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2009 SOUTHEASTERN NATURALIST 8(1):55–70
Aspects of the Reproductive Biology of the Skate
Fenestraja plutonia (Garman) off North Carolina
Andrea M. Quattrini1,2,*, Melissa L. Partyka1,3, and Steve W. Ross1
Abstract - Fenestraja plutonia is an abundant member of the slope community
in the western North Atlantic, occurring at depths of 293–1042 m. Aspects of the
reproductive biology of F. plutonia were examined for specimens collected off
North Carolina, in the summer–fall of 2001, 2002, and 2006. Male-to-female sex
ratios were not significantly different from 1:1. The smallest mature male was 215
mm TL, and the smallest mature female was 230 mm TL. Length at 50% maturity
was estimated at 231 mm TL for females and 233 mm TL for males, 89 and 90% of
maximum TL, respectively. Deposited egg cases (n = 107; six containing embryos),
three egg-bearing females, and 11 newly hatched juveniles were collected. It appears
that the upper slope off Cape Lookout, NC, at the northern end of the species range,
constitutes both an egg-laying area and possibly a nursery area for this species.
Skates (Family Rajidae) are a common component of continental shelf
and slope demersal communities throughout the world (e.g., Ebert 2005). An
increased global concern about fisheries (including bycatch) impacts on the
population structure, abundance, and distribution of skates has lead to recent
increases in biological and ecological studies of skates (Ebert and Sulikowski
2007). However, life-history data exist mostly for larger and/or economically
important species (e.g., Ebert 2005, Gedamke et al. 2005, Henderson et al.
2005, Ruocco et al. 2006, Sulikowski et al. 2005a). Very little is known about
the ecology and biology of the deeper living (>200 m) and smaller (<400
mm total length) members of this family (Sulikowski et al. 2007a), such as
Fenestraja plutonia (Garman) (Pluto Skate; Compagno 2005).
Fenestraja plutonia is one of the smallest skate species found in the western
North Atlantic (McEachran 2002, McEachran and de Carvalho 2002),
reaching a maximum recorded total length of only 275 mm (Bigelow and
Schroeder 1968). It occurs at depths of 293–1042 m (McEachran and de
Carvalho 2002) and appears to be abundant on the upper continental slope.
Fenestraja plutonia occurs from North Carolina to the Florida Keys (Bigelow
and Schroeder 1953, 1962), off Cuba (Claro and Parenti 2001), in the northeastern
Gulf of Mexico, off the Bahamas, Costa Rica, and the northern coast
of South America (McEachran and de Carvalho 2002). Ross and Quattrini
(2007) commonly observed this species near deep coral banks off the southeastern
US (SEUS: North Carolina to Florida), especially off North Carolina.
1University of North Carolina Wilmington, Center for Marine Science, 5600 Marvin
Moss Lane, Wilmington, NC 28409. 2Current address - Biology Department, Temple
University, 1900 N 12th Street, Philadelphia, PA 19460. 3Current address - NOAA
MOC-P, 1801 Fairview Avenue E, Seattle, WA 98102. *Corresponding author - quattrini@
56 Southeastern Naturalist Vol. 8, No. 1
In the western North Atlantic, most research on skates has focused on
species north of Cape Hatteras, NC, while little biological and ecological
information exists for species inhabiting SE US and Gulf of Mexico waters.
With the exception of taxonomic accounts, and the comprehensive studies
on Raja eglanteria Bosc (Clearnose Skate) in captivity (e.g., Luer and
Gilbert 1985, Luer et al. 2007) and Raja texana Chandler (Roundel Skate;
Sulikowski et al. 2007b), only basic biological information (e.g., size ranges,
male maturity sizes, egg case descriptions) exists for many species in the
region (e.g., Bigelow and Schroeder 1953, 1962, 1968; McEachran and de
Carvalho 2002). Recent cruises off North Carolina to assess slope fish and invertebrate
assemblages yielded F. plutonia specimens (and their egg cases) in
various reproductive stages, including advanced embryos and newly hatched
juveniles. These collections provided the opportunity to describe life-history
characteristics of this species. While more extensive sampling would be
preferred, trawl surveys on the SE US slope (>200 m) are rare. Therefore,
we hope that these data, though limited, contribute to the knowledge of skate
life histories by providing information on one of the smallest members of the
family. In addition, we hope to stimulate research on the ecology and biology
of other poorly known deep-water species of the region.
The Cape Lookout coral banks, located ≈75 km off Cape Lookout, NC
(Fig. 1), are the northernmost deep coral banks along the SE US slope, and
are formed by the deep- or cold-water coral Lophelia pertusa (L.) (Ross
and Nizinski 2007). The reefs rise as much as 80–100 m above the seafl oor
and are surrounded at their bases by soft substrata mixed with coral or rock
rubble. Mean bottom temperatures in these areas were 5.8–10.9 ºC, while
mean bottom salinities were 35.0–35.4 (Ross and Quattrini 2007). Thirty otter
trawl tows were conducted around the coral banks in low-relief reef (n =
15 tows) and non-reef (n = 15 tows) habitats (356–504 m) during summer–
fall of 2001, 2002, 2004, and 2006 (Fig. 1, Table 1). An additional tow was
completed east of the Cape Lookout B area in 2004 in deeper (657–910 m)
off-reef habitat (Fig. 1). Prior to trawling, the area was surveyed with sonar
so that trawls avoided major coral areas; however, the trawling objective was
to tow as close to coral mounds as possible. The otter trawl (4.9-m head rope,
38.1-mm mesh) was towed for 29–45 min at ≈2 knot (3.7 km/hr) ground
All skates and egg cases were preserved at sea in 10% formalin seawater
solution and later transferred to 40% isopropanol. Preserved skates were
identified, sexed, weighed (W) to the nearest 0.1 g, and measured to the
nearest mm total length (TL) and disk width (D). During the August 2001
cruise, 20 specimens were measured (D, Table 1) and discarded at sea; therefore,
these specimens were excluded from analyses. Left and right claspers
were measured (mm) from the point of insertion at the cloaca to the tip (inner
clasper length; LC), and the larger of the two LC were used in analyses.
2009 A.M. Quattrini, M.L. Partyka, and S.W. Ross 57
For each individual, either testes or ovaries were weighed to the nearest
0.001 g to calculate total gonad weights for males (TW) and females (OW),
respectively. Oviducal gland width (mm) was measured across the widest
section of the gland, perpendicular to the oviduct (following Gedamke et al.
2005). Egg cases were measured in length and width (mm), excluding the
horns; the horns were measured separately for egg cases that were intact. We
determined that egg cases collected with the otter trawl were from F. plutonia
because: 1) identical egg cases were present in egg-bearing females,
Figure 1. Otter trawl tows (summer–fall, 2001–2006) at the Cape Lookout A and B
deep coral areas off North Carolina (NC).
58 Southeastern Naturalist Vol. 8, No. 1
2) F. plutonia embryos were found within trawled egg cases, and 3) measurements
and description of egg cases closely follow Bigelow and Schroeder’s
Sexual maturity was determined for each individual using criteria based
on previous studies (e.g., Ebert 2005, Henderson et al. 2005, Walmsley-Hart
et al. 1999). Immature females had undifferentiated, thin, leaf-like ovaries,
undeveloped oviducal glands, and thread-like oviducts and uteri. Maturing
females were identified by the presence of small (≤1 mm diameter) white
oocytes in the ovaries, developing oviducal glands, and narrow oviducts
and uteri. Mature females had ovaries that contained small to large (<4 mm
diameter) oocytes with one to four of the larger (3–4 mm) ones yolked. They
also had developed oviducal glands, thickened and tubular oviducts, and
uteri that were thickened or obviously stretched. Maturity criteria were supported
by measurements taken from the mature females that had egg cases
in their reproductive tracts. Males were determined to be immature if their
claspers were fl exible, not fully calcified, and did not extend past the posterior
margin of the pelvic fins. Epididymides and vasa deferentia in immature
males were thin and undeveloped. Maturing males possessed claspers that
extended beyond the pelvic fins and were not fully calcified; epididymides
and vasa deferentia were thickened, but were not fully coiled. Males were
classified as mature when claspers were both elongated and fully calcified
and alar thorns were well developed. Mature males had fully developed testes
and thickened, fully coiled epididymides and vasa deferentia.
Table 1. Fenestraja plutonia data from three cruises conducted off North Carolina. I = immature,
A = maturing, M = mature, and U = undetermined (specimens discarded at sea).
Total Total Disk Gonad
number length (mm) width (mm) Weight (g) weight (g) GSI
Female–I 4 176–229 72–101 15.2–37.8 0.114–0.214 0.57–0.94
Female–A* 1 216 99 32.9
Female–M 8 230–260 101–115 45.0–65.9 0.450–0.964 0.84–1.81
Male–I 1 204 89 24.5 0.162 0.67
Male–A 3 223–245 110–112 30.8–48.5 0.219–0.508 0.72–1.21
Male–M 6 230–241 110–115 44.6–62.8 0.635–0.827 1.26–1.63
U 20 57–121
Males–M 1 246 116 48.4 0.556 1.16
Female–I 18 61–245 28–109 0.7–43.9 0.002–0.234 0.21–0.76
Female–A 1 239 116 55.9 0.262 0.47
Female–M 5 232–252 106–112 49.9–61.4 0.652–1.329 1.23–2.28
Male–I 11 87–232 38–109 1.8–36.6 0.002–0.280 0.11–0.85
Male–A 5 235–247 104–115 40.0–56.3 0.257–0.559 0.58–1.00
Male–M 11 215–258 104–129 35.4–67.8 0.506–0.771 0.97–1.58
Total 95 61–260 28–129 0.7–67.8 0.002–1.329 0.11–2.28
*One ovary of this maturing female was damaged
2009 A.M. Quattrini, M.L. Partyka, and S.W. Ross 59
Male-to-female sex ratios were calculated for all specimens and also at
each maturity stage. Chi-square tests with a Yates correction (Zar 1999) were
used to determine if the ratios were significantly different from 1:1. Regressions
for D–TL (linear) and W–TL relationships (W = aTLb) were examined
for both male and female skates. Analysis of covariance (ANCOVA) was
used to test for differences in these relationships between sexes. We used the
D–TL regression to estimate the TL of skates with damaged tails (two cases).
A two-way analysis of variance (ANOVA) on log-transformed data was used
to determine whether TL and W differed between males and females at all
three maturity stages.
Reproductive data were analyzed to determine the relationship of sexual
maturity to size for both males and females. LC and TW for males and OW for
females were each plotted against TL, and TW and OW were plotted against W.
Rapid increases in these parameters relative to TL were used as indicators
of the onset of sexual maturity (e.g., Ebert 2005, Sulikowski et al. 2005a,
Walmsley-Hart et al. 1999). We also calculated the gonadosomatic index
(GSI = OW or TW / [W- OW or TW] x 100) for both males and females to provide
baseline summer–fall data for specimens off North Carolina. One male
and seven females were eliminated from gonad analyses because of damage
to the gonads. In addition, proportional maturity for each sex was calculated.
First, individuals were assigned a maturity category (binomial data: immature
= 0, mature = 1) and placed into 10-mm size classes. For each size class
per sex, we then calculated mean TL of individuals and the proportion of
mature to immature individuals. Logistic regression models of proportional
maturity versus TL were then applied to each sex to estimate length at 50%
maturity (TL50%; e.g., Roa et al. 1999). Chi-square goodness of fit was used
to test how well proportional maturity data conformed to the models.
Ninety-five F. plutonia specimens were collected at depths of 378–504 m
in 20 of the 31 otter trawl tows (356–910 m; Fig. 1). Similar numbers were
collected in August 2001 (10 tows, 43 specimens) and in September 2006
(14 tows, 51 specimens) (Table 1). Only one individual was collected out
of 4 tows in August 2002. No skates were collected in September 2001 or
June 2004, probably because of reduced trawl sampling (1 tow in September,
4 tows in June) during these cruises. Besides the collection of 11 recently
hatched individuals, six embryos, and five egg cases filled with yolk (including
one egg case that was extruded upon collection) in September 2006,
there were no other spatial or temporal patterns in the distribution of individuals
by maturity stage or sex.
Male-to-female sex ratios were not significantly different from 1:1 at any
maturity stage (all stages: χ2 = 0.00; mature: χ2 = 0.52; maturing: χ2 = 2.36;
immature: χ2 = 2.48; P > 0.05). Of the 75 skates that were sexed (20 individuals
discarded at sea), 37 were females (13 mature) and 38 were males
(18 mature). Eleven immature skates collected in September 2006 were
60 Southeastern Naturalist Vol. 8, No. 1
much smaller than all other immature individuals (>170 mm TL, 75 mm D)
and eight of these were females (61–108 mm TL, 28–42 mm D, 0.7–2.7 g)
and three were males (87–107 mm TL, 48–44 mm D, 1.8–3.3 g). D–TL relationships
were significant for both sexes (females: D = 0.47TL - 3.93, r2 =
0.99, P < 0.05; males: D = 0.49TL - 6.17, r 2 = 0.97, P < 0.05) and not significantly different (ANCOVA: F = 0.35, P > 0.05) between sexes (Fig. 2A).
W–TL relationships were also significant (females: W = 1.43X10-6 * TL3.17,
r 2 = 0.99, P < 0.05; males: W = 9.04X10-7 * TL3.25, r2 = 0.98, P < 0.05), but
Figure 2. A. Total length (TL)–disk width (D) linear relationship. B. weight (W) =
aTLb relationship in both female (open circles, dotted line, n = 37) and male (black
squares, solid line, n = 38) Fenestraja plutonia collected off North Carolina.
2009 A.M. Quattrini, M.L. Partyka, and S.W. Ross 61
there was no significant difference between males and females (ANCOVA:
F = 0.76, P > 0.05) (Fig. 2B).
All maturity stages of male F. plutonia were collected during this study.
Maturing males ranged from 223 to 247 mm TL (104–115 mm D, 30.8–
56.3 g), and the largest immature male was 232 mm TL (109 mm D, 36.6 g)
(Table 1). The smallest mature male was 215 mm TL (104 mm D, 35.4 g),
indicating first maturity at 83% of maximum TL (258 mm TL). TL50% was
233 mm (χ2 = 17.24, P < 0.05; Fig. 3), 90% of maximum TL. The relationship
of LC–TL was significant (LC = 0.825e0.016TL, r2 = 0.80, P < 0.05) with a
sharp increase in LC around 230–240 mm TL, indicating the onset of maturity
(Fig. 4A). For mature males, LC ranged from 50.0 to 60.0 mm, LC for immature
males ranged from 4.0 to 20.0 mm, and LC for maturing males were
20.0–55.0 mm. Two maturing males had LC (51 and 55 mm) within the range
of mature males. Similar to the LC–TL relationship, TW rapidly increased
around 230–240 mm TL (TW = 0.0002e0.032TL, r2 = 0.92, P < 0.05) (Fig. 4B).
TW also increased with W (TW = 0.001W1.626, r2 = 0.96, P < 0.05); however,
this was a more gradual increase than an abrupt change as observed in the
TW–TL relationship (Fig. 4C). Mature males had higher GSIs (mean = 1.24
± 0.05 SE, n = 17) compared with maturing (mean = 0.87 ± 0.07 SE, n = 8)
and immature (mean = 0.45 ± 0.06 SE, n = 12) males (Table 1).
Figure 3. Fitted logistic curves of proportional maturity (P) of Fenestraja plutonia
collected off North Carolina in relation to total length (TL) in females (open
circles, dotted line) and males (black squares, solid line). Symbols are observed
values and lines are predicted curves. TL50% is indicated on graphs with perpendicular
62 Southeastern Naturalist Vol. 8, No. 1
Figure 4. Relationships of: A. total length (TL) to clasper length (LC); B. testes
weight (TW) to TL; and C. TW to weight (W) in mature (black squares, n = 18 for LC,
n = 17 for TW), maturing (gray squares, n = 8), and immature (open squares, n = 12)
male Fenestraja plutonia collected off North Carolina.
2009 A.M. Quattrini, M.L. Partyka, and S.W. Ross 63
Females matured at relatively the same size as males. TL and W were
not significantly different (two-way ANOVA, TL: F = 0.39, W: F = 0.44,
P > 0.05) between males and females at any maturity stage. The largest
immature female was 245 mm TL (109 mm D, 43.9 g), while the two maturing
females were 216 and 239 mm TL (99 and 116 mm D, 32.9 and 55.9 g;
Table 1). The smallest mature female was 230 mm TL (101 mm D, 45.0 g),
indicating first maturity at 88% of maximum TL (260 mm TL). TL50% was
231 mm (χ2 = 27.91, P < 0.05; Fig. 3), 89% of maximum TL. OW–TL (OW
= 0.001e0.028TL; r2 = 0.92) and OW–W (OW = 0.009e0.081W; r2 = 0.85) relationships
were significant (P < 0.05; Fig. 5). There was little change in OW with
increasing size (TL or W) until ca. 230–240 mm TL and 50 g, when a sharp
Figure 5. Relationships of ovarian weight (OW) to: A. total length (TL); and B. weight
(W) in mature (black circles, n = 9), maturing (gray circles, n = 1), and immature
(open circles, n = 20) female Fenestraja plutonia collected off North Carolina.
64 Southeastern Naturalist Vol. 8, No. 1
increase indicated the onset of maturity (Fig. 5). Mature females had higher
GSI (mean = 1.50 ± 0.09 SE, n = 9) compared to immature females (mean
= 0.55 ± 0.04 SE, n = 20) (Table 1). Both ovaries of only one maturing female
could be weighed; therefore, we could not compare GSIs of maturing
individuals with other maturity stages. Oviducal glands were undeveloped
in immature individuals, while they were ca. 1% of TL (2–3 mm wide) in
maturing individuals and 4–5% of TL (10–13 mm wide) in mature and eggbearing
Three egg-bearing females were collected near the Cape Lookout deep
coral banks. Of the two females collected in September 2006 from the same
trawl, one (232 mm TL, 106 mm D, 56.8 g) had a partially developed egg
case in each uterus. Both cases were of near equal size, though the case on
the right side was not fully extruded from the oviducal gland (Fig. 6A).
Cases were yellowish-green in color, smooth with longitudinal striations,
and covered with mucus. The anterior horns (anterior to the embryo at hatching)
of both cases were folded back in loops across the ventral case surfaces.
Ovaries contained large (3–4 mm) yolky oocytes; the OW was 1.268 g and
the GSI was 2.28, the highest GSI of all females. The oviducal glands of
this female were 10 mm wide. The second egg-bearing female (235 mm TL,
105 mm D, 61.4 g) released a fully formed egg case shortly after collection.
The case was golden-brown, smooth with longitudinal striations, covered in
mucus, and filled with yolk. The right ovary was thin and defl ated (0.383 g),
while the left ovary (0.946 g) contained large (3–4 mm), yolky oocytes. Both
oviducal glands were 10 mm wide. The GSI for this individual was 2.21. The
third female (240 mm TL, 108 mm D, 53.7 g), collected in August 2001, had
an egg case present in each uterus; however, egg cases were in early stages
of extrusion with anterior horns (ca. 5 mm) of each case formed. The left
ovary of this female was damaged, but the right ovary contained large, yolky
Figure 6. Fenestraja plutonia egg cases collected off North Carolina in different
stages of development. A: Partially formed egg case removed from egg-bearing
female (232 mm TL); B: fully formed case with yolk; C: egg case with early
embryo indicated by arrow; D–G: advanced embryos with varying amounts of
2009 A.M. Quattrini, M.L. Partyka, and S.W. Ross 65
oocytes and weighed 0.872 g. The oviducal gland on the right was 10 mm
wide, while the left was 13 mm wide.
In addition to the egg cases in utero, 107 egg cases of F. plutonia were
collected by trawl during the September 2006 and August 2001 cruises near
the Cape Lookout coral banks. Cases were scattered throughout the trawl
catches, and there was no indication that they were attached to any bottom
structures. Deposited egg cases were golden to brown in color (darker than
those in utero) and smooth with longitudinal striations and had long, fl exible
anterior horns and short, stout posterior horns (Fig. 6). Egg cases ranged in
length from 20 to 25 mm (mean = 22.3 mm ± 0.1 SE) and in width from 12 to
15 mm (mean = 14.3 ± 0.1 SE). The horns on many specimens were damaged;
however, of the few that could be measured, anterior horns ranged from 25
to 28 mm and posterior horns ranged from 8 to 10 mm. Four egg cases were
filled with yolk with no visible embryos (Fig. 6B). Two others held mainly
yolk and very early embryos yet to develop typical rajoid features (Fig. 6C).
Four egg cases held embryos that were in advanced stages of development
and easily identified to species (deposited in the North Carolina Museum
of Natural Sciences Ichthyology Collection). The largest female embryo
(NCSM 47061, 41 mm TL, 20 mm D, 0.658 g; Fig. 6G) had a small amount
of yolk remaining external to the abdomen, with a large amount visible under
the abdominal wall. The smaller female embryo (NCSM 47060, 37 mm TL,
15 mm D, 0.317 g) was well developed with little yolk (Fig. 6F). The largest
male embryo (NCSM 47060, 44 mm TL, 18 mm D, 0.372 g, 2.0 mm LC) had
a small amount of yolk remaining and was partially emerged from its case
(Fig. 6E). While the smaller male embryo (NCSM 47061, 28 mm TL, 12 mm
D, 0.211 g, 2.0 mm LC) still possessed a large yolk sac (Fig. 6D), it was well
developed and possessed adult characteristics. These embryo data combined
with data on the 11 smallest juveniles collected indicated that hatching occurs
at ca. 41–61 mm TL for females and ca. 44–87 mm TL for males.
Sexual dimorphism in skates is highly variable. It is largely species
dependent and can even change among populations within the same species
(e.g., Braccini and Chiaramonte 2002; Ebert 2005; Ebert et al. 2008;
Mabragaña and Cousseau 2004; Mabragaña et al. 2002; Oddone et al.
2005; Richards et al. 1963; Ruocco et al. 2006; Sulikowski et al. 2007b;
Templeman 1987a,b). However, many species of skates show little to no
difference in size at maturity between sexes (Ebert 2005, Ebert et al. 2008,
Mabragaña et al. 2002, Matta and Gunderson 2007, Ruocco et al. 2006,
Walmsley-Hart et al. 1999). Unlike their viviparous relatives, there may
be no advantages for oviparous females to attain larger sizes to produce
larger young (Ebert et al. 2008). Also, attaining first maturity at 75–90%
of maximum TL is indicative of many species of skates and suggests that
after reaching sexual maturity, skates grow very little (Ebert 2005, Ebert et
al. 2008, Sulikowski et al. 2007b). Fenestraja plutonia fits this life-history
66 Southeastern Naturalist Vol. 8, No. 1
strategy, as both sexes matured at similar sizes at high (>80%) percentages
of maximum TL. In addition to size at maturity, F. plutonia did not exhibit
sexual dimorphism in relative sizes or disk shape. Sexual dimorphism in
disk shape occurs when male disks become more bell-shaped with maturation,
which results in differences in the D–TL relationship between sexes
(Ebert et al. 2008). In comparison to other small (<400 mm maximum TL)
skates for which reproductive data are known—Neoraja stehmanni (Hulley)
(South African Pygmy Skate; Ebert et al. 2008), Dipturus polyommata
(Ogilby) (Argus Skate; Kyne et al. 2008), and Psammobatis extenta (Garman)
(Zipper Sand Skate; Braccini and Chiaramonte 2002)—F. plutonia is
the only small species that displays a lack of sexual dimorphism in size at
maturity and relative sizes.
Some elasmobranchs segregate by size, sex, or maturity status (Pratt
1993, Springer 1967). Sexual or ontogenetic segregation was not observed
in the present study (at least not at the scale allowed by trawl sampling), as
several life stages of male and female F. plutonia were collected within the
same geographic area in the summer–fall, often within the same trawl. The
1:1 sex ratio of F. plutonia in this study is typical of many rajids (Ebert 2005;
Ebert et al. 2008; Gedamke et al. 2005; Henderson et al. 2005; Sulikowski et
al. 2005b, 2007a), and further suggests a lack of segregation at this time and
location. It is possible, however, that migration of both sexes of F. plutonia
to the Cape Lookout area occurred during the sampling period for reproductive
purposes, and size or sexual segregation could occur at other times and/
or places or at small spatial scales.
Although data on F. plutonia movements and population structure are
lacking, our data and those of Ross and Quattrini (2007) suggest that the
coral bank area off Cape Lookout, NC (at the northern end of this species’
range) represents important habitat for summer–fall reproduction. During
submersible operations (65 dives, summer–fall 2000–2005) around deep
reef areas throughout the SE US (Ross and Quattrini 2007), 52% of the
observed F. plutonia (n = 99) occurred near the Cape Lookout banks, and
both sexes were similar in size (≈100–120 mm D). This skewed distribution
of observed F. plutonia toward the slope off Cape Lookout supports the
hypothesis that the area is relatively more important than other areas, especially
considering that Ross and Quattrini (2007) surveyed deep reefs over a
700-km range in 366–783 m depths. In situ observations of egg cases (presumably
Scyliorhinus retifer (Garman) [Chain Catshark]) attached to soft
corals in 533 m in the Gulf of Mexico suggested that deep-coral areas may
be important nursery habitat for certain oviparous elasmobranchs (Etnoyer
and Warrenchuk 2007). Ebert and Davis (2007) also documented nursery
areas for two unidentified skate species in deep seamount and hardbottom
habitats with the use of in situ observations, while Richards et al. (1963)
speculated that rough, hard bottom habitats were important egg-laying areas
for Leucoraja erinacea (Mitchell) (Little Skate). Ross and Quattrini (2007)
did not observe any egg cases attached to hardbottom or deep-water corals
2009 A.M. Quattrini, M.L. Partyka, and S.W. Ross 67
along the SEUS slope. Nevertheless, F. plutonia lays eggs on or near the
Cape Lookout coral banks, as evidenced by the collections of females with
egg cases both in utero and being extruded upon collection and egg cases
in various stages of embryonic development. In addition, this area may be
a nursery area for this species, as newly hatched juveniles were collected.
More data, however, throughout this species’ range is needed to assess
whether F. plutonia lays eggs along the entire SEUS slope or in defined areas
such as off Cape Lookout.
Skate species exhibit varying patterns in reproductive cycles, such as
reproduction throughout the year, a prolonged annual cycle with periods of
increased reproductive activity, or a well-defined annual or biennial reproductive
cycle (Hamlett and Koob 1999, Richards et al. 1963, Wourms 1977).
With the exception of R. eglanteria (Fitz and Daiber 1963), western North
Atlantic skates from coastal waters north of Cape Hatteras, NC reproduce
all year long with or without peaks in reproductive activity (McEachran
1970, 2002; Richards et al. 1963; Sulikowski et al. 2004, 2005b, 2007a).
Our results indicate that F. plutonia reproduces at least in the late summer–
early fall off Cape Lookout, NC, carries a single egg case per uterus (single
oviparity), and lays two egg cases near or at the same time. Additionally, the
collection of egg cases in various stages of embryonic development, along
with very young juveniles and females with egg cases in utero may indicate
an extended breeding season and/or multiple clutches in this area. The low
GSI values for mature (and egg-bearing) female F. plutonia are comparable
(GSI range = 1.0–2.0 throughout the year) to females that reproduce all year
long, such as Amblyraja radiata (Donovan) (Thorny Skate), Malacoraja
senta (Garman) (Smooth Skate) (Sulikowski et al. 2005b, 2007a), and P.
extenta (Braccini and Chiaramonte 2002). Relatively low GSI values may
be normal for skate species that continually reproduce, compared with species
that produce large, active gonads for annual or biennial reproduction,
such as Sympterygia bonapartii Müller and Henle (Smallnose Fanskate;
Mabragaña et al. 2002). Compared to the males of A. radiata and M. senta,
male F. plutonia (and male P. extenta) exhibited high GSI values. Whether
the high GSI values of male F. plutonia and P. extenta are due to differences
in reproductive strategies (e.g., timing of sperm production, sperm storage
in females) or maximum sizes/weights is unknown.
Despite limited sampling, this study contributed information on the
biology of a poorly known species of Rajidae that occurs off the SEUS.
Previously, the only life-history information for F. plutonia included size
ranges and description of egg cases (Bigelow and Schroeder 1953, 1962,
1968). To fully assess the reproductive strategy used by F. plutonia and
other small members of Rajidae, data are needed on incubation periods, age
at first reproduction, reproductive periodicity, and growth rates. In addition,
comparative studies are needed between shallow- and deep-water skate species
in the region to assess differences in reproductive cycles and associated
environmental parameters. Since deep-water skates are a major component
68 Southeastern Naturalist Vol. 8, No. 1
of the SEUS slope benthic fauna, future research efforts should concentrate
on temporal and regional sampling to better understand the biology and ecology
of these species.
The August 2001 and September 2006 cruises were sponsored by the Duke/UNC
Oceanographic Consortium (grant to S.W. Ross), and we thank that ship’s personnel
for excellent support. NOAA Office of Ocean Exploration (grants to S.W. Ross,
lead PI) largely supported fieldwork and some data analyses. We thank M. Nizinski
(NOAA Fisheries), E. Baird (NC Museum of Natural Sciences), C. Morrison
(USGS), T. Casazza, A. Necaise, and J. McClain for help in the field and M. Peterson
and S. Artabane for assistance during manuscript development.
Bigelow, H.B., and W.C. Schroeder. 1953. Fishes of the western North Atlantic.
Sawfishes, guitarfishes, skates, and rays. Memoir Sears Foundation for Marine
Bigelow, H.B., and W.C. Schroeder. 1962. New and little known batoids fishes
from the western Atlantic. Bulletin of the Museum of Comparative Zoology
Bigelow, H.B., and W.C. Schroeder. 1968. Additional notes on batoid fishes from the
western Atlantic. Breviora 281:1–22.
Braccini, J.M., and G.E. Chiaramonte. 2002. Reproductive biology of Psammobatis
extenta. Journal of Fish Biology 61:272–288.
Claro, R.C., and L.R Parenti. 2001. The marine ichthyofauna of Cuba. Pp. 21–57,
In R.C. Claro, K.C. Lindeman, and L.R. Parenti (Eds.). Ecology of the Marine
Fishes of Cuba. Smithsonian Institution, Washington DC. 253 pp.
Compagno, L.J.V. 2005. Checklist of living Chondrichthyes. Pp. 503–548, In W.C.
Hamlett (Ed.). Reproductive Biology and Phylogeny of Chondrichthyes: Sharks,
Batoids, and Chimaeras. Science Publishers Inc., Enfield, NH.
Ebert, D.A. 2005. Reproductive biology of skates, Bathyraja (Ishiyama), along the
eastern Bering Sea continental slope. Journal of Fish Biology 66:618–649.
Ebert, D.A., and C.D. Davis. 2007. Descriptions of skate egg cases (Chondrichthyes:
Rajiformes: Rajoidei) from the eastern North Pacific. Zootaxa 1393:1–18.
Ebert, D.A., and J.A. Sulikowski. 2007. Preface: Biology of skates. Environmental
Biology of Fishes 80:107–110.
Ebert, D.A., L.J.V. Compagno, and P.D. Cowley. 2008. Aspects of the reproductive
biology of skates (Chondrichthyes: Rajiformes: Rajoidei) from southern Africa.
ICES Journal of Marine Science 65:81–102.
Etnoyer, P., and J. Warrenchuk. 2007. A Catshark nursery in a deep gorgonian
field in the Mississippi Canyon, Gulf of Mexico. Bulletin of Marine Science
Fitz, E.S., Jr., and F.C. Daiber. 1963. An introduction to the biology of Raja eglanteria
Bosc 1802 and Raja erinacea Mitchell 1925 as they occur in Delaware Bay.
Bulletin of the Bingham Oceanographic Collection 18:69–97.
Gedamke, T., W.D. DuPaul, and J.A. Musick. 2005. Observations on the life history
of the Barndoor Skate, Dipturus laevis, on Georges Bank (Western North Atlantic).
Journal of Northwest Atlantic Fishery Science 35:67–78.
2009 A.M. Quattrini, M.L. Partyka, and S.W. Ross 69
Hamlett, W.C., and T.J. Koob. 1999. Female reproductive system. Pp. 398–443, In
W.C. Hamlett (Ed.). Sharks, Skates, and Rays: The Biology of Elasmobranch
Fishes. John Hopkins University Press, Baltimore, MD. 528 pp.
Henderson, A.C., A.I. Arkhipkin, and J.N. Chtcherbich. 2005. Distribution, growth,
and reproduction of the White-spotted Skate Bathyraja albomaculata (Norman,
1937) around the Falkland Islands. Journal of Northwest Atlantic Fishery Science
Kyne, P.M., A.J. Courtney, and M.B. Bennett. 2008. Aspects of reproduction and diet
of the Australian endemic skate Dipturus polyommata (Ogilby) (Elasmobranchii:
Rajidae), by-catch of a commercial prawn trawl fishery. Journal of Fish Biology
Luer C.A., and P.W. Gilbert. 1985. Mating behavior, egg deposition, incubation
period, and hatching in the Clearnose skate, Raja eglanteria. Environmental
Biology of Fishes 13:161–171.
Luer, C.A., C.J. Walsh, A.B. Bodine, and J.T. Wyffels. 2007. Normal embryonic
development in the Clearnose skate, Raja eglanteria, with experimental observations
on artificial insemination. Environmental Biology of Fishes 80:239–255.
Mabragaña, E., and M.B. Cousseau. 2004. Reproductive biology of two sympatric
skates in the southwest Atlantic: Psammobatis rudis and Psammobatis normani.
Journal of Fish Biology 65:559–573.
Mabragaña, E., L.O. Lucifora, and A.M. Massa. 2002. The reproductive ecology and
abundance of Sympterygia bonapartii endemic to the southwest Atlantic. Journal
of Fish Biology 60:951–967.
Matta, M.E., and D.R. Gunderson. 2007. Age, growth, and mortality of the Alaska
Skate, Bathyraja parmifera, in the eastern Bering Sea. Environmental Biology
of Fishes 80:309–323.
McEachran, J.D. 1970. Egg capsules and reproductive biology of the skate Raja
garmani (Pisces, Rajidae). Copeia 1970:197–199.
McEachran, J.D. 2002. Skates. Family Rajidae. Pp. 60–75, In B.B Collette and G.
Klein-MacPhee (Eds.). Bigelow and Schroeder’s Fishes of the Gulf of Maine.
Smithsonian Institution Press, Washington, DC. 748 pp.
McEachran, J.D., and M.R. de Carvalho. 2002. Batoid Fishes. Pp. 507–589, In K.E.
Carpenter (Ed.). The Living Marine Resources of the Western Central Atlantic.
Volume 1: Introduction, Molluscs, Crustaceans, Hagfishes, Sharks, Batoid Fishes
and Chimaeras. FAO Species Identification Guide for Fisheries Purposes and
American Society of Ichthyologists and Herpetologists Special Publication No
5, FAO, Rome, Italy.
Oddone, M.C., L. Paesch, and W. Norbis. 2005. Size at first sexual maturity of
two species of rajoid skates, genera Atlantoraja and Dipturus (Pisces, Elasmobranchii,
Rajidae), from the southwestern Atlantic Ocean. Journal of Applied
Pratt, H.L. 1993. The storage of spermatozoa in the oviducal glands of western North
Atlantic sharks. Environmental Biology of Fishes 38:139–149.
Richards, S.W., D. Merriman, and L.H. Calhoun. 1963. Studies in the marine resources
of southern New England. IX. The biology of the Little Skate Raja erinacea,
Mitchell. Bulletin of the Bingham Oceanographic Collection 18:5–67.
Roa, R., B. Ernst, and F. Tapia.1999. Estimation of size at sexual maturity: An evaluation
of analytical and resampling procedures. Fishery Bulletin 97:570–580.
70 Southeastern Naturalist Vol. 8, No. 1
Ross, S.W., and M.S. Nizinski. 2007. State of deep coral ecosystems in the US
southeast region: Cape Hatteras to southeastern Florida. Pp. 233–270, In S.E.
Lumsden, T.F. Hourigan, A.W. Bruckner, and G. Dorr (Eds.). The State of Deep
Coral Ecosystems of the United States. NOAA Technical Memorandum CRCP-3.
Silver Spring, MD. 365 pp.
Ross, S.W., and A.M. Quattrini. 2007. The fish fauna associated with deep coral
banks off the southeastern United States. Deep-sea Research I 54:975–1007.
Ruocco, N.L, L.O. Lucifora, J.M. Díaz de Astarloa, and O. Wöhler. 2006. Reproductive
biology and abundance of the White-dotted Skate, Bathyraja albomaculata,
in the Southwest Atlantic. ICES Journal of Marine Science 63:105–116.
Springer, S. 1967. Social organization of shark populations. Pp. 149–174, In P.W.
Gilbert, R.F. Mathewson, and D.P. Rall (Eds.). Sharks, Skates, and Rays. John
Hopkins University Press, Baltimore, MD. 525 pp.
Sulikowski, J.A., P.C.W. Tsang, and W. Huntting Howell. 2004. An annual cycle of
steroid hormone concentrations and gonad development in the Winter Skate, Leucoraja
ocellata, from the western Gulf of Maine. Marine Biology 144:845–853.
Sulikowski, J.A., P.C.W. Tsang, and W. Huntting Howell. 2005a. Age and size at
sexual maturity for the Winter Skate, Leucoraja ocellata, in the western Gulf
of Maine based on morphological, histological, and steroid hormone analyses.
Environmental Biology of Fishes 72:429–441.
Sulikowski, J.A., J. Kneebone, S. Elzey, J. Jurek, P.D. Danley, W. Huntting Howell,
and P.C. W. Tsang. 2005b. The reproductive cycle of the Thorny Skate, Amblyraja
radiata, in the western Gulf of Maine. Fishery Bulletin 103:536–543.
Sulikowski, J.A., S. Elzey, J. Kneebone, J. Jurek, W. Huntting Howell, and P.C.W.
Tsang. 2007a. The reproductive cycle of the Smooth Skate, Malacoraja senta, in
the Gulf of Maine. Marine and Freshwater Research 58:98–103.
Sulikowski, J.A., S.B. Irvine, K.C. DeValerio, and J.K. Carlson. 2007b. Age, growth,
and maturity of the Roundel Skate, Raja texana, from the Gulf of Mexico, USA.
Marine and Freshwater Research 58:41–53.
Templeman, W. 1987a. Differences in sexual maturity and related characteristics
between populations of Thorny Skate (Raja radiata) in the Northwest Atlantic.
Journal of Northwest Atlantic Fishery Science 7:155–167.
Templeman, W. 1987b. Length-weight relationships, morphometric characteristics,
and thorniness of Thorny Skate Raja radiata from the northwest Atlantic. Journal
of Northwest Atlantic Fishery Science 7:89–98.
Walmsley-Hart, S.A., W.H. Sauer, and C.D. Buxton. 1999. The biology of the skates
Raja wallacei and R. pullopunctata (Batoidea: Rajidae) on the Agulhas Bank,
South Africa. South African Journal of Marine Science 21:165–179.
Wourms, J.P. 1977. Reproduction and development in chondrichthyan fishes. American
Zar, J.H. 1999. Biostatistical Analysis. 4th Edition. Prentice Hall, NJ. 663 pp.