Fish and Game (ADF&G), I thank Mike Byerly, Ken Goldman,
Tory O’Connell, Lynne Mattes, and Kally Spalinger for their advice on port sampling and allowing us to participate in ADF&G surveys. I was lucky to have participated on two research cruises in the Gulf of Alaska; I thank the crew and scientists of the F/V
v Gladiator and R/V Pandalus for their generosity and assistance while processing tons of fish over many beautiful summer days. In particular, I thank Katherine Pearson-
Maslenikov (University of Washington) and Cindy Tribuzio (NMFS-AFSC) for helping process skates and for sharing in my joy of spiny lumpsuckers. I also must thank the many NMFS observers who collecting samples throughout the Bering Sea.
I thank James Sulikowski (University of New England) and Cheryl Crowder
(Louisiana State University) for assisting with histology samples. Thank you to Josh
Bauman and Ashley McPeek who volunteered their time (and a little blood – sorry Josh) to help clean vertebrae. Amber Szoboszlai graciously provided translations of Russian journal articles. Thank you to my colleagues at the Department of Fish and Game for their support, especially Sean Hoobler, Scot Lucas, Dave Osorio and Chuck Valle.
An amazing community at Moss Landing Marine Labs has provided much help and encouragement. I thank Kenneth Coale, Donna Kline, Drew Seals, Lynn McMasters,
Jeffery Arlt, John Witkowski, Rhett Frantz, Jocelyn Douglas, and Joan Parker and the library staff for years (many, many years) of support. I also thank James Cochran and
Bubba for always having a smile and making me feel safe during late nights at the lab.
Thank you to members of PSRC, who have been involved in countless ways, including sample collections, dissections, conferences, practice talks, long van rides, sea safety training, the list goes on. Wade Smith, Heather Robinson, Chanté Davis, Lewis
Barnett, Shaara Ainsley, Jasmine Maurer, Ashley Neway, Simon Brown, Mariah Boyle, and Joe Bizzarro (who also created my map) were particularly instrumental to this study.
vi I learned a lot from Wade, especially while going through skate slime on Kodiak. Shaara and I will always share the stresses and joys of the NPRB report together.
I will cherish the memories that have been made with many friends at MLML. I loved sharing in costume parties, open houses, carpools, field trips and more. I would especially like to thank Shaara Ainsley, Mariah Boyle, Lewis Barnett, Cassandra Brooks,
Simon Brown, Chanté Davis, Cori Gibble, Kristen Green, Ashley Greenley, Phil Hoos,
Daphne Molin, Ashley Neway, Erin Loury, Jasmine Maurer, Ben Perlman, Rosemary
Romero, Jayna Schaaf-DaSilva, Jöelle Sweeney, Jon Walsh, Megan Wehrenberg, Megan
Winton, and Colleen Young. Kim Quaranta, in particular, will always have a special place in my heart.
I am so thankful to my committee members. Gregor Cailliet‘s passion for ichthyology is infectious, and I am proud to be his 115th graduate student. Dave Ebert cultivated my interest in elasmobranchs and systematics. I thank him for sending me to
Alaska, and for his multiple roles that resulted in my first publications. Thank you to Jim
Harvey for his wealth of statistical knowledge and editorial skills that helped me improve as a scientist. I would not have learned as much as I did without the enthusiasm, knowledge, patience, and kindness of my committee.
Finally, I thank my family for their encouragement though my long journey. I thank my mom, dad, Donna, Jim and Mary Haas, and Grandma and Grandpa Hardy for believing in me. I thank my husband and best friend Robert Haas for enduring the many ups and downs of my graduate life; for his love, understanding and generosity; and for taking care of our “kids” and me. Here’s to the next chapter in our lives.
vii
TABLE OF CONTENTS
LIST OF TABLES...... ix
LIST OF FIGURES ...... x
CHAPTER ONE: AGE AND GROWTH...... 1
INTRODUCTION...... 2
METHODS ...... 6
RESULTS...... 15
DISCUSSION ...... 19
LITERATURE CITED...... 32
TABLES ...... 44
FIGURES...... 48
CHAPTER TWO: MATURITY AND REPRODUCTION...... 61
INTRODUCTION...... 62
METHODS ...... 64
RESULTS...... 68
DISCUSSION ...... 72
CONCLUSIONS...... 80
LITERATURE CITED...... 84
TABLES ...... 93
FIGURES...... 94
viii LIST OF TABLES
Chapter One: Age and Growth
Table 1. Categories applied for assessing readability and clarity of vertebral centra and caudal thorns...... 44
Table 2. Parameters for each growth model for females and males of Bathyraja aleutica by location...... 45
Table 3. Longevity (ω) estimates (year) for Bathyraja aleutica based on the maximum observed age and three theoretical methods...... 46
Table 4. Comparison of age and growth parameters for several species of eastern North Pacific skates...... 47
Chapter Two: Maturity and Reproduction
Table 1. Maturity stages of female and male skates as determined by macroscopic inspection of reproductive organs...... 93
ix LIST OF FIGURES
Chapter One: Age and Growth
Figure 1. Map indicating trawl locations where Bathyraja aleutica were collected in the eastern Bering Sea and Gulf of Alaska ...... 48
Figure 2. Vertebral thin section and caudal thorn from a 100 cm total length Bathyraja aleutica aged to 9 years ...... 49
Figure 3. Length frequencies of Bathyraja aleutica used for age analysis...... 50
Figure 4. Relationship between mean centrum diameter and total length for combined sexes of Bathyraja aleutica...... 51
Figure 5. Comparison of band counts from anterior and posterior vertebrae ...... 52
Figure 6. Relationships between caudal thorn base length, width, and height with total length of Bathyraja aleutica ...... 53
Figure 7. Variation in band counts of caudal thorns along the tails of two Bathyraja aleutica ...... 54
Figure 8. Age bias plots of age estimates between independent reads of vertebral thin sections from Bathyraja aleutica from the eastern Bering Sea ...... 55
Figure 9. Age bias plots of age estimates between independent reads of Bathyraja aleutica caudal thorns...... 56
Figure 10. Comparison of caudal thorn and vertebral band counts...... 57
Figure 11. Monthly variation in centrum edge type and mean marginal increment ratio (MIR) ± 1 standard error determined for skates from the eastern Bering Sea...... 58
Figure 12. Monthly variation in centrum edge type and mean marginal increment ratio (MIR) ± 1 standard error determined for skates from the Gulf of Alaska...... 59
Figure. 13. Two-parameter von Bertalanffy growth functions fitted to observed length-at- age data for female and male Bathyraja aleutica from the eastern Bering Sea and Gulf of Alaska...... 60
Chapter Two: Maturity and Reproduction
x Figure 1. Stages III through VI of spermatogenesis used to classify spermatocysts in Bathyraja aleutica at 200× magnification ...... 94
Figure 2. Length frequencies of Bathyraja aleutica used for reproductive analysis...... 95
Figure 3. Relationships between total length and mass in Bathyraja aleutica plotted by sex and region ...... 96
Figure 4. Linear relationships between total length and disc width of Bathyraja aleutica plotted by sex for the eastern Bering Sea and Gulf of Alaska...... 97
Figure 5. Relationships between oviducal gland width and total length for female Bathyraja aleutica from the eastern Bering Sea and Gulf of Alaska...... 98
Figure 6. Relationships between uterus width and total length for female Bathyraja aleutica from the eastern Bering Sea and Gulf of Alaska ...... 99
Figure 7. Relationships between inner clasper length and proportion of mature spermatocysts with total length for mature male Bathyraja aleutica from the eastern Bering Sea and Gulf of Alaska ...... 100
Figure 8. Estimated size at maturity for female and male Bathyraja aleutica from the eastern Bering Sea and Gulf of Alaska...... 101
Figure 9. Estimated age at maturity for female and male Bathyraja aleutica from the eastern Bering Sea and Gulf of Alaska...... 102
Figure 10. Comparison between the total number of mature ova in left and right ovaries for female Bathyraja aleutica from the eastern Bering Sea and Gulf of Alaska.... 103
Figure 11. Relationships between total number of mature ova and maximum ovum diameter (MOD) with total length for female Bathyraja aleutica from the eastern Bering Sea and the Gulf of Alaska...... 104
Figure 12. Relationships between total number of mature ova and maximum ovum diameter with estimated age for female Bathyraja aleutica from the eastern Bering Sea and the Gulf of Alaska ...... 105
Figure 13. Proportion of gravid female Bathyraja aleutica by month from the eastern Bering Sea and Gulf of Alaska ...... 106
Figure 14. Monthly changes in spermatogenesis in adult male Bathyraja aleutica from the eastern Bering Sea and Gulf of Alaska...... 107
xi
CHAPTER ONE: AGE AND GROWTH
INTRODUCTION
Skates (Chondrichthyes: Rajiformes) are the largest and most diverse group of elasmobranchs, with approximately 275 described species and possibly another 75 undescribed (Ebert and Compagno 2007; Last and Gledhill 2007; Last et al. 2008a, b;
Last and Seret 2008). Found worldwide from inshore to depths greater than 3,000 meters
(Compagno 2005), skates are common demersal inhabitants of soft-bottom substrates.
Consequently, skates frequently represent a significant proportion of the biomass in commercial groundfish fisheries, either as targeted species or as incidental landings
(Ishihara 1990; Martin and Zorzi 1993; Walker and Hislop 1998). This is disconcerting because many skates have biological traits typical of most elasmobranchs, e.g. slow growth, long life span, low fecundity, and late age at maturity, which may severely restrict their ability to sustain direct or indirect fishing pressure, or recover from overexploitation (Holden 1974; Walker and Hislop 1998; Reynolds et al. 2005).
The effects of fishing pressure have been exemplified by impacts to the abundance, distribution, and population structure of several skate species. For example, the species composition of skate fisheries in the Falkland Islands was altered after only 6 years of directed fishing, with larger, later-maturing graytail skates (B. griseocauda) being replaced by smaller, earlier-maturing white-dotted (B. albomaculata) and broadnose (B. brachyurops) skates (Agnew et al. 2000). Population declines and local extirpations also have been reported for several North Atlantic species (Brander 1981;
Casey and Meyers 1998; Dulvy and Reynolds 2002). These significant changes to skate
2 abundance and population structure resulted from both direct and indirect fisheries, and emphasize the need for precautionary management of skates.
In the eastern North Pacific, skates are among the most commonly caught elasmobranchs in commercial groundfish fisheries (Camhi 1999). They primarily occur as bycatch in longline and bottom trawl fisheries in Alaska (Mattes and Spalinger 2006).
Skates represent the greatest proportion of non-target biomass landed, accounting for 51-
78% of the estimated totals of “other species” between 1992 and 2009 in the Bering Sea and Aleutian Islands (Ormseth et al. 2010). Species compositions and relative abundance of skate landings, however, remain unknown, as skates historically have been only identified to gross taxa (i.e. “skate unidentified”).
Skates have been managed as part of the “other species” category until 2004, when skates in the Gulf of Alaska were moved to a separate target species category. This management change was driven by the onset of directed fishing for skates in 2003 around
Kodiak Island where big (Raja binoculata) and longnose (R. rhina) skates were targeted with some minor harvest of bathyrajids (Mattes and Spalinger 2006). Directed fisheries for skates were prohibited in the Gulf of Alaska in 2005, due to the high levels of incidental catch and uncertainty in commercial catch data (Ormseth and Matta 2010).
Yet, a new directed skate fishery began in 2009 in Prince William Sound (Ormseth and
Matta 2010). Given the relatively large landings in previous years and frequent presence in bycatch, it is likely that directed fisheries will expand to other areas of Alaska, and skates will be increasingly targeted.
3 Fifteen species of skates occur in Alaskan waters (Stevenson et. al 2007; Orr et al.
2011). The Aleutian skate, Bathyraja aleutica (Gilbert, 1896), is one of the largest species in the North Pacific, having a maximum total length of about 161 cm (Zenger
2004). Distributed throughout the eastern North Pacific, B. aleutica ranges from northern
Japan to the Bering Sea to southeastern Alaska, and from northern British Columbia to
Cape Mendocino (Love et al. 2005). It is a deepwater skate, found at depths of 15-1,602 m, but usually occurs at 100-800 m over the continental shelf and upper slope
(Mecklenberg et al. 2002). Among the complex of 12 valid species of Bathyraja occurring in Alaska, B. aleutica dominates the biomass throughout the Gulf of Alaska
(Ormseth and Matta 2010). In the eastern Bering Sea, it comprises the majority of the skate biomass on the continental slope (> 200 m depth; Ormseth et al. 2008). Despite its common occurrence in the bycatch of Alaskan fisheries, age and growth parameters, which are essential components of life history and used extensively in stock assessments, have not been estimated.
Although skates are generally considered k-selected or equilibrium strategists, variability in their life history parameters may result in differential susceptibility to fishery exploitation (Walker and Hislop 1998; Agnew et al. 2000). In addition, intraspecific life history traits may be affected by latitude or local environmental conditions. Studies of geographic variation in elasmobranch growth parameters have primarily been on sharks (Yamaguchi et al. 1998; Carlson et al. 1999; Driggers et al.
2004). Recent investigations reporting regional variability in batoids (Frisk and Miller
2006; Licandeo and Cerna 2007) indicate that animals in higher latitudes have larger
4 maximum sizes, slower growth rates and greater longevities than their conspecifics in lower latitudes. Regional differences were found in life history parameters for two rajids between the Gulf of Alaska, British Columbia, and US west coast, including California
(Zeiner and Wolf 1993; McFarlane and King 2006; Thompson 2006; Gburski et al.
2007), though these differences did not follow a latitudinal gradient. Bathyraja aleutica is a wide-ranging species occurring in both the eastern Bering Sea and Gulf of Alaska, two large marine ecosystems separated largely by the Aleutian Islands chain, therefore the life history traits may differ between regions. Although occurring at nearly the same latitudinal gradients, populations in these large marine ecosystems experience differential temperature, ice extent, and productivity that may affect their growth characteristics
(Mundy 2005; NRC 1996).
The assessment of age and growth in teleost fishes typically relies on the examination of hard parts, such as otoliths, scales, and fin rays (Chilton and Beamish
1982). Elasmobranchs lack these highly calcified structures, and are usually aged by counting growth bands in vertebrae, dorsal spines, or neural arches (Cailliet et al. 1983;
McFarlane and Beamish 1987; McFarlane et al. 2002; Cailliet and Goldman 2004). In the past decade, caudal thorns have been successfully applied to age estimation in some skates (Gallagher and Nolan 1999; Serra-Pereira et al. 2005; Gallagher et al. 2006). Their use, however, has been inconclusive for bathyrajids (Davis et al. 2007; Matta and
Gunderson 2007). Caudal thorns should be examined for each species, especially as they may provide a non-lethal means of ageing. Banding patterns and growth rates vary considerably within and among elasmobranchs (Cailliet 1990), therefore a species-
5 specific approach is necessary when assessing ageing structures (Cailliet and Goldman
2004; Goldman 2004).
My specific objectives were to: 1) assess the suitability of vertebral centra and caudal thorns as appropriate ageing structures for B. aleutica; 2) validate age estimates using edge analysis and marginal increment analysis; and 3) describe and compare growth patterns for males and females between the eastern Bering Sea and Gulf of
Alaska. This study is the first to provide estimates of age and growth for B. aleutica from two large marine ecosystems in Alaska.
METHODS
Sample collection
Specimens of B. aleutica were collected from June 2004 to September 2007 in the eastern Bering Sea (EBS) and Gulf of Alaska (GOA; Fig. 1). Skates were collected along the EBS between June and August 2004 during a research trawl survey conducted by the
National Marine Fisheries Service Alaska Fisheries Science Center (NMFS-AFSC). The survey area extended the length of the EBS continental slope from northwest of Unalaska and Akutan Islands (approximately 54o N, 166o W) to the southern Navarin Canyon (61o
N, 180o W) on the U.S.-Russia border at depths of 194 to 1,169 m (Hoff and Brit 2005).
Additional samples were collected along the EBS continental slope during 2004-2006 by
NMFS-AFSC staff and via the NMFS Fisheries Observer Program. In the GOA, skates were obtained from April 2005 to September 2007 from surveys conducted by the Alaska
Department of Fish and Game (ADFG) and NMFS-AFSC along the Alaskan Peninsula to
6 Kamishak Bay and eastwards to the Kenai Peninsula, with much of the survey effort concentrated around Kodiak Island. Specimens were collected mostly in waters between
20 and 396 m deep. Samples also were obtained from port sampling of direct and indirect fishery landings on Kodiak Island.
Biological measurements, mass, sex, maturity status, and ageing structures were collected from skates at the time of capture. Measurements included total length (TL) and disc width (DW) as measured on a straight line to the nearest millimeter (mm) with the skate lying in its natural position. Mass was measured to the nearest 0.1 kg when possible. Maturity status was assessed by visual inspection of the reproductive organs following Ebert (2005). At least eight vertebral centra were excised from the region posterior to the cranium between the 5th and 20th vertebral elements. Because centra located in the range of the 10th to 20th vertebrae are generally of constant diameter
(Ishiyama 1958), they may vary the least and provide the most consistent age estimates.
To allow for comparison in band pairs along the vertebral column, segments were taken from anterior and posterior regions of the vertebral column. At least five caudal thorns were removed from the anterior portion of the tail. Ageing structures after removal were frozen and returned to the lab for processing.
Ageing structure preparation and evaluation
Vertebral sections were cleaned of extraneous tissue, soaked with 70% ethanol, and air-dried. Vertebrae were mounted in polyester casting resin on waxed paper retail tags, and sectioned along the saggital plane through the focus to a thickness of 0.4 mm using a Buehler® Isomet® 1000 precision saw with double diamond blades. Thin
7 sections were mounted on slides with Cytoseal 60 and polished using wet sandpaper of successive grits (grades 600, 800, and 1200) to a thickness of 0.2-0.3 mm.
To determine if vertebrae grew proportionally to body size in B. aleutica, and whether centra were appropriate for estimating growth rates, mean centrum diameter
(CD) was plotted against TL. Centrum diameter was measured to the nearest 0.1 mm at two perpendicular axes, and the mean calculated. A simple linear regression of TL and
CD was estimated for males and females separately from the EBS and GOA, and were compared using Analysis of Covariance (ANCOVA) to evaluate potential differences between TL and CD by sex. To determine whether banding patterns in centra differed along the vertebral column, mean age estimates from anterior and posterior regions were compared using a paired sample t-test (Zar 1999).
Caudal thorns were cleaned by removing excess tissue with a scalpel, followed either by soaking in 1% trypsin solution for 2 to 5 days, or boiling in fresh water until remaining tissue was easily removed. Thorns were rinsed in fresh water and stored dry.
To determine if caudal thorns were appropriate for estimating growth rate, caudal thorn height, width, and base length were measured to the nearest 0.1 mm and plotted against
TL. Sexes were compared using likelihood ratio tests (Kimura 1980) because curves were non-linear. Samples also were selected to assess variability of band counts within an individual. Ages were estimated from all caudal thorns of each skate, and charted as thorn number against age to assess consistency of age estimates along the tail.
8 Age determination and validation
Vertebral sections and whole caudal thorns were examined for the birthmark (age
0) and number of band pairs. In vertebrae, the birthmark was defined as the first distinct mark distal to the focus that coincided with an angle and density change in the corpus calcareum (Walmsley-Hart et al. 1999; Sulikowski et al. 2003), and band counts began subsequent to that point. A band pair consisted of a narrow translucent band and a wide opaque band when viewed under transmitted light (Fig. 2a; Cailliet et al. 2006). Band pairs have typically been assumed to represent annual growth in skates (Zeiner and Wolf
1993; Sulikowski et al. 2005; Frisk and Miller 2006), and ages were estimated by counting the number of narrow translucent and associated opaque bands. A coat of mineral oil was used to enhance the banding patterns.
In caudal thorns, a band pair was defined as a concentric ridge and an associated broad growth zone on the surface of the thorn (Gallagher et al. 2006). Age estimates were made by counting band pairs distal to the protothorn (birthmark increment) located at the thorn apex (Fig. 2b; Gallagher and Nolan 1999; Matta 2006). Whole thorns were viewed under alternating transmitted and reflected light. A combination of oil enhancement and lead microtopography (Neer and Cailliet 2001) best improved the clarity of bands in caudal thorns.
Analyses of precision and bias were used to assess reproducibility between reads and reader consistency. Band counts were made by a single reader in three randomized trials for each specimen, with at least two weeks between successive reads, and no prior knowledge of sex, length, or previous counts. Final age estimates were assigned based on
9 the agreement of two or more reads. If no agreement was reached in two of the first three reads, a fourth read was made to clarify age estimates. If no agreement could be made after the fourth read, the sample was omitted from further age analysis.
The readability of each ageing structure was assessed with methods similar to
Smith et al. (2007), with grade 1 being the lowest clarity and grade 5 the highest (Table
1). Individuals given a grade 1 or 2 were re-sectioned and examined again. If the readability was still a 1, those samples were excluded from further analysis.
Several measures were used to assess reader precision. The index of average percent error (IAPE) for the entire sample set was calculated as:
N $ R ' 1 1 X ij " X j IAPE j =100%* #& # ) N j 1& R i 1 X j ) = % = ( where N is the total number of samples, R is the number of reads per ageing structure, Xij
th th is the i age determination! of the j ageing structure, and Xj is the mean age determination for the jth ageing structure (Beamish and Fournier 1981). Because age 0 samples can distort APE estimates (Officer et al. 1996), they were excluded from precision calculations. Coefficient of variation (CV) also was estimated for the entire sample set to facilitate comparison with other studies (Chang 1982). This was calculated as:
R 2 (Xij " X j ) # R "1 CV =100%* i=1 j X j
th where CVj represents a precision estimate for the j ageing structure (Chang 1982). !
10 Chi-square tests of symmetry (McNemar 1947; Bowker 1948; Evans and Hoenig
1998) using contingency tables tested if differences between reads were biased or due to random error. In addition, percent reader agreement (PA) was used to evaluate intra- reader consistency (Goldman 2004) and age bias plots modified after Campana et al.
(1995) were produced to graphically examine variability among paired reads. Age estimates from vertebral centra were compared with caudal thorn age estimates using age bias plots and paired t-tests (Zar 1999).
Age validation, the process of testing hypotheses about the temporal periodicity of band deposition, was performed to determine whether bands were deposited predictably
(Cailliet et al. 1986). Validation of age estimates was necessary to ensure the accuracy of the assumption that growth zones being counted represent some temporal unit, such as year (Cailliet et al. 2006). For example, growth band deposition in the vertebral centra of
Squatina californica and Cetorhinus maximus was not predictable (Natanson and Cailliet
1990; Natanson et al. 2008). Two types of indirect age validation were used to assess the temporal periodicity of growth band formation in the vertebrae: marginal increment ratio and centrum edge analysis. Because age-zero animals do not have fully formed growth bands, they were excluded from validation assessments.
Marginal increment ratio (quantitative) was performed on vertebral thin sections following Conrath et al. (2002). The marginal increment ratio (MIR) was calculated as:
MIR = MW/PBW where the marginal band pair width (MW), or the distance from the last wide opaque band to the edge of the margin, is divided by previous band pair width (PBW). MIR
11 measurements were conducted along the axis of the corpus calcareum using Image Pro
Plus software (Media Cybernetics, Silver Springs, MD, USA). The resulting MIR values were plotted against month of capture. Differences in mean MIR among months were assessed using ANOVA (Zar 1999) to test for seasonality of band deposition.
Centrum edge analysis qualitatively compares the relative proportion of individuals with opaque or translucent centrum edges through time to discern seasonal changes in growth (Tanaka and Mizue 1979; Cailliet et al. 2006). The centrum marginal edge was graded into 4 categories, following Smith et al. (2007): narrow opaque band forming (O1), broad opaque band well-formed (O2), narrow translucent band forming
(T1), and broad translucent band well-formed (T2). The proportion of edge types was compared for each sampled month to detect seasonal differences in growth.
Growth
Four different growth models were fit to observed length-at-age data for males and females at each location. Growth model parameters were estimated using a non- linear least-squares regression and SigmaPlot graphical software (SPSS Inc., 2002).
The three-parameter von Bertalanffy function (3VBGF; Beverton and Holt 1957) is widely used in fisheries biology to estimate demographic parameters (Haddon 2001), and is the most common growth model used in elasmobranch age and growth studies.
The 3VBGF was fitted to the data with the following equation:
L = L 1# e(#k(t#to )) t "( ),
!
12 where Lt = length at age t; L∞ = asymptotic or maximum length; k = growth coefficient; and to = age at theoretical length zero (Ricker 1979). Length at birth (L0) was then calculated as:
kt 0 L0 = L! (1" e ), to confirm whether the resulting value falls within the range of observed length at birth
(Cailliet et al. 2006). Alternatively, a two-parameter von Bertalanffy growth function
(2VBGF) was fitted to the data, which uses estimates of L0 and does not require calculation of to, as it is more biologically meaningful and may provide more robust results (Cailliet and Goldman 2004; Cailliet et al. 2006):
(#k+t ) Lt = L" # (L" # L0 )(e ), where parameters are as previously defined.
The Gompertz! growth function also was fitted to the data, as it has provided the best fit for some batoids (Mollet et al. 2002; Neer and Thompson 2005; Smith et al.
2007). Because of the limited weight data, the Gompertz parameters were estimated by substituting length-at-age data for weight variables using the following form:
(#ke ( #gt ) ) Lt = L"(e ), where Lt, L∞ and t are as previously defined; k = a constant such that kg is the ! instantaneous growth rate when t = 0 and Lt = L0; and g = instantaneous rate of growth when t = to (Ricker 1979).
Finally, a logistic model (modified from Ricker 1979) was fit to TL-at-age data.
Logistic parameters were estimated using:
13 L L = ! t "g(t "t 0 ) 1 + e , where g = instantaneous rate of growth, to the inflection point, and other parameters as previously defined.
Growth model goodness-of-fit was assessed by comparisons of several values.
The coefficient of determination (r2), significance level (p < 0.05), and residual mean square error (MSE) were compared to determine which model best fit the size-at-age estimates (Carlson and Baremore 2005; Neer and Thompson 2005). Biological reality and significance also were considered (Cailliet et al. 2006). Differences in growth curves between sexes and locations were tested using Kimura’s (1980) likelihood ratio test.
Four methods were used to estimate longevity. The oldest observed individuals provided initial longevity estimates, however, these are likely to be underestimates in a fished population. Theoretical longevity (ω) was estimated following Taylor (1958), who defined longevity as the age at which 95% of the L∞ is reached, and was calculated as:
ln(1" 0.95) ! = t0 + k using parameters derived from the 2VBGF. Longevity also was predicted at 95%
(5(ln2)/k) and 99% (7(ln2)/k) of the L∞ following Ricker (1979) and Fabens (1965), respectively.
14 RESULTS
Sample collection
In total, 1,281 skates were collected in the EBS and GOA during exploratory trawl surveys, by fisheries observers, and from fishery landings. Vertebral centra of 410 skates from the EBS and 247 skates from the GOA were used for age analysis. Skates were collected during 10 months, although not from all months within each sampling year. Males from the EBS (n = 187) were 23.9 to 149.9 cm TL, and females (n = 223)
20.6 to 153.4 cm TL (Fig. 3a). Males from the GOA (n = 112) were 31.5 to 140.1 cm TL, and females (n = 135) 26.0 to 153.6 cm TL (Fig. 3b).
Ageing structure preparation and evaluation
Vertebral centra from 657 B. aleutica were processed for ageing. Measurements of centrum diameter indicated a significant linear relationship between TL and CD for skates from both the EBS (TL = 6.59 + 14.67CD, r2 = 0.975) and GOA (TL = 13.19
+13.53CD, r2 = 0.934). No significant difference in this relationship was detected between males and females from the EBS, so these data were combined (ANCOVA, F =
0.600, p = 0.440, n = 157), resulting in a positive linear regression (TL = 6.593 +
14.671CD, r2 = 0.973; Fig. 4a). Differences between sexes from the GOA were not significant, so these data also were combined (ANCOVA, F = 0.326, p = 0.569, n = 173), resulting in a positive linear relationship (TL = 13.186 + 13.531CD, r2 = 0.967; Fig. 4b).
There was no detectable bias in centrum banding patterns from anterior and posterior regions of the vertebral column (Fig. 5). Differences between paired age
15 estimates were not significant (t = -1.564, p = 0.130, n = 27), therefore, all age estimates were based on anterior vertebral centra.
Caudal thorns from 75 B. aleutica from the EBS were evaluated. Relationships of caudal thorn measurements to TL were best described by power functions. The relationship of TL (cm) to thorn base length (TBL; mm) resulted in the best fit when compared with thorn width to TL (r2 = 0.780) and thorn height to TL (r2 = 0.638) regressions (Fig. 6). Differences between the TL to TBL relationship for males and females were not significant, so these data were combined (χ2 = 1.7446, p = 0.418, n =
68), and were described by the following power function: TBL = 0.2493 x TL0.7581 (r2 =
0.812).
All caudal thorns from the tails of two individuals were aged and charted against corresponding thorn number (Fig. 7). Caudal thorn band counts for each individual were highly variable, with age estimates ranging from 5 to 10 in one specimen, and no apparent pattern along the tail.
Age determination and validation
Examination of ageing structures indicated that quality of banding patterns was highly variable within each structure. Of the 410 centra from EBS skates, 325 (80%) had suitable quality (grade 2 or greater) and agreement among age estimates for further analysis. Of the 247 centra examined from GOA skates, 186 (74%) were of suitable quality and agreement for use in age analysis.
Overall precision among the three age estimates from vertebral thin sections was generally great for both EBS (IAPE = 8.91%, CV = 11.45%) and GOA (IAPE = 8.08%,
16 CV = 10.50%) samples. Age bias plots demonstrated no appreciable bias between vertebral reads (Fig. 8). Results of contingency tables indicated no differences between reads of EBS vertebrae. All reads of GOA vertebrae were significantly different except reads 1 and 3. Percent agreement analysis indicated great precision among vertebral reads, with 99.4% of all ages within 3 years for EBS vertebrae, and 97.3% within 3 years for GOA vertebrae.
Among caudal thorns, 21 of 75 (28%) were unsuitable for age analysis due to poor quality and lack of agreement. Therefore, age estimates from 54 caudal thorns were compared with vertebral thin sections from the same specimens. Precision of caudal thorn age estimates was less than for vertebrae (IAPE = 10.84%, CV = 14.08%). Age bias plots indicated minimal variation around the 1:1 ratio and no systematic bias among caudal thorn reads (Fig. 9). Results of contingency tables indicated no biases between thorn reads.
Vertebral thin section and caudal thorn age estimates were positively correlated
(r2 = 0.87), however a paired t-test revealed significant differences between age estimates
(t = 4.517, p < 0.001). Comparisons between ageing structures indicated a tendency for thorn age estimates to be greater than those from vertebrae (Fig. 10). Precision was poor between paired caudal thorn and vertebral thin section age estimates (IAPE = 22.00%,
CV = 31.11%).
An annual pattern of band deposition could not be validated using applied marginal increment and edge analysis methods. Among vertebral samples from the EBS,
109 were considered usable for marginal increment analysis. The greatest mean MIR
17 value (0.80) occurred in January and the least (0.42) in March. Differences in mean MIR values among months were not significant (F =1.824, p = 0.081; Fig. 11). Comparison of centrum edge types from 125 vertebral samples demonstrated that translucent bands were present most frequently at the edge during January and opaque bands during July.
Among the 175 vertebral thin sections from GOA skates that were examined, there was no evident pattern of centrum edge types among months. The greatest mean
MIR value (0.82) occurred in July and the lowest (0.45) in March. Mean MIR values did not differ significantly among months (F =1.415, p = 0.214; Fig. 12).
Growth
Vertebral age estimates for skates from the EBS were 0 to 16 years for males (n =
149) and 0 to 17 years for females (n = 176). The largest male was 149.9 cm TL and 13 years, whereas the oldest male, aged to 16 years, was 132.4 cm TL. The largest female was 153.4 cm TL and to 15 years. The oldest female, aged to 17 years, was 144.4 cm TL.
Skates from the GOA attained greater ages, and were 0 to 18 years for males (n =
83) and 0 to 19 years for females (n = 103). The largest male, 15 years old, was 140.1 cm
TL, whereas the oldest male was 130.6 cm TL and 18 years. The largest female was
153.6 cm TL and 15 years. The oldest females, aged to 19 years, were 152.5, 149.4, and
140.6 cm TL.
All growth models fit the length-at-age data well and were highly significant in both locations, though models fit the EBS data better (Table 2). For skates in the EBS, all growth models were biologically reasonable, but the 3VBGF had the best goodness-of- fit. Growth model parameters were generally similar for GOA skates, however, the
18 theoretical maximum length estimated by the 3VBGF was biologically unrealistic, and likely was skewed by the lack of length-at-age data for small skates (<50 cm TL). Further age and growth results, therefore, were compared using the 2VBGF.
Female skates from the EBS reached a larger maximum size (L∞ = 162.1 cm) and had a slightly lesser growth coefficient (k = 0.13) than males (L∞= 158.9 cm, k = 0.14), however, differences in growth were not significant between sexes (χ2 = 0.47, p = 0.791).
Similarly, GOA females attained a larger maximum size (L∞ = 160.0 cm) and had a lesser growth coefficient (k = 0.11) than males (L∞= 138.2 cm, k = 0.15). Male and female growth curves, however, were significantly different (χ2 = 11.13, p = 0.0038). Significant differences in 2VBGFs between locations occurred for both females and males (Fig. 13; females χ2 = 34.25, p < 0.0001; males χ2 = 44.62, p < 0.0001).
Vertebral growth bands indicate longevity of 17 years (females) and 16 years
(males) in the EBS, and 19 years (females) and 18 years (males) in the GOA. Theoretical longevity estimates were greater than the maximum band counts, reaching 26 years for
GOA females based on Taylor (1958) and high as 44 years based on Fabens (1965; Table
3).
DISCUSSION
Ageing structures
An important requirement of age and growth studies is to ensure that the calcified structures used to estimate age represent continuous growth of the animal (Casselman
1983). The strong positive relationship between CD and TL indicated vertebral centrum
19 size increased proportionally with somatic growth, and centra were appropriate structures for age and growth analysis in B. aleutica. Vertebral centra have become the predominant structure used in elasmobranch age and growth studies after Ridewood (1921) first documented calcified growth bands in shark and ray centra.
Caudal thorn size also was positively correlated with somatic growth, yet fit more poorly than vertebrae. Variability in thorn height was likely attributed to thorn erosion, particularly near the tip in larger skates (Gallagher and Nolan 1999). All thorn measures, however, appeared to increase in variability with TL, as indicated by the nonlinear regressions and weaker coefficients of determination. Logarithmic and variable thorn size to body size regressions also were found for several Bathyraja (Davis et al. 2007; Perez et al. 2010) and Amblyraja spp. (Francis and Maolagáin 2005; Gallagher et al. 2006).
These data indicate that thorns may not be suitable ageing structures, particularly as skates reach asymptotic length. Unlike vertebrae, caudal thorns, which originate from dermal denticle scales, do not function in supporting body mass and may not be intrinsically connected to somatic growth (Gallagher et al. 2005; Davis et al 2007).
Caudal thorns may perform similarly to scales of larger slow growing teleosts, which virtually cease in growth at a certain body size (Casselman 1990).
Age estimates were evaluated by structure sampling region (i.e. anterior vs. posterior centra; thorn position along the tail) to confirm that patterns of growth band deposition were consistent, regardless of where vertebral centra or caudal thorns were taken from the skate. Although sampling region along the vertebral column can significantly affect band counts (Officer et al. 1996), ages from paired anterior and
20 posterior regions of the vertebral column were similar for Bathyraja aleutica. Band counts from caudal thorns, however, were highly variable along the tail, again indicating inconsistent or slowed growth in these structures and further supporting their unsuitability. Similarly, the caudal thorn series from a specimen of B. kincaidii failed to show agreement of age estimates, in addition to having evidence of thorn replacement
(Perez 2005). Arkhipkin et al. (2008) consistently found lesser band counts in the first anterior thorns of two Falkland Island skate species, and suggested that anterior caudal thorns were more prone to damage than those from the posterior tail region.
Age determination and validation
Several methods of evaluating precision were used, given the variability in clarity of growth patterns and the importance of ensuring that age estimates were repeatable. The measures of precision were reasonable for both vertebral centra and caudal thorn age estimates, and were consistent with other elasmobranch studies. Estimates of APE and
CV were better than those found for B. trachura (Davis et al. 2007) and Raja rhina
(Thompson 2006). CV values typically exceeded 10% in most shark ageing studies
(Campana 2001), therefore, precision of age estimates was considered acceptable for each structure in Bathyraja aleutica, though less favorable for caudal thorns.
Comparison between paired ageing structures demonstrated poor precision. Band counts from caudal thorns were greater than those from vertebral centra. This indicated greater variability in ages using thorns, or an underestimation of ages from vertebral centra. A bias may have resulted from the reader ageing the vertebral centra before the caudal thorns, as experienced readers tend to discern more bands in ageing structures
21 (Officer et al. 1996; Gallagher et al. 2006). In B. brachyurops, vertebral growth increments were more difficult to discern than those in thorns, and caused underestimation of age in older fishes (Arkhipkin et al. 2008). Although age estimates between centra and thorns were in agreement for B. parmifera (Matta and Gunderson
2007), caudal thorn age estimates have been unreliable for six other eastern North Pacific bathyrajids (Davis et al. 2007; Maurer 2009; Ebert et al. 2009; Perez et al. 2010; Ainsley et al. 2011). Because the level of precision was greater for vertebrae, and given that thorn growth may not be intrinsically linked to somatic growth, vertebral centra were chosen as the most reliable ageing structure for B. aleutica.
Validation of annual band deposition was inconclusive in B. aleutica. In skates from the EBS, the majority of translucent bands were present in January and opaque bands in July (excluding March, as n = 3). This may suggest a trend, as the proportion of centrum edge types was consistent with the expected pattern of greatest opaque edges in the summer (fast growth) and translucent edges in the winter (slow growth; Waring
1984), as was found in B. parmifera (Matta and Gunderson 2007). MIR values were not highly significantly different among months, but a 0.08 p-value indicated a weak biological change occurring in the vertebrae through time. Natanson et al. (2007) noted similar results for female Malacoraja senta, although mean monthly MIRs were significantly different for males, and timing of MIR peaks was incongruent between sexes. MIRs were combined for male and female B. aleutica, and may have contributed to their variability. Direct validation of annual band pair formation using bomb
22 radiocarbon has only been reported for one skate species, Amblyraja radiata (McPhie and
Campana 2009).
The resolution of an annual banding pattern may have been precluded by several factors. Samples were not available for all months, there were minimal sample sizes for some months, and samples were included from multiple years. Poor edge clarity due to reduced calcification, overpolishing, or lack of photographic resolution resulted in fewer samples available for edge analysis. However, edge analyses have supported the annual deposition pattern of one opaque and one translucent band for several other skate species, including A. radiata (Sulikowski et al. 2005), Raja texana (Sulikowski et al. 2007), and
Bathyraja parmifera (Matta and Gunderson 2007). In addition, age validation using oxytetracycline injection has been successful in several sharks (Kusher et al. 1992;
Natanson et al. 2002) and skates (Holden and Vince 1973; Natanson 1993; Cicia et al.
2009). I therefore assumed a pattern of annual band deposition for B. aleutica. Because of the possibility of over or underestimation of ages in this study, however, estimates for fisheries management must be used cautiously (Campana 2001).
Growth
Among batoids, maximum ages vary widely, from 3 years in Himantura imbricata (Tanaka and Ohnishi 1998) to 26 years in Raja binoculata and R. rhina
(McFarlane and King 2006). Recently, Ainsley et al. (2011) determined Bathyraja minispinosa reached 37 years, the greatest estimated age attained by skates to date.
Maurer (2009) determined B. lindbergi and B. maculata both reached 32 years using histological methods. This method can provide for more counts, however, it also may
23 yield too much detail and overestimate age (Maurer 2009). Nonetheless, histology has been accepted for B. interrupta and B. trachura (Ainsley 2009; Winton 2011), and should be investigated for B. aleutica in the future. Although the use of histology to estimate ages could reveal greater longevities, regional differences would still be expected.
Maximum ages estimated for B. aleutica using standard sectioning methods were
17 years for skates from the EBS and 19 years for skates from the GOA. These ages were similar to some of the smaller sized skates from the eastern North Pacific, with reported maximum ages of 18 years for B. kincaidii (Perez et al. 2010), 17 years for B. parmifera
(Matta and Gunderson 2007), and 20 years for B. trachura (Davis et al. 2007). Although
Raja binoculata from British Columbia attained larger sizes and older ages (204 cm TL,
26 years), the same species studied in the GOA were from approximately the same size classes as Bathyraja aleutica yet reached a lesser maximum age of 15 years (McFarlane and King 2006; Gburski et al. 2007). Raja rhina from the GOA and British Columbia, which were only 10-20 cm smaller in length, attained greater maximum age estimates of
25 and 26 years. Overall, Bathyraja aleutica generally falls within the mid-range of longevity estimates for skates (Sulikowski et al. 2005). The oldest skate aged from vertebral centra, which was a 19 year old skate from the GOA, provided an initial estimate of longevity. This value is likely an underestimate of longevity in a fished population (Natanson et al. 2002).
Theoretical longevities estimated with 2VBGF parameters varied depending on the method used, but all were greater than maximum band counts. Fabens’ (1965) estimates, based on the time it takes to reach 99% of L∞, were generally twice the
24 maximum band counts and may not be the best method for B. aleutica. Taylor’s (1958) method resulted in estimates closest to vertebral ages, and was considered the most biologically reasonable method. McPhie and Campana (2009) also found Taylor’s estimates closest to maximum observed ages for four North Atlantic skate species.
Researchers of chondrichthyan age and growth primarily apply the 3VBGF to age-at-length data. However, because of limitations identified with this growth function, the application and comparison of alternative growth models was suggested (Cailliet et al. 2006). Based on the criteria of statistical fit, biological relevance, and convenience
(Roff 1979; Moreau 1987; Cailliet et al. 2006), the 2VBGF best fit the length-at-age data of B. aleutica. Although the statistical fit to the 3VBGF was best for age-at-length data from the EBS and GOA, the growth parameters estimated by this function were the least biologically reasonable in size at birth and asymptotic length.
Model generated estimates of size at birth (Lo) were greater than reported birth sizes. Teshima and Tomonaga (1986) estimated Lo as 19.6 to 26.3 cm TL, whereas Hoff
(2009) determined B. aleutica embryos at 23.5-25.8 cm TL had completely internalized their yolk and were near egg-case emergence. For skates in the EBS, the Lo predicted by the 3VBGF (29.7 cm TL) and Gompertz models (31.8 cm TL) were greater than the smallest free-swimming individuals (20.6 cm TL female and 23.9 cm TL male).
Estimates of Lo for GOA skates using the 3VBGF were much greater (females 44.0 cm, males 41.4 cm). These overestimates may indicate the limited ability of the 3VBGF to describe early growth (Gamito 1998). This also may reflect the use of whole ages, as prescribing ages with half-year increments may have provided more precise model fits,
25 especially during initial growth (Frisk and Miller 2006; Smith et al. 2007). Because the
2VBGF best fit the growth of skates from the GOA, and fits well for skates from the
EBS, this function was considered to be the most convenient as it allowed for more meaningful comparisons between locations.
The estimates of asymptotic length (L∞) further supported the use of alternative growth models. The L∞ estimated by the 3VBGF for females from the GOA (211 cm TL) was unrealistic as it was much greater than the largest skate reported (161 cm TL; Zenger
2001), and likely resulted from the lack of small skates (<50 cm TL) in the sample. L∞ estimates from the 2VBGF were closest to the maximum observed sizes for all skates except males from the GOA, which were influenced by the lack of samples greater than
140 cm. Although samples were obtained through most of the known size range for skates from the EBS, the low number of samples from the oldest age classes may have affected L∞ estimates.
The von Bertalanffy growth coefficient (k) is commonly used to compare life history strategies and address the potential vulnerability of a population. Although the conventional view has been that most elasmobranchs exhibit slow growth in comparison with bony fishes (Camhi et al. 1998), a wide range of growth rates has been found in batoids. Estimates of k values among skates are quite broad (Musick 1999; Cailliet and
Goldman 2004), with reported growth coefficients ranging from 0.05 yr-1 for Dipturus pullopunctata (Walmsley-Hart et al. 1999) to 0.50 yr-1 for Raja miraletus (Abdel-Aziz
1992). Bathyraja aleutica, therefore, is considered a moderately slow growing, large bodied species. Growth coefficients were similar to those in the smaller sized B.
26 parmifera (Table 4; Matta and Gunderson 2007). Likewise, growth rates were greater than in comparably sized Raja rhina (k = 0.037-0.056 yr-1), but within the range of estimates for the larger species, R. binoculata (k = 0.080-0.152 yr-1; Gburski et al. 2007), from the GOA.
Growth parameters differed between sexes of Bathyraja aleutica. Female skates reached larger sizes and grew more slowly than males in both locations, however growth curves were significantly different only between males and females from the GOA. Of the skate sexes and locations sampled, males from the GOA were the only skates that did not reach 150 cm TL. This likely contributed to differences in 2VBGF parameters between sexes from the GOA. Slower growth rates and larger sizes in females have been reported for several skates (MacFarlane and King 2006; Gburski et al. 2007; Licandeo and Cerna 2007) and sharks (Carlson and Parsons 1997; Goldman and Musick 2006).
In comparing growth between locations, male and female skates from the EBS attained greater lengths at age than those from the GOA, and skates from the GOA reached maximum ages that were greater by two years. Ainsley (2009) also found that B. interrupta from the GOA attained older ages than those from the EBS. In B. aleutica, L∞ and k estimates were less in the GOA, except for males, which had a lesser growth coefficient in the EBS. Although differences between growth curves were statistically significant, variability does not seem biologically significant between locations, and may be the result of similar levels of productivity.
Greater levels of primary productivity and phytoplankton biomass in the water column reflect a greater benthic biomass (Grebmeier et al. 1988). The GOA is considered
27 a Class I highly productive ecosystem, with greater than 300 g C m-2 y-1, whereas the
EBS generates between 150 and 300 g C m-2 y-1and is a Class II moderately high productivity ecosystem (NOAA 2008a, b). Although net primary productivity may be slightly higher and occur over a longer period in the GOA (Meuter et al. 2009), skates living along the shelf edge of the EBS may benefit from areas of greater productivity. In the region along the edge of continental shelf, known as the Bering Sea Green Belt, productivity can be 60% greater than on the outer shelf. The Bering Slope Current can entrain plankton from the shelf, shelf edge and basin, and enhance feeding opportunities
(Springer et al. 1996). If skates in both regions receive about the same levels of biomass, similar levels of productivity may be expected to provide similar feeding opportunities and growth characteristics.
In a study of food habits, Brown (2010) found that B. aleutica from the GOA primarily consume pink shrimp and tanner crabs, indicating potential resource competition with both commercially important groundfish species. Diet information for
B. aleutica from the EBS is only available as a complex with other bathyrajids, but skates in Russian waters shifted from crustaceans to fishes and cephalopods with increasing size
(Orlov 1998). The removal of competitive groups in either region could affect life history traits by increasing available food resources. Because B. aleutica is distributed differently in the GOA and EBS, different ecosystem relationships are expected.
The slight differences in life history characteristics of B. aleutica between ecosystems also may be the result of migrations and mixing of populations. Grant and
Utter (1980) found that populations of walleye pollock, Theragra chalcogramma, in the
28 EBS and GOA were not distinct stocks but had minor genetic differences in fish between regions. These small but detectable differences may have been due to restricted migrations between regions, homing to and mixing between spawning areas, or a combination of both (Grant and Utter 1980). Yellowfin sole, Limanda aspera, also exhibited genetic differences between the EBS and GOA regions (Grant et al. 1983). In a tagging study off British Columbia, King and McFarlane (2010) found that though the majority of tagged big skate (Raja binoculata) were recaptured within 21 km of the original capture location, some skates made long-range movements into Oregon,
Washington, the GOA, and the Bering Sea. Tagging studies also have indicated that
Pacific cod, Gadus macrocephalus, in the EBS migrate to the GOA and Aleutian Islands regions, intermingling with populations in those areas (Bakkala 1993).
Apparent differences in growth between regions also may have been due to sampling methods or environmental factors. A temporal effect may have occurred, as the majority of EBS samples were collected in 2004 whereas skates from the GOA were captured during 2005-2007. Sampling depth also may have attributed to variability in growth parameters. All skates from the EBS were collected in the continental slope region, between 194 and 1,169 m (mean 510 m), whereas skates from the GOA were taken from shallower shelf areas between 20 and 396 m (mean 123 m). Though life history patterns have been linked with size in some skate assemblages (Dulvy and
Reynolds 2002), longevities of Alaskan skate species may scale with depth (Cailliet et al
2001). In addition, skates inhabiting the slope may shift from deeper to shallower waters with size (Orlov et al. 2006; Hoff 2010).
29 Temperature, a factor of region and sampling depth, also may have attributed to variation in growth between skates from EBS and GOA. In tows where B. aleutica were captured, during the 2004 EBS survey temperatures ranged from 2.3 to 4.3°C (mean
3.5°C), whereas during the 2005 GOA survey, temperatures were about two degrees greater, ranging from 4.0 to 6.7 °C (mean 5.5°C). Though temperature may have a significant effect on banding patterns in elasmobranchs (Goldman 2004), no effects were apparent on vertebral band deposition in Leucoraja (Raja) erinacea (Natanson 1993;
Sagarese and Frisk 2010).
Geographic variations in life history parameters have been documented in several elasmobranchs. Several researchers discussing variation by latitude have found that animals in higher latitudes are larger and grow more slowly to older ages than their conspecifics at lower latitudes (Carlson and Parsons 1997; Yamaguchi et al. 1998; Frisk and Miller 2006; Licandeo and Cerna 2007). However geographic variations do not always follow this pattern, such as in Raja undulata, which in higher latitudes had faster growth (Moura et al. 2007). The northern areas of Portugal were colder for an extended period, and differences in growth rates may relate to a longer breeding season. In blacknose sharks, Carcharinus acronotus, females in the western North Atlantic (higher latitudes) were of significantly smaller size but had lesser growth rates and greater longevities than sharks from the Gulf of Mexico (Driggers et al. 2004). Conversely, western Atlantic rays, Rhinoptera bonasus, were larger but grew faster and had lesser longevities than rays from the Gulf of Mexico (Neer and Thompson 2005). Geographic variation was found in R. bonasus, but a gradient was not apparent, and variation may
30 have been due to methodologies. In this study, B. aleutica were collected from both the
EBS and GOA in an overlapping range of ~55-61° N latitude, which may attribute to similarities in growth.
Many species with wide geographic distributions inhabit environments with different annual temperatures and varying duration of the growing season. Though the conditions experienced by these populations may differ, disparities in growth, such as in size at the end of the first growing season, may be minimal (Conover 1990; 1992).
Several models of growth compensation have been suggested to explain similar growth at different latitudes. Size-selective mortality may be more pronounced in high latitude populations, where only the largest, fastest-growing individuals survive; a greater proportion of slower-growing survivors may occur at lower latitudes (Jobling 2002).
Growth rates of fish at lower latitudes may be more constrained by food availability, thus fish may not grow to their full physiological potential (Jobling 2002). Negative effects of lesser temperature and a short growth season on the growth of fish in high latitudes may be counteracted by compensatory mechanisms, such as local thermal adaptation or countergradient variation (Conover and Schultz 1995; Yamahira and Conover 2002)
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43 Table 1. Categories applied for assessing readability and clarity of vertebral centra and caudal thorns based on Smith et al. 2007.
Grade Criteria
1 Banding pattern vague; increments irregular or cloudy; limited confidence distinguishing band count; sample may be damaged
2 More than two band counts possible; indefinite banding pattern in one or more sample locations; best estimate recorded
3 Two band counts possible; recorded estimate is the most probable
4 Band count unambiguous but increment/s are not of exceptional clarity
5 Band count unambiguous; all increments are distinct and readily distinguished
TABLE
44 Table 2. Parameters for each growth model for females and males of Bathyraja aleutica by location. 3VBGF = 3 parameter von Bertalanffy growth function; 2VBGF = 2- parameter von Bertalanffy growth function using set Lo; L∞ = asymptotic total length in cm; k and g = growth coefficients; t0 = theoretical age at 0 length; L0 = total length at birth in cm.
2 Model L∞ k t0 L0 g r MSE SEE p Eastern Bering Sea Females 3VBGF 174.4 0.10 1.86 30.3 - 0.9545 63.38 7.96 <0.0001 2VBGF 162.1 0.13 - 23.0 - 0.9455 75.59 8.69 <0.0001 Gompertz 150.4 1.54 - 32.2 0.21 0.9535 64.85 8.05 <0.0001 Logistic 142.3 - 3.56 - 0.32 0.9495 70.41 8.39 <0.0001
Males 3VBGF 170.5 0.11 1.69 29.0 - 0.9569 60.41 7.77 <0.0001 2VBGF 158.9 0.14 - 23.0 - 0.9497 70.04 8.37 <0.0001 Gompertz 147.6 1.55 - 31.3 0.22 0.9566 60.92 7.81 <0.0001 Logistic 140.1 - 3.45 - 0.34 0.9531 65.84 8.11 <0.0001
Gulf of Alaska Females 3VBGF 211.8 0.05 4.55 44.0 - 0.8860 95.33 9.76 <0.0001 2VBGF 160.0 0.11 - 23.0 - 0.8620 114.27 10.69 <0.0001 Gompertz 176.3 1.31 - 47.6 0.10 0.8859 95.40 9.77 <0.0001 Logistic 162.7 - 5.14 - 0.16 0.8859 95.37 9.77 <0.0001
Males 3VBGF 158.3 0.09 3.41 41.4 - 0.8554 83.22 9.12 <0.0001 2VBGF 138.2 0.15 - 23.0 - 0.8351 93.71 9.68 <0.0001 Gompertz 147.3 1.16 - 46.1 0.14 0.8521 85.12 9.23 <0.0001 Logistic 141.7 - 3.34 - 0.19 0.8489 86.90 9.32 <0.0001
45 Table 3. Longevity (ω) estimates (year) for Bathyraja aleutica based on the maximum observed age and three theoretical methods. Vertebral age and growth parameters estimated from the 2-parameter von Bertalanffy growth function were used to obtain ω.
Method EBS GOA Female ω Male ω Female ω Male ω Maximum band count 17 16 19 18
Taylor (95% L∞) 21.9 20.3 25.8 18.7
Ricker (95% L∞) 26.7 24.8 31.5 23.1 Fabens (99% L∞) 37.3 34.7 44.1 32.3
46 Table 4. Comparison of age and growth parameters for several species of eastern North Pacific skates. Max Lobs, observed maximum length; L∞ and k, von Bertalanffy growth parameters; Max Ageobs, observed maximum age. Parameters are from the three- parameter von Bertalanffy function to facilitate comparisons between studies.
Max L L Max Species Source obs ∞ k Location (cm) (cm) Ageobs Bathyraja 153.4 (F) 174.4 0.10 17 E. Bering This study aleutica 149.9 (M) 170.5 0.11 16 Sea Bathyraja 153.6 (F) 211.8 0.05 19 Gulf of This study aleutica 140.1 (M) 158.3 0.09 18 Alaska Bathyraja 87 (F) E. Bering Ainsley (2009) 112.5 0.06 19 interrupta 89 (M) Sea Bathyraja 88 (F) Gulf of Ainsley (2009) 119.2 0.06 21 interrupta 84 (M) Alaska Bathyraja 102.1 (F) E. Bering Maurer (2009) 131.9 0.04 32 lindbergi 93.2 (M) Sea Bathyraja 61.0 (F) E. North Perez et al. (2010) 56.0 0.21 18 kincaidii 63.5 (M) Pacific Bathyraja 114.5 (F) E. Bering Maurer (2009) 155.6 0.04 32 maculata 114.4 (M) Sea Bathyraja 89.5 (F) E. Bering Ainsley et al. (2011) 146.9 0.02 37 minispinosa 83.7 (M) Sea Bathyraja Matta and Gunderson 119.6 (F) E. Bering 135.4 0.10 17 parmifera (2007) 118.0 (M) Sea Bathyraja 72.5 (F) E. Bering Ebert et al. (2009) 78.1 0.13 14 taranetzi 66.3 (M) Sea Bathyraja 94.2 (F) E. Bering Winton (2011) 119.2 0.04 30 trachura 91.8 (M) Sea Bathyraja 86.5 (F) E. North Davis (2006) 112.1 0.06 20 trachura 91.0 (M) Pacific Raja 178 (F) Gulf of Gburski et al. (2007) 189.6 0.11 15 binoculata 141 (M) Alaska Raja McFarlane and King 203.9 (F) British 293.4 0.04 26 binoculata (2006) 183.6 (M) Columbia 140 (F) Gulf of Raja rhina Gburski et al. (2007) 203.8 0.04 25 129 (M) Alaska McFarlane and King 124.6 (F) British Raja rhina 133.8 0.07 26 (2006) 122.0 (M) Columbia
47
Figure 1. Map indicating trawl locations where Bathyraja aleutica were collected in eastern Bering Sea ( ) and Gulf of Alaska ( ).
FIGURES
48 a
b
Figure 2. Vertebral thin section (a) and caudal thorn (b) from a 100 cm total length Bathyraja aleutica aged to 9 years. Arrows identify the birthmark, signified by a change in angle and density of the corpus calcareum in the vertebral thin section, and a ridge associated with the protothorn on the caudal thorn. Band pairs (i.e. one opaque and one translucent band) are indicated by white dots. Bar = 1 mm.
49 EBS
GOA
Figure 3. Length frequencies of Bathyraja aleutica used for age analysis. Top: Females (n = 223) and males (n = 187) from the eastern Bering Sea; and bottom: females (n = 135) and males (n = 112) from the Gulf of Alaska.
50
EBS
GOA
Figure 4. Relationship between mean centrum diameter and total length for combined sexes of Bathyraja aleutica from a) the eastern Bering Sea (n = 157) and b) the Gulf of Alaska (n = 173).
51
Figure 5. Comparison of band counts from anterior and posterior vertebrae for Bathyraja aleutica (n = 27). The 45º line represents 1:1 agreement between band counts. Differences between paired band counts were not significant (t = -1.564, p = 0.13). Bars represent one standard error.
52
Figure 6. Relationships between caudal thorn base length, width, and height and total length of Bathyraja aleutica (n = 68). All three curvilinear regressions were significant, however thorn base length (TBL) best fit total length (TL; TBL = 0.2493 x TL0.7581, r2 = 0.81).
53
Figure 7. Variation in band counts of caudal thorns along the tails of two Bathyraja aleutica. Position 1 is the most anterior and 17 the most posterior thorn.
54
Figure 8. Age bias plots of age estimates between independent reads of vertebral thin sections from Bathyraja aleutica from the eastern Bering Sea (n = 325). Plots demonstrated no biases between reads. The 45º line represents 1:1 agreement between band counts. Bars represent one standard error.
55
Figure 9. Age bias plots of age estimates between independent reads of Bathyraja aleutica caudal thorns (n = 54). Plots demonstrated no biases between reads. The 45º line represents 1:1 agreement between band counts. Bars represent one standard error.
56
Figure 10. Comparison of caudal thorn and vertebral band counts from Bathyraja aleutica (n = 27). The 45º line represents 1:1 agreement between band counts. Bars represent one standard error.
57
Figure 11. Monthly variation in centrum edge type (n = 124) and mean marginal increment ratio (MIR) ± 1 standard error (n = 109) determined for skates from the eastern Bering Sea. Values listed above the histogram represent the number of samples used in centrum edge analyses. Sample sizes included in MIR analyses are depicted below month in parentheses. T1, narrow translucent edge; T2, broad translucent edge; O1, narrow opaque edge; O2, broad opaque edge.
58
Figure 12. Monthly variation in centrum edge type (n = 175) and mean marginal increment ratio (MIR) ± 1 standard error (n = 136) determined for skates from the Gulf of Alaska. Values listed above the histogram represent the number of samples used in centrum edge analyses. Sample sizes included in MIR analyses are depicted below month in parentheses. T1, narrow translucent edge; T2, broad translucent edge; O1, narrow opaque edge; O2, broad opaque edge.
59 a
b
Figure. 13. Two-parameter von Bertalanffy growth functions fitted to observed length-at- age data for a) female and b) male Bathyraja aleutica from the eastern Bering Sea and Gulf of Alaska.
60
CHAPTER TWO: MATURITY AND REPRODUCTION
INTRODUCTION
The reproductive success of a species is an important determination in fisheries management. Measures of reproduction are used in stock assessments of harvested species, ecological risk assessments of bycatch species, and species assessments against extinction risk criteria (Walker 2004; 2005). Specific reproductive parameters include the relationships between fecundity and maturity with the age or size of the animal (Walker
2005). Estimates of these parameters and other life history traits, such as age and growth, are imperative for the management of elasmobranchs, as they are often characterized as having late age at maturity and low fecundity at large size (Reynolds et al. 2005).
Information on size and age at maturity, fecundity and reproductive patterns for many skates, including Bathyraja aleutica, are limited.
Existing biological information for B. aleutica includes geographic distribution and descriptions of embryos and egg cases. Its distribution has been reviewed in North
Pacific waters (Teshima and Wilderbuer 1990; Dolganov 1999; Stevenson 2004).
Reproductive information has been collected regarding embryonic development (Teshima and Tomonaga 1986), observations of egg cases (Ishiyama 1958a; Ebert 2005), and details of clasper anatomy (Ishiyama 1958b). Food habits of B. aleutica have been examined from the western Pacific (Orlov 1998), and recently from Alaskan waters
(Brown 2010). Hoff (2009a, b) described embryo development events and egg predation from nursery sites in the eastern Bering Sea (EBS) for B. aleutica and B. parmifera.
Aspects on the reproductive biology of B. aleutica have been previously studied and provide some basis for comparisons. Dolganov (1998) estimated size and age at
62 maturity for skates from Russian waters, which included the western Bering Sea. Ebert
(2005) presented maturity estimates for B. aleutica from the EBS, however only nine mature males were examined, and none were greater than 133 cm TL although the maximum observed size for males is 150 cm TL (Ishiyama 1958b). In addition, maturity was assessed by visual inspection of gonads and secondary sex organs, but studies indicate maturity should be evaluated using a combination of analyses, such as a comparison with histological criteria (Sulikowski et al. 2005a; 2006). Determining histological changes in gonad structure may be useful because gross morphology alone may not be a reliable means of assessing reproductive readiness (Maruska et al. 1996;
Henderson and Arkhipkin 2010).
The size and age at maturity of a species may vary by latitude or region.
Geographical differences in these life history parameters have been observed in several elasmobranch species (Yamaguchi et al. 2000; Lombardi-Carlson et al. 2003; Neer and
Thompson 2005; Licandeo and Cerna 2007; Quiroz et al. 2009). However, because
Bathyraja aleutica is distributed across two management regions in Alaska, the Gulf of
Alaska (GOA) and the Bering Sea and Aleutian Islands (BSAI) regions, comparative information on reproduction and maturity from both areas will be useful for regional fishery management plans.
The recent re-emergence of directed fisheries for skates in Prince William Sound exemplifies the need to collect life history information for skate species in Alaska. Skates that attain a large size, are highly abundant, and are easily accessible, such as B. aleutica, are likely targets in directed fisheries (Hoff 2009a). Management plans for skates in
63 Alaska, based on survey estimates and life history information, continue to evolve
(Ormseth and Matta 2010; Ormseth et al. 2010).
Given the limited data on this relatively large skate in Alaska and the possibility that it may be subject to targeted fisheries in the future, the objectives of this study were to 1) determine maturity status using external and histological observations of the reproductive organs; 2) compare size and age at first, 50%, and 100% maturity between sexes and between the eastern Bering Sea (EBS) and GOA; 3) examine relationships between maternal size or age with oocyte size and number; and 4) determine if seasonal spawning peaks occur in B. aleutica.
METHODS
Sample collection
External and internal morphometrics were determined from the same B. aleutica specimens as described in the previous chapter. Mass (M) was recorded when possible, to the nearest 0.1 kg. The relationship of total length (TL) to M was described by the power equation M = aTLb, where a and b are fitted constants (Ricker 1973). Linear regressions were fitted to log-transformed M data, and an analysis of covariance (ANCOVA) was used to compare this relationship between sexes and regions.
Disc width (DW) is a commonly used metric in skate biological studies, however
TL is recommended as the main body measurement (Francis 2006). DW was measured on a straight line from wing tip to wing tip to the nearest millimeter (mm) with the skate lying in its natural position. To facilitate comparisons with other studies, DW was plotted
64 against TL. Due to interactions between sex and location, a t-test was used to evaluate the linear relationships between sexes by location (Zar 1999).
Measurements of male and female reproductive organs were determined from fresh specimens at sea or dockside. Inner clasper length, as measured from the point of insertion of the clasper shaft to the tip, was recorded for males. Oviducal gland (= shell or nidamental; Hamlett and Koob 1999) width and uterus width, as well as the total number of mature ova in both ovaries (ovarian fecundity) and maximum ovum diameter, were recorded for females. The uterus widths of gravid females were not recorded as the egg cases inside stretched the uteri. Reproductive tracts were preserved in 10% buffered formalin for further processing.
Maturity status was determined in the field by visual inspection of the reproductive organs following Ebert (2005; Table 1). Three maturity stages (juvenile, adolescent, adult) were determined for each sex, with an additional gravid stage assigned for females. Changes in reproductive organ size were used to further assess or verify the onset of maturity. Oviducal gland width and uterus width of females and inner clasper length of males were plotted against TL. A sharp increase in growth of each structure relative to TL was assumed to correspond with the onset of maturity, followed by a slowing of growth, which was assumed to correspond with full maturation of the individual (Ebert 2005).
Histology
Histological assays of reproductive tracts were conducted to examine potential seasonal changes in the reproductive cycle and to verify macroscopic maturity
65 assessments. A cross section (3-4 mm thick) from the center of each preserved testis was placed in tissue cassettes for sectioning, and stored in 70% ethanol. Gonad sections were shipped to the University of New Hampshire and Louisiana State University veterinary laboratories for embedding, sectioning and processing using standard hematoxylin and eosin staining (e.g. Maruska et al. 1996). Prepared slides were then examined under a compound microscope.
The maturity stages of sperm in the testes were evaluated from samples for each available month. The developmental stages of spermatogenesis have been well described for several elasmobranch groups, including skates, and hormonal analyses have confirmed that spermatocyst and spermatid stages are associated with reproductive readiness (Heupel et al. 1999; Sulikowski et al. 2004). Therefore, these specific stages were evaluated: stage III, spermatocytes; stage IV, spermatids; stage V, immature spermatozoa; and stage VI, mature spermatocysts (Fig. 1; Maruska et al. 1996; Conrath and Musick 2002). Stage VII, consisting of empty spermatocysts and free spermatogonia, was considered mature and included with stage VI estimates. The mean proportion of mature spermatocysts was estimated along a transect crossing a full, representative section of testis lobe. The tightness and organization of sperm packets in the spermatocysts were used to corroborate macroscopic maturity status (Sulikowski et al.
2005a, b).
66 Maturity
Once maturity was assessed visually and confirmed via histology, size and age at first, median, and 100% maturity were estimated. First maturity was determined by the size and age of the smallest mature individuals examined for each sex and location.
Maturity ogives were used to estimate size and age at median maturity. Binomial maturity data (0 = immature; 1 = mature) were binned into 5 cm TL size classes or 1 year age classes (Roa et al. 1999; Mollet et al. 2000). A logistic equation was fitted using least squares non-linear regression and SigmaPlot graphical software (SPSS Inc., vers. 8.0,
Chicago, IL) in the following form:
1 Y = (1+ e !(a+bx) ) where Y = maturity status and x = TL in cm or age in years. Median size (TL50) or age
(Age50) at maturity was calculated as –a/b, with males and females analyzed separately for each location. 100% maturity was considered the size and age at which all examined skates were subsequently mature.
The effects of maternal size and age on reproduction were assessed using regressions of ova size and number of mature ova on maternal size and age. All mature ova visible on the surface of each ovary were enumerated, and the diameter of the largest ovum was measured to the nearest mm. Mature ova were characterized by their yolky appearance and size, typically exceeding 10 mm in diameter (Ebert 2005). The number of mature ova and maximum ovum diameter each were regressed against length and age to see if either of these factors contributed to variation of ova size and number (Matta 2006).
67 The number of mature ova in left and right ovaries was compared for significant differences using a paired sample t-test (Zar 1999).
To discern any seasonal peaks in reproductive activity, the percentage of mature females with developing egg cases in utero were plotted against each sampled month, and differences in proportion were assessed using a Chi-square (χ2) test for homogeneity (Zar
1999). In mature males, the mean proportion of testes occupied by each stage of spermatogenesis per month was compared to discern any seasonal pattern in testis development.
RESULTS
Reproductive observations were recorded from a subsample of 1,076 B. aleutica
(320 female and 298 male skates from the EBS, and 280 female and 177 male skates from the GOA; Fig. 2). Skates throughout the entire size range were used for analyses
(see Chapter 1), however, few skates less than 60 cm TL and no males greater than 140 cm TL were collected from the GOA. Reproductive metrics and measurements were not collected from every skate, therefore, numbers do not add up to the total number of skates sampled.
Relationships between total length and mass (TL-M) were similar between sexes
(ANCOVA, F = 0.006, p = 0.938) and regions (F = 2.765, p = 0.097). No significant interaction between the factors was found (F = 1.662, p = 0.198). Female and male skates from the EBS greater than 100 cm TL attained greater mass at length than their GOA
68 counterparts, however these differences were not significant and data were pooled (M =
0.000004*TL3.0602, r2 = 0.943; Fig. 3).
The relationships between TL and DW were strong. A significant interaction was found between sex and location (ANCOVA, F = 8.163, p = 0.004), therefore t-tests were used to compare regressions by location. There were no differences in the TL-DW relationship between sexes in the EBS (t = 0.339, p = 0.734) therefore females and males were pooled, resulting in a strong linear relationship (DW = 0.6603TL – 2.2493, r2 =
0.995). Differences between sexes in the GOA were insignificant (t = 0.449, p = 0.653) and those data also were pooled (DW = 0.6350TL – 1.4716, r2 = 0.984; Fig. 4).
The onset of maturity was indicated by measures of gonad morphology in females. Oviducal gland widths reached 88 mm in skates from the EBS and 82 mm in skates from the GOA. Uterus widths reached 39 mm in skates from the EBS, and were greater in skates from the GOA, reaching 55 mm. The abrupt changes in the relationships between oviducal gland widths and uterus widths with TL indicated maturity began at approximately 110 to 115 cm TL in both regions (Figs. 5 and 6).
In males, the onset of maturity was evident using observations of inner clasper lengths (ICLs) and analysis of histological samples. In skates from the EBS, ICLs exceeded 200 mm in all mature males, and reached a maximum of 266 mm. Among skates from the GOA, the smallest mature skate had an ICL of 193 mm, the largest immature skate had an ICL of 287 mm, and the maximum ICL reached 304 mm.
Maturity was indicated by sharp increases in the ICL – TL relationship, and was apparent at ~115 cm TL for skates from both the EBS and GOA (Fig. 7). In histological samples,
69 mature spermatocysts were visible among males by 116.4 cm TL in the EBS and by
110.7 cm TL in the GOA. The proportion of mature spermatocysts was greater than 5% in all males over 129.2 cm TL from the EBS and over 114.5 cm TL from the GOA.
Skates from the EBS and GOA attained maturity at similar sizes. Among skates from the EBS, first and 100% maturity were attained at 111.6 and 137.6 cm TL for females, and 117.7 and 133.3 cm TL for males. Based on maturity ogives, TL50 was estimated as 124.1 cm for females and 122.8 cm for males. Among skates from the GOA, females attained first and 100% maturity at 121.2 and 140.6 cm TL, whereas males attained first maturity and 100% maturity at 117.2 and 129.3 cm TL. Using maturity ogives, TL50 was estimated as 125.7 cm for females and 122.7 cm for males (Fig. 8).
Estimated ages at maturity were more similar between sexes than between regions. Females from the EBS matured at slightly older ages than males. First and 100% maturity was attained at 9 and 12 years in females, and at 7 and 11 years in males.
Median ages at maturity were estimated as 10.4 years for females and 10.2 years for males. Skates from the GOA matured over older ages in comparison to skates from the
EBS. Females from the GOA attained first and 100% maturity at 13 and 18 years, and males attained first and 100% maturity at 12 to 18 years. Using maturity ogives, median ages at maturity were 13.7 yrs for females and 13.6 yrs for males (Fig. 9).
The number of mature ova in left and right ovaries was highly correlated but not significantly different in skates from the EBS (t = 1.129, p = 0.285, n = 11). Ovaries of females from the GOA did differ significantly in ova number (t = 2.144, p = 0.037, n =
54; Fig. 10). The left ovary contained slightly greater mean (10 vs. 9) and maximum (22
70 vs. 20) numbers of ova than the right ovaries. The number of ova from both ovaries was used for further analyses.
The number of mature ova was 7 to 60 ova in females in the EBS, and 3 to 36 ova in females in the GOA. The maximum ovum diameter (MOD) was 59 mm for females in the EBS and 71 mm for females in the GOA females. Both total number of mature ova and MOD increased with female size in skates from EBS and GOA. The relationships were relatively weak between TL and total number of mature ova (EBS r2= 0.14; GOA r2= 0.03). The relationships between MOD and TL were slightly stronger (EBS r2 = 0.35;
GOA r2= 0.16; Fig. 11). There was no apparent relationship between the total number of mature ova with age (EBS r2 = 0.05; GOA r2 = 0.0003), though there was a slight increase in MOD with age (EBS r2 = 0.004; GOA r2 = 0.10; Fig 12.)
The proportion of gravid females per month was compared to discern reproductive seasonality. Among skates from the EBS, no gravid females were found in
August, however, the proportion of gravid females was similar among the three months sampled (χ2 = 1.18, n = 27). Gravid females from the GOA were found in all months sampled except April. The proportion of gravid females was significantly different between months (χ2 = 15.90, n = 53; Fig. 13).
In adult males, mature spermatocysts occurred in all months sampled in both regions. The relative proportion of mature spermatocysts decreased from the earlier to later months, with the exception of a slight increase in September for skates from the
GOA (Fig. 14).
71 DISCUSSION
Sexual dimorphism in body size or shape is common among elasmobranchs, often with females attaining larger sizes than males (Cortés 2004). This trend has been observed in several skates (Walmsley-Hart et al. 1999), including Bathyraja aleutica from the EBS (Ebert 2005). In my study, however, males and females obtained similar sizes; only females from GOA were ~10 cm greater in length than males. Larger skates
(>150 cm TL) such as Raja binoculata may be more likely to exhibit dimorphic differences than smaller species (Ainsley 2011; Ebert et al. 2008a). In oviparous species, the relative importance of body size decreases because eggs develop in protective egg cases and are deposited on the sea floor. In viviparous elasmobranchs, fecundity is limited by body size because they produce large, heavily yolked eggs with prolonged embryonic development (Sims 2005). In an analysis of 159 shark species, viviparous females were 10-16% longer than male conspecifics, whereas this difference was only
~1% in oviparous species (Sims 2005).
Length and mass (weight) relationships also are often sexually dimorphic. Using the regression slope from the length-weight equation, Orlov and Binohlan (2009) found that Bathyraja aleutica females from the western Bering Sea were heavier than males.
This value, similar to condition factor (CF), indicates a pattern of change in body form and condition with an increase in size, usually reflecting growth in gonadal tissue (Moyle and Cech 2004). Although differences in mass were not significant between sexes or locations in this study, CF values were greater in females compared with males.
Condition factor was positively allometric for skates from the EBS (females b = 3.45;
72 males b = 3.33), and similar to those from the western Bering Sea (Orlov and Binohlan
2009). Skates from the GOA exhibited lesser CF values (females b = 2.78, males b =
2.94), and may indicate that the general condition of skates from the EBS was greater than those from the GOA. Variation in CF may be related to food availability, reproductive events, or liver weight (Oddone and Velasco 2006; Oddone et al. 2007).
Sample size, seasonal variation, and size-specific comparisons should also be considered
(Oddone et al. 2007).
Maturity in sharks is typically determined by the direct observation of reproductive tracts or secondary sex organs (Conrath 2004). Rapid changes in the size of the oviducal glands in females or the inner clasper length in males indicate onset of maturity. Ebert (2005) found that oviducal glands widths of B. aleutica in the EBS increased at 120-130 cm TL, and males ICLs increased rapidly in length at 103-120 mm
TL. In my study, both male and female reproductive organs began increasing in size at approximately 115 cm TL. These discrepancies may have been due to differences in sample sizes, sampling years, locations, or food resources.
Reproductive readiness in males is not only determined by the presence of fully developed claspers, but also requires mature sperm within the reproductive tract (Conrath
2004). Histological analysis of gonads has been used to confirm maturity stages determined by morphological examination in several skates (Sulikowski et al. 2006,
2007; Henderson and Arkhipkin 2010). Increases in clasper length correlated with increases in mature spermatocysts for skates from both the EBS and GOA. A slight delay was observed in functional maturity as claspers began developing before spermatocysts.
73 Similar observations have been noted in several other skates (Sulikowski et al. 2005b,
2006, 2007; Ebert et al. 2008a).
Based on maturity ogives, females and males from the EBS reached 50% maturity at a similar size and age (females 124.1 cm, 10.4 years; males 122.8 cm, 10.2 years).
These values corresponded to 81-82% of maximum observed length and 61-64% of maximum observed age in females and males. Maturity in skates from the GOA was reached at similar lengths to skates from the EBS but at ages older by about 3 years, corresponding to 82-87% of maximum observed length and 72-76% of maximum observed age. In a review of life history patterns, Cortés (2000) concluded that sharks reached maturity around 75% of their maximum size and 50% of maximum age, therefore B. aleutica may be considered a late maturing species.
Size at maturity estimates for B. aleutica differed slightly from previous studies.
Ebert (2005) estimated that first maturity in EBS females occurred at greater size (133.0 cm TL, 86.4% of observed maximum length) than found in my study (111.6 cm TL,
72.7% of observed maximum length). Additionally, I found males from the EBS first matured at 117.7 cm TL, which corresponded with 78.5% of maximum observed TL.
Although previous reports were similar, indicating first maturity at 119.0 cm TL, Ebert
(2005) determined this was 89.4% of maximum length, which was likely an artifact of smaller maximum size observed in that study.
Reported size (and age) at first maturity for B. aleutica from Russian waters, which included the western Bering Sea, was most similar to females from the EBS, but less for males. Maturity estimates were from 112.0 to 133.2 cm TL (9-10 years) for
74 females and 108.0 to 116.0 cm TL (8-9 years) for males (Dolganov 1998; Fadeev 2005), corresponding to 72.7–86.5% and 72.0–77.3% of maximum length. These data indicate a cline from the western to eastern North Pacific, with age at maturity increasing from
Russian water to the GOA. Differences between studies may be attributed to discrepancies in methods for assessing maturity, differences between sampling locations or years, environmental conditions, or a combination of these factors.
A mature 94.4 cm TL female was observed from the EBS carrying half formed egg cases in the oviducal glands, but was considered an outlier as it was considerably smaller (~17 cm) than the next mature female. Bizzarro and Vaughn (2009), however, observed a 98.0 cm TL gravid female off southeast Alaska. The gravid maturity stage is usually indicated by observations of egg cases in the uterus; partially formed egg cases that are still within the oviducal gland are not as conspicuous. Although it is possible that other smaller gravid females were present with incomplete egg cases, no other skates less than 111.6 cm TL contained mature ova.
Female elasmobranchs possess either paired ovaries, in which both are capable of producing eggs, or may have one predominant and one absent or rudimentary ovary
(Hamlett and Koob 1999; Lutton et al. 2005). In most skates, ovaries are paired and symmetrical, as was found in B. aleutica. The number of mature ova in skates from the
EBS was similar between left and right ovaries, a result consistent with other skates
(Braccini and Chiaramonte 2002; Ebert 2005; Ruocco et al. 2006). Although a greater number of ova occurred in the left ovary of skates from the GOA, these measures were only slightly greater than what occurred in the right ovary (left/right ovary: mean number
75 of ova 10/9; maximum number of ova 22/20). The nature of the left ovary may be a residual effect of the evolution of egg-laying from live-bearing (Dulvy and Reynolds
1997). Among those viviparous elasmobranchs with one principal ovary, the right ovary is generally dominant in sharks, whereas only the left ovary produces mature ova in most rays (Hamlett and Koob 1999).
Maximum ovarian fecundity in EBS skates ranged from 7 to 60 ova (mean = 30.9
± 5.6 SE), whereas GOA skates were less productive, with ovarian fecundity ranging from 3 to 36 ova (mean = 18.5 ± 1.2 SE). Similarly, Quiroz et al. (2009) estimated average annual fecundity for Dipturus chilensis was 23.4 ova. The annual fecundity of skates ranged from 2 to 140 eggs per year, and averaged 58.9 eggs per year (Musick and
Ellis 2005). Values of annual fecundity in Bathyraja aleutica are likely underestimates.
Determining fecundity via ovum counts in oviparous species is difficult because many species have an extended breeding season with eggs developing throughout the year.
Another method of estimating fecundity is the determination of ovulation rates and egg laying period, usually using animals in captivity (Conrath 2004). Annual fecundities of captive bred skates averaged 40.5 eggs for Amblyraja radiata, 48.1 eggs for Leucoraja ocellata, and 69-85 eggs for Dipturus laevis, with one female laying up to 115 eggs
(Parent et al. 2008). Although similar in size to D. laevis, the lesser potential fecundity of
Bathyraja aleutica, particularly for skates from the GOA, may indicate increased vulnerability to fishing pressure..
The number of mature ova (ovarian fecundity) appeared to increase with maternal size. Similar to Ebert (2005), ova number increased with TL then decreased for most
76 individuals greater than 145 cm TL. A slight but significant relationship was found for B. parmifera (Matta and Gunderson 2007), where ovarian fecundity was only loosely correlated with maternal size in B. albomaculata (Henderson et al. 2005). Similar results have been reported for Psammobatis extenta (Braccini and Chiaramonte 2002), Dipturus laevis (Gedamke et al. 2005), and D. chilensis (Licandeo et al. 2006). Positive relationships between uterine fecundity and maternal length also have been observed in viviparous rays (Kyne and Bennett 2002; Yamaguchi and Kume 2009).
Among teleosts, the importance of size and age on fecundity has been demonstrated, particularly in the genus Sebastes (e.g. “Big Old Fecund Females” or
BOFFs; Berkeley et al. 2004; Cailliet and Andrews 2008). Size may be more important to fecundity than age in some elasmobranchs, as was suggested for Triakis semifasciata
(Ebert and Ebert 2005). In my study, total length was a slightly better predictor of ovarian fecundity than age in Bathyraja aleutica, however, the sample sizes were small. Results were inconclusive, as the greatest fecundity of 60 ova was found in a 134.1 cm TL female of 11 years, while the oldest and largest female (144 cm TL and 17 years) had 53 ova from the EBS. The maximum fecundity in aged females from the GOA was 32 ova from a 17-year old, 138.3 cm female, and exceeded the number of ova found in the largest and oldest females. A decline in fecundity with size or age and may be indicative of recrudescence or senescence, and was previously noted to occur in B. aleutica within the last 6% of maximum observed size (Ebert 2005).
Bathyraja aleutica from the EBS and GOA exhibited similarities in size and size at maturity, yet differences in condition factor, age at maturity, and fecundity were
77 observed. These may be linked to the slight differences in age and growth observed with geographic variation (see Chapter 1). Ebert et al. (2008b) suggested the existence of discrete west and south coast populations of several South African skates species due to differences in size or size at maturity. Size at maturity increased with latitude in
Leucoraja erinacea, although it was not observed in its congener L. ocellata (Frisk and
Miller 2009). In Sphyrna tiburo, life history traits, including asymptotic size, and size/age at maturity, varied by latitude (Lombardi-Carlson et al. 2003). Latitudinal gradients also have been observed in teleosts, attributed to clines in growth rate (Vinagre et al. 2009), onset of spawning season (Vinagre et al. 2009), and asymptotic length (Gertseva et al.
2010).
Evidence indicates that B. aleutica, like B. parmifera, depend on the stable environment at nursery sites along the shelf-slope interface for successful reproduction
(Hoff 2007). Though some rajids move to shallower depths for egg deposition (Steven
1936), B. aleutica nursery sites are found in deeper waters. Egg cases were found at maximum densities in two nesting sites in the EBS at 320 and 380 m depth (Hoff 2010).
Fadeev (2005) found that in Russian waters, adult B. aleutica concentrate at depths of
250-550 during the summer, and gather at deeper depths of 470-700 m during the winter, whereas young (<1 year old) stay on the continental shelf. Greater concentrations of gravid females and small juveniles of B. albomaculata at slightly deeper depths also indicate spawning in deeper waters (Henderson et al. 2005).
The reproductive cycle of oviparous species was generally described as “year- round egg production with seasonal periods when a greater proportion of adult females
78 are laying eggs” (Hamlett and Koob 1999). Three types of reproductive cycles have been described for skates: 1) a well-defined annual or biennial cycle, 2) a partially defined annual cycle with one or two peaks, and 3) reproductively active throughout the year
(Wourms 1977). Species with defined annual cycles include Raja eglanteria, with a gravid period occurring only between January and mid-July (Rasmussen et al. 1999).
Sympterygia bonapartii also may be a seasonal breeder, as egg cases were present only during summer months (Mabragaña et al. 2002). Partially defined reproductive cycles were observed in Raja clavata (Holden 1975), Leucoraja garmani (McEachran 1970), and Psammobatis normani (Mabragaña and Cousseau 2004). Both defined and partially defined annual cycles were observed in Leucoraja erinacea, in which most females were gravid either in summer or late fall, whereas a small proportion of the population was gravid year round (Bigelow and Schroeder 1953).
Many skates appear to be reproductively active throughout the year with no evident seasonality. These include several deeper water skates, such as Leucoraja garmani (McEachran 1970), Bathyraja albomaculata (Ruocco et al. 2006), and B. trachura (Davis et al. 2007). Evidence of year-round reproduction (e.g. GSI, continuous egg deposition and hatching) also was observed for B. parmifera from the GOA and EBS
(Matta 2006; Hoff 2007). The lack of seasonal reproduction may be attributed to the relatively stable environmental conditions experienced by skates in the deep sea.
Although reproductive data for B. aleutica were limited, the presence of gravid females from June through September indicated at least an extended reproductive season.
Histological data indicated males with mature spermatocysts also were present through
79 all sampled months, but monthly data were inadequate to fully describe the seasonality of spermatogenesis. Additional sampling including expanded histological analyses, gonadosomatic and hepatosomatic indices, or hormonal assays may be needed to further evaluate reproductive seasonality (Parsons and Grier 1992; Tricas et al. 2000; Sulikowski et al. 2005b).
The ability to store sperm in the oviducal glands enhances reproductive success in elasmobranchs, particularly in nomadic species or those with low densities (Hamlett et al.
1998; Pratt 1993). Among skates, sperm storage was indicated by the production of fertilized eggs in the absence of males for five weeks in Raja brachyura (Clark 1922) and at least three months in Raja eglanteria (Luer and Gilbert 1985). Though spermatozoa were present in the oviducal glands of female Bathyraja albomaculata, long-term sperm storage was not observed (Henderson and Arkhipkin 2010). Analysis of reproductive tracts for the presence of stored sperm may provide more insight on the reproduction of
B. aleutica.
CONCLUSIONS
Moderate growth to large maximum size, late size and age at maturity, and low fecundity were all observed in the Aleutian skate, Bathyraja aleutica. Like many other elasmobranchs, these characteristics categorize B. aleutica as equilibrium (K) strategists
(Winemiller and Rose 1992). Because of this strategy, these species tend to have low maximum sustainable yields and recover slowly from overexploitation (Adams 1980;
Walker and Hislop 1998). The effects of fishing pressure on abundance, distribution, and
80 population structure have been documented in several skates (Brander 1981; Casey and
Meyers 1998; Agnew et al. 2000; Stevens et al. 2000; Dulvy and Reynolds 2002).
The life history traits of B. aleutica were generally similar between sexes and between EBS and GOA ecosystems. The possibility of a lower reproductive potential in skates from the GOA, however, indicate that they may be more vulnerable to fishing pressure than those from the EBS. Although skates from the GOA reached 19 yrs, they mature later in life than skates from the EBS, and actually have 1 less year of potential reproductive viability.
Federal management of skates continues by region in the BSAI and GOA.
Beginning this year, skates from the BSAI will be removed from the “Other species” category and managed as a single complex with skate-specific allowable biological catch
(ABC) and overfishing limits (OFL; Ormseth et al. 2010). Although skates will not yet be managed at a species level, as it is for Raja rhina and R. binoculata in the GOA, this is a step towards reducing uncertainty in skate catch. Management of skates also occurs in state waters in the GOA, primarily around Kodiak Island and Prince William Sound. The
Alaska Department of Fish and Game has the authority to define seasons, establish minimum fishing depths, and require other conditions deemed necessary for conservation and management purposes (Sagalkin et al. 2010).
Improvements to management have included species identification. Initiated in
2003 by the AFSC Observer program, species identification has moved away from “skate unidentified”, however, about 50% of skate catch remains unidentified to species level
(Ormseth et al. 2010). Misidentification of skates in Alaska with may be improved with
81 genetic identification (Spies et al. 2006). The importance of species level identification was apparent in Dipturus batis, for which Iglésias et al. (2009) stated erroneous taxonomic confusion exacerbated its extinction risk and that of its species-complex by masking species-specific declines.
Among 13 skate species occurring throughout Alaska, Stevenson et al. (2008) found B. aleutica produced the highest mean densities in the Bering Sea slope region, in comparison to the Bering Sea shelf, Aleutian Islands and GOA. Bottom trawl survey estimates indicated that B. aleutica is the second most abundant skate in Alaskan waters
(B. parmifera being the most abundant), with a mean density of 21 skates/km2, and a maximum of 3,910 skates/km2 on the Bering Sea slope (Stevenson et al. 2008). B. aleutica dominated the biomass in the EBS slope, accounting for 46% of the biomass in
2008 (17,160 tons; Ormseth et al. 2010). Among surveys in the GOA, B. aleutica is the
3rd most abundant species, accounting for 19% of the biomass overall, and 76% of all skates excluding Raja sp. (21,134 tons; Ormseth and Matta 2010). Observers estimate that B. aleutica accounts for 6.6% of the total BSAI catch, however this may not reflect true catch composition due to selective retention of larger species or greater likelihood of identifying distinctive species (Ormseth et al. 2010).
With the recent reemergence of directed skate fisheries in Alaska, and the continued presence of skates as bycatch in trawl and longline fisheries, the importance of conservative management is emphasized. Several species primarily taken as commercial bycatch have experienced dramatic declines in population size (Ebert and Winton 2010).
Of particular concern is unevaluated rajids that could become targets of developing
82 fisheries, as fishers look to alternative and bycatch species in the face of declining stocks of traditional species (Ebert et al. 2007). Also, in mixed-species fisheries, long-lived animals would suffer the greatest threats as they could become depleted as the more productive species continues to be fished (Musick 1999). As several chondrichthyan species have proven unsustainable in the past, data from my study should be considered in augmenting current management strategies or developing new fishery management plans.
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92 Table 1. Maturity stages of female and male skates as determined by macroscopic inspection of reproductive organs.
Stage Female Male
Juvenile Ovaries white and undifferentiated; Testes white and undifferentiated; oviducal glands undeveloped and epididymides thin and filamentous; not distinct from uteri claspers short and flexible and do not extend past pelvic fins
Adolescent Ova small and clear; oviducal Testes becoming lobular; glands poorly developed; uteri epididymides thickening and loosely narrow and constricted coiled; claspers extend past pelvic fins but terminal cartilage elements not calcified
Adult Ova large, yellow, and vascularized; Testes lobular; epididymides highly oviducal glands distinct from uteri; coiled; claspers fully calcified and uteri thick and pendulous elongate
Gravid Egg cases present in utero N/A
TABLES
93
FIGURES Figure 1. Stages III through VI of spermatogenesis used to classify spermatocysts in Bathyraja aleutica at 200× magnification following Maruska et al. (1996): a) stage III spermatocytes; b) stage IV spermatids; c) stage V immature spermatozoa; and d) stage VI mature spermatocysts. Bar = 100 µm.
94 EBS
GOA
Figure 2. Length frequencies of Bathyraja aleutica used for reproductive analysis. Skates were examined from fishery independent surveys, fishery landings, and fisheries observer samples, 2004-2007. Top: eastern Bering Sea females (n=320) and males (n=298); and bottom: Gulf of Alaska females (n=280) and males (n=177).
95
Figure 3. Relationships between total length and mass in Bathyraja aleutica plotted by sex and region. There were no differences between these relationships between sexes or regions, therefore, data were pooled (n=326; r2=0.943).
96
EBS
GOA
Figure 4. Linear relationships between total length and disc width of Bathyraja aleutica plotted by sex for the eastern Bering Sea (top) and Gulf of Alaska (bottom). Sexes were pooled for both EBS (n=586, r2 = 0.995) and GOA (n=462, r2 = 0.984).
97 EBS
GOA
Figure 5. Relationships between oviducal gland width and total length for female Bathyraja aleutica from the eastern Bering Sea (top; n=266) and Gulf of Alaska (bottom; n=270).
98 EBS
GOA
Figure 6. Relationships between uterus width and total length for female Bathyraja aleutica from the eastern Bering Sea (top; n=258) and Gulf of Alaska (bottom; n=257).
99 EBS
GOA
Figure 7. Relationships between inner clasper length and proportion of mature spermatocysts with total length for mature male B. aleutica from the eastern Bering Sea (top; n=278) and Gulf of Alaska (bottom; n=171).
100 EBS
GOA
Figure 8. Estimated size at maturity for female and male Bathyraja aleutica from the eastern Bering Sea (top) and Gulf of Alaska (bottom). The dashed lines represent the 95% confidence intervals for female (red) and male (blue) ogives. The black line represents 50% maturity.
101
EBS
GOA
Figure 9. Estimated age at maturity for female and male Bathyraja aleutica from the eastern Bering Sea (top) and Gulf of Alaska (bottom). The dashed lines represent the 95% confidence intervals for female (red) and male (blue) ogives. The black line represents 50% maturity.
102
Figure 10. Comparison between the total number of mature ova in left and right ovaries for female Bathyraja aleutica from the eastern Bering Sea (top; n=11) and Gulf of Alaska (bottom; n=54). 45º line represents 1:1 agreement in ova counts.
103 EBS
GOA
Figure 11. Relationships between total number of mature ova and maximum ovum diameter (MOD) with total length for female Bathyraja aleutica from the eastern Bering Sea (top) and the Gulf of Alaska (bottom). Regressions for total number of mature ova (black line): EBS n=11, GOA n=54; and MOD (dashed line): EBS n=15, GOA n=69.
104 EBS
GOA
Figure 12. Relationships between total number of mature ova and maximum ovum diameter with estimated age for female Bathyraja aleutica from the eastern Bering Sea (top) and the Gulf of Alaska (bottom). Regressions for total number of mature ova (black line): EBS n=5, GOA n=19; and MOD (dashed line): EBS n=8, GOA n=29.
105 EBS
GOA
Figure 13. Proportion of gravid female Bathyraja aleutica by month from the eastern Bering Sea (top) and Gulf of Alaska (bottom). Numbers below the bars represent monthly sample size.
106
EBS
GOA
Figure 14. Monthly changes in spermatogenesis in adult male Bathyraja aleutica from the eastern Bering Sea (top) and Gulf of Alaska (bottom). Stage III, spermatocytes; stage IV, spermatids; stage V, immature spermatozoa; and stage VI and VII, mature spermatocysts and spermatogonia. Numbers below bars represent monthly sample size.
107