age, growth, and latitudinal patterns of two rajidae ...frisk/frisk and miller, 2006.pdf ·...

Age, growth, and latitudinal patterns of twoRajidae species in the northwestern Atlantic: littleskate (Leucoraja erinacea) and winter skate(Leucoraja ocellata)

Michael G. Frisk and Thomas J. Miller

Abstract: Vertebral samples of little skate (Leucoraja erinacea) and winter skate (Leucoraja ocellata) were collectedfrom Cape Hatteras, USA, to Canadian waters to estimate age, growth, and length at weight relationships for both spe-cies throughout this range. Maximum observed age was 12.5 and 20.5 years for little skate and winter skate, respec-tively. Significant length at weight relationships were found for both species. von Bertalanffy growth curves for thenorthwestern Atlantic were estimated for little skate (k = 0.19, L∞ = 56.1 cm, t0 = –1.17, p < 0.0001, n = 236) andwinter skate (k = 0.07, L∞ = 122.1 cm, t0 = –2.07, p < 0.0001, n = 229). Additionally, latitudinal patterns in size andgrowth were observed in little skate, with individuals in northern regions growing slower and reaching a larger asymp-totic size: von Bertalanffy growth estimates (mid-Atlantic, k = 0.22, L∞ = 53.26 cm, t0 = –1.04, p < 0.0001; southernNew England – Georges Bank, k = 0.20, L∞ = 54.34 cm, t0 = –1.22, p < 0.0001; Gulf of Maine, k = 0.18, L∞ =59.31 cm, t0 = –1.15, p < 0.0001). Although differences were observed for sex-specific growth curves for both species,only winter skate curves were significantly different.

Résumé : Nous avons prélevé des échantillons de vertèbres chez la raie hérisson (Leucoraja erinacea) et la raie ta-chetée (Leucoraja ocellata) depuis le cap Hatteras, É.-U., jusque dans les eaux canadiennes afin d’estimer l’âge, lacroissance et les relations de la longueur en fonction de la masse chez les deux espèces dans cette aire de répartition.L’âge maximal observé est de 12,5 ans chez la raie hérisson et de 20,5 ans chez la raie tachetée. Il existe des relationssignificatives de la longueur en fonction de la masse chez les deux espèces. Nous avons estimé les courbes de crois-sance de von Bertalanffy pour la raie hérisson (k = 0,19, L∞ = 56,1 cm, t0 = –1,17, p < 0,0001, n = 236) et pour laraie tachetée (k = 0,07, L∞ = 122,1 cm, t0 = –2,07, p < 0,0001, n = 229) dans le nord-ouest de l’Atlantique. De plus,nous avons observé des patrons latitudinaux de taille et de croissance chez la raie hérisson; en effet, les individus desrégions nordiques croissent plus lentement et atteignent une taille plus grande à l’asymptote (Atlantique moyen, k =0,22, L∞ = 53,26 cm, t0 = –1,04, p < 0,0001; sud de la Nouvelle Angleterre et banc Georges, k = 0,20, L∞ = 54,34 cm,t0 = –1,22, p < 0,0001; golfe du Maine, k = 0,18, L∞ = 59,31 cm, t0 = –1,15, p < 0,0001). Bien que des différencesaient été observées entre les courbes de croissance spécifiques à chaque sexe chez les deux espèces, seules les différen-ces entre les courbes de la raie tachetée sont significatives.

[Traduit par la Rédaction] Frisk and Miller 1091

Introduction

Adaptation and evolution work in a framework of trade-offs where vital rates are selected to maximize individual fit-ness. In many species there is a latitudinal gradient of lifehistories wherein local populations adapt and evolve to max-imize fitness for specific environmental conditions. For in-stance, the rattlesnake (Crotalus viridis) exhibits a latitudinalgradient in both age at maturity and mortality rate (Shineand Charnov 1992). However, life history gradients and the

bioenergetics that underlie them are not always straightfor-ward. Conover and Present (1990) have proposed a“countergradient” hypothesis wherein the potential forgrowth varies inversely with latitude. Based on their workon silversides (Menidia menidia), Conover and colleaguessuggested that the shorter growth season and temperature-induced overwinter mortality at high latitudes selects forfaster growth rates. However, many marine fish species ex-hibit a latitudinal gradient where populations in higher lati-tudes exhibit slower growth, later age at maturity, increased

Can. J. Fish. Aquat. Sci. 63: 1078–1091 (2006) doi:10.1139/F06-005 © 2006 NRC Canada

1078

Received 22 February 2005. Accepted 9 November 2005. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on21 April 2006.J18571

M.G. Frisk1,2 and T.J. Miller. Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science,P.O. Box 38, Solomons, MD 20688, USA.

1Corresponding author (e-mail: [email protected]).2Present address: Marine Sciences Research Center, Stony Brook University, Stony Brook, NY 11794-5000, USA.

longevity, and likely lower population productivity (Taylor1958; Beverton and Holt 1959; Beverton 1992). Latitudinalpatterns in growth are a common feature of fish life histo-ries, despite the variation in the nature of the response ob-served.

Little skate and winter skate are both in the genusLeucoraja, yet they have diverging life histories and thepotential to exhibit latitudinal gradients. Little skate(L. erinacea) is a small species, reaching a size of 57 cm (to-tal length, TL) with moderate growth rates, whereas winterskate (L. ocellata) is larger, reaching 111 cm TL, and isslower growing (Waring 1984; Northeast Fisheries ScienceCenter (NEFSC) 2000; Sulikowski et al. 2003). Little skateand winter skate occur from North Carolina, US, to Cana-dian waters, with the centers of abundance in the southernNew England and Georges Bank regions (NEFSC 2000;McEachran 2002). Little skate is abundant in the mid-Atlantic, and both species are common in the Gulf of Maineand off the coasts of the Canadian maritime provinces(McEachran and Musick 1973; McEachran 2002).

Both species are ecologically important and constitute alarge proportion of the demersal fish biomass in the westernAtlantic (Link et al. 2002). Skates likely play an importantrole in the trophodynamics of western Atlantic ecosystemsas predators on the benthic fauna, including amphipods, crabs,small fish, shrimp, mollusks, and worms (Nelson 1993;Murdy at al. 1997). Although traditionally not targeted bythe domestic fleet, skates were targeted by foreign fleets be-fore implementation of the 200-mile (370.4 km) nationallimit in 1976 (Fogarty and Murawski 1998). Recently, skateshave become more valuable as a commercial species and arebeing landed and removed from the demersal community atgreater rates (NEFSC 2000; McEachran 2002). McEachran(2002) reported that US landings in the Gulf of Maine grewfrom 297 tonnes (t) in 1981 to 15 000 t in 1996. Similartrends have been observed on Georges Bank and southernNew England (NEFSC 2000). Skates are sought for theirmild-tasting meat, characterized by low fat and cholesterolcontent and a taste similar to that of shellfish (McEachran2002). Skate wings are sold to the European market and in-creasingly the US domestic market (McEachran 2002). Esti-mates of fishing mortality indicate that winter skate wasoverfished during the last decade (NEFSC 2000), but recentanalyses indicate that they are no longer overfished (Na-tional Marine Fisheries Service (NMFS) 2002).

Knowledge of skate life histories in the western Atlanticis increasing. However, the lack of data for some species hasmade the formulation of management policies difficult. Al-though there is little information about the vital rates ofwestern Atlantic skates compared with teleost fishes, therehas been progress in ageing many elasmobranch species, in-cluding several skates (Cailliet and Goldman 2004). SevenRajidae species have had annual band formation verified withseveral techniques, including lab-based tetracycline taggingstudies and marginal-increment, back-calculation, and size-frequency analyses (Cailliet and Goldman 2004; Natanson1993). Previous ageing studies have verified annual bandformation in both little skate and winter skate (Natanson1993; Sulikowski et al. 2003). Natanson (1993) conductedlaboratory experiments under varying temperature conditions

and verified that annual bands were formed in little skate. Herexperimental evidence suggested that temperature did nothave an impact on band formation (Natanson 1993).Natanson’s (1993) results indicated that previous estimatesof age (Richards et al. 1963; Johnson 1979; Waring 1984)were conservative in their interpretation of annuli and mayhave underestimated ages in little skate. Sulikowski et al.(2003) estimated the age of winter skate in the Gulf ofMaine and performed a successful marginal increment anal-ysis to verify annual band formation. In the Gulf of Maine,maximum marginal increment widths in winter skate oc-curred in May and minimum increment widths occurred inJuly, indicating that band formation likely occurs betweenJune and July (Sulikowski et al. 2003).

Given the increasing fishing pressure on skates, it is im-portant to understand their growth dynamics throughout thespecies’ ranges. In this project we collected little skate andwinter skate samples from over the species range to estimateregion-specific age and growth estimates. Specifically, thegoals of the study were to perform regional analyses of vitalrates covering the ranges of little skate and winter skatefrom Cape Hatteras to Canadian waters by estimating age,growth, and longevity of each species.

Materials and methods

SamplingSamples were collected during the NMFS’s annual fall

(September and October 2001), winter (February 2002),spring (March and April 2002), and summer (June, July, andAugust 2001) surveys from the National Oceanic and Atmo-spheric Administration (NOAA) R/V Albatross IV. Skateswere collected along the Atlantic coast from Cape Hatterasto Canadian waters (Figs. 1, 2). The fall, spring, and wintersurveys used a bottom trawl equipped with 1.27 cm meshliner that was towed for 30 min at 3 kn (1 knot (kn) =

© 2006 NRC Canada

Frisk and Miller 1079

Fig. 1. Location of study area along the northeastern coast of the USA.

1.852 km·h–1). Additionally, the winter survey gear wasequipped with a flat net and sweep chain. The summer sur-vey used a standard 8-ft (1 foot (ft) = 0.3048 m) New Bed-ford scallop dredge with a 2-in (1 inch (in) = 25.4 mm) ringchain bag and 1.5-in mesh webbing that was towed for15 min at 3.8 kn. Latitude and longitude were recorded foreach tow and used to provide location information for speci-mens. Total length, disk width, weight, and sex of individualskates were recorded on board the ship. Small specimens(<20 cm TL) were frozen whole at sea. Vertebral and tissue

samples of larger specimens were removed and frozen at sea.All samples were then shipped to the Chesapeake BiologicalLaboratory for further analyses. Additional little skate sam-ples were collected on 12 December 2000, 29 March 2001,and 25 May 2001 on board the F/V Tony & Jane, a 57-ftscalloper registered in Ocean City, Maryland, captained byMr. J. Eustler.

Skates >30 cm TL were identified morphologically to spe-cies. However, little skate and winter skate <30 cm TL arevery difficult to differentiate morphometrically (McEachran

© 2006 NRC Canada

1080 Can. J. Fish. Aquat. Sci. Vol. 63, 2006

Fig. 2. Locations where (a) little skate (Leucoraja erinacea) and (b) winter skate (Leucoraja ocellata) vertebrae were sampled alongthe US northeastern coast. The data are coded by region: triangles, the mid-Atlantic; circles, southern New England – Georges Bank;and squares, the Gulf of Maine.

and Musick 1973); therefore, to differentiate between thesespecies, we used a rapid PCR–RFLP (polymerase chainreaction – restriction fragment length polymorphism) assaybased on the restriction endonuclease Sty I, which generatesfragments that are easily characterized through agarose gelelectrophoresis (Alvarado Bremer et al. 2005). All skates<30 cm TL were genetically identified before further analyses.

The sampling covered the area from Cape Hatteras to theupper regions of the Gulf of Maine (Figs. 2a, 2b). Forregion-specific analyses, the areas were divided into threeregions based on potential physical features that may sepa-rate stocks. The following three regions were defined:(i) mid-Atlantic, representing areas north of Cape Hatteras tothe Hudson River canyon; (ii) southern New England – Geor-ges Bank, north of the Hudson River canyon to the outeredges of Georges Bank; and (iii) the Gulf of Maine, from theNortheast Channel southwest to Cape Cod. When perform-ing analyses of all regions combined, we will refer to the en-tire region as the northeast coast. In total, 675 male and1034 female winter skate and 1222 male and 1118 femalelittle skate specimens were collected for age, growth, and re-productive analyses (reproductive results reported in Frisk(2004)). The higher number of female winter skate likelydoes not reflect a biased population sex ratio, but rather thesampling protocol that also collected ovaries, in addition tovertebrae. Limited numbers of mature female (n = 168) andmale (n = 172) winter skate (>76 cm TL) were caught. Spec-imens for age analyses were selected to ensure coverage ofspecies, size, geographic region, and inshore and offshore ar-eas.

Length–weight analysesThe relationship between individual length and weight

was analyzed for the mid-Atlantic, southern New England –Georges Bank, and the Gulf of Maine regions. Little skatehad ample data, and comparisons were made for each regionbased on the following more refined area designationsdesigned to provide greater separation between regions:(i) mid-Atlantic was defined as the area south of latitude of38.72°N; (ii) southern New England – Georges Bank wasdefined as the area west of longitude 72.00°W and south oflatitude 41.70°N; and (iii) the Gulf of Maine was defined asthe area above latitude 42.45°N. Additionally, separate mod-els were estimated for male and female little skate. Linearregression models were fit using log10-transformed data forlength and weight (Proc REG; SAS Institute Inc. 2001).Analysis of covariance was performed in Proc GLM (SASInstitute Inc. 2001) to test for significant regional and sex-specific trends. The three regions were compared for signifi-cant differences by employing orthogonal contrasts.

Preparation of vertebral sectionsVertebral samples were cleaned of adhering tissue and the

4th and 8th vertebrae were removed. When the first com-plete vertebral section could not be identified, one of thefirst 10 was used. To aid in the cleaning process, vertebralsections were soaked in warm water for several minutes untiltissue was softened. Warm water treatment did not interferewith band appearance or composition (James Gelsleichter,Mote Marine Laboratory, 1600 Ken Thompson Parkway,Sarasota, FL 34236, USA, personal communication, 2003).

Vertebral centra were then air dried, mounted, and cutsagittally using a Isomet® low-speed saw (Buehler Ltd.,Lake Bluff, Ill.) into thin (1–2 mm) sections that were gluedto a glass slide, wet sanded with graded sand paper (250–1000 µm), and stained with Toluidine Blue. For small speci-mens (<20 cm TL), the centra were embedded in Struers ep-oxy before being sectioned.

Several techniques were evaluated to enhance the read-ability of slides, including no treatment, immersion of centrain 95% ethanol or RDO (a rapid decalcifying agent) beforedrying and sectioning, and staining (after sectioning) withRose Bengal or Toluidine Blue. The best results were ob-tained with immersion in 95% ethanol for at least 12–24 hand staining with Toluidine Blue. We had limited successpolishing sections with 0.3 µm alpha-alumina powder ascontrast was often reduced.

Ageing little skate and winter skateWe followed Natanson’s (1993) interpretation of annual

growth bands for little skate and Sulikowski et al.’s (2003)interpretation for winter skate. For each specimen, only onevertebral section was read. To estimate age and growth rela-tionships, each centrum section was read by two readers (R1and R2) without knowledge of prior age estimates or skatelength.

The following criteria were used in reading little skatevertebral sections. For most little skate sections, R1 readeach centrum twice and R2 read each centrum only once. Ifone of the two R1 readings was within 2 years of the R2reading, then the sample was kept and the average of the tworeadings in agreement was used. In some cases, the averageof the two readings by R1 equaled the single reading by R2;in this circumstance, the average of the readings by R1 wasused. In some cases, only R2 read a centrum. In these cases,it was read twice, and if the readings were within 2 years,then the average age was used. Additionally, the readabilityor quality of all little skate vertebral sections were rankedfrom 0 to 5, with 5 being very high readability and 0 indicat-ing very low readability.

Annuli are easily interpreted for winter skate up to ap-proximately 10 years, depending on the specimen. In somesamples, false rings or check marks were difficult to distin-guish from true annuli, especially for old individuals. Twoapproaches have been used to estimate the age of winterskate: (i) the “liberal read” approach, in which anything thatcan be interpreted as an annual band is counted; and (ii) the“conservative read” approach, in which only the most obvi-ous bands are counted as annuli. The liberal read approachwas adopted as our standard ageing technique. This decisionwas based on the lesson of Natanson’s (1993) validationstudy for little skate and a “precautionary” management per-spective.

To ensure that the choice of the liberal ageing techniqueas the standard did not unduly bias results, the two ap-proaches were compared. Winter skate specimens were readonce assuming a liberal criterion by R1 and R2, except for afew that were read only by R2. If R1 agreed within 3 yearsof R2 or if R2 made two readings and they agreed within3 years, then the specimen was kept for further analyses.Winter skate conservative readings were read by R2 twiceand if they did not agree within 3 years, then the specimen

© 2006 NRC Canada


was not included in growth estimates. Subsequently, the re-sulting growth curves estimated by “liberal” and “conserva-tive” readings were compared. As was done with little skate,the readability or quality of all winter skate vertebral sec-tions were ranked from 0 to 6, with 6 being very high read-ability and 0 indicating very low readability. Comparisonswere made between growth curves based on different read-ability rankings.

Ageing precision and reader biasReader precision was estimated on raw data with no culling

of specimens. Average percent error (APE) was used to esti-mate precision within and between readers. APE is given by

APE jij j

ji

R

R

X X

X=

−×

=∑1

1001

where R is the number of readings, Xij is the ith reading ofthe jth fish, and X j is the mean of readings of the jth fish(Campana 2001).

Precision estimates were made between and within read-ers R1 and R2. In addition, a third reader (R3) read a sub-sample of centra and these readings were only used forprecision estimates. Reader bias was estimated using mixedmodel analysis of variance in which readers were treatedas random variables (Proc Mixed; SAS Institute Inc. 2001).We tested the null hypothesis of no significant reader effecton estimated mean ages.

Growth analysisA von Bertalanffy growth function was fit to estimated

age and length data at capture (von Bertalanffy 1957). Thefunction took the following form:

L Ltk t t= −∞

− −( )( )1 0e

where Lt is length at age t, L∞ is the asymptotic length, t isage, t0 is the age at zero length, and k is the growth coeffi-cient. We used the average of all readings that met the pre-determined standards (above) as the basis for age in ourgrowth models. All growth models were fit in Proc Nlin(SAS Institute Inc. 2001). Because of a lack of small sam-ples in some model fits for winter skate, we assumed ahatching size of 16 cm TL and set the theoretical size at zero(t0) accordingly. Additionally, a theoretical size at zero (t0)of 11.2 cm TL was assumed for little skate in the Gulf ofMaine.

To test if growth curves differed significantly by region,the nonlinear residual sum of squares comparison method ofChen et al. (1992) was employed. Separate growth modelswere fit to data from each region and to data representing apooling of all the regions combined. The test of significanceto indicate that the individual models are a better descriptionof the data than the pooled model is given by

F

P i

P i

i

i

=

− ∑− ∑

∑∑

RSS RSSDF DF

RSSDF

where RSS is the sum of squares, DF is degrees of freedom,and individual and pooled values are indicated by the i andp, respectively. The procedure is performed by estimating anF statistic with 3 × (C – 1) degrees of freedom and compar-ing it with an F with (N – 3 × C) degrees of freedom (Chenet al. 1992), where C is the number of curves being com-pared and N is the total or pooled sample size. If significantdifferences were found between curves, Kimura’s (1980)likelihood ratio test was used to test for significant differ-ences in model parameters.

Results

Little and winter skate were collected widely throughoutthe sample domain (Figs. 2a, 2b). Results presented beloware based on species identification by morphological(>30 cm TL) and genetic (<30 cm TL) criteria. PCR–RFLPanalyses indicated that little skate dominated catches ofskate <30 cm TL. All skates less than 15 cm TL (n = 55)were little skate, 25 out of 29 skates 16–20 cm TL were lit-tle skate and 66 of 71 skates 21–39 cm TL were little skate.All winter skate <30 cm TL were caught on Georges Bankexcept one 29 cm TL winter skate caught in the mid-Atlanticregion. In contrast, little skate <30 cm TL were caughtthroughout their range.

© 2006 NRC Canada


Fig. 3. Allometric relationship between length (cm total length,TL) and weight (kg) for (a) little skate (Leucoraja erinacea) and(b) winter skate (Leucoraja ocellata). Data shown are for the USnortheastern coast separated by males (circles, broken line) andfemales (triangles, solid line).

The maximum sizes of female and male little skate werebroadly similar (Fig. 3a; Table 1). When compared betweenregions, length–weight relationships were significantlydifferent between the Gulf of Maine and Southern NewEngland – Georges Bank and the Gulf of Maine and themid-Atlantic; however, there was no significant differencebetween the mid-Atlantic and southern New England –Georges Bank (Table 1).

There was a significant allometric relationship betweenweight and length for winter skate for the northeast coast(Fig. 3b; Table 1). Females tended to be heavier at size thanmales (Table 1). However, male winter skate grew to sub-stantially larger and heavier sizes (Fig. 3b). Winter skatealso exhibited a significant length–weight relationship foreach region (Table 1). However, this relationship did not dif-fer among regions (Table 1).

Age and growth analyses were based on age determina-tions of 236 little skate and 229 winter skate from through-out their range. Sample images of sections of vertebralcentra from little skate and winter skate are shown in Fig. 4.Annual band interpretation in both species was satisfactoryover the geographic range of the species. For little skate, thepercentage of specimens by readability ranking (0–5) was asfollows: 0.9, 18.8, 36.7, 34.5, 8.3, and 0.9. For winter skate,the percentage of specimens by readability rankings (0–6)was as follows: 0.7, 8.5, 24.3, 33.8, 17.3, 13.2, and 2.2.

The largest female little skate aged was 56 cm TL longand 12 years old, whereas the largest male aged was 57 cmTL long and 12 years old. The oldest aged little skate was afemale, Tmax = 12.5 years and TL = 46 cm. The oldest indi-vidual from the mid-Atlantic was estimated to be 11 yearsold, and all other individuals 11 years old or older camefrom southern New England – Georges Bank and the Gulf ofMaine regions.

The largest female winter skate aged was 90 cm TL longand the largest male aged was 107 cm TL long. The oldestfemale winter skate was 76 cm TL long and was estimatedto be 19.5 years old, and the oldest male was 74 cm TL longand was estimated to be 20.5 years old. We note in passingthat a male 88 cm TL long was assigned an age of 24 yearsby one reader but the other reader did not agree with this age(R1 age = 24, R2 age = 20) and so age estimates for this in-dividual were not included in analyses.

Between readers R1 and R2, 99% of their estimates of lit-tle skate age were within 2 years. The little skate APE preci-sion estimate across readers was 20.1% (n = 137; R1, tworeadings; R2, one reading) and within-reader precision was11.6% (n = 35; R2, three readings). No significant differ-ences were found in reader bias for little skate (reader–fishinteraction, F[1,101] = 1.28, p = 0.10).

Eighty percent of the R1 and R2 readings of winter skatespecimens were within 3 years of age. The winter skate APE

© 2006 NRC Canada


n Wmax (g) Lmax (cm) Intercept Slope F p

Little skateRegions

NE coast 2356 1.19 57 –5.42 3.12 54796.5 0.0001Mid 1093 0.84 53 –5.41 3.12 23547.3 0.0001SNE–GB 1209 1.19 55 –5.42 3.12 31603.3 0.0001GOM 54 1.14 57 –5.82 3.35 1407.39 0.0001

Male 1119 1.14 57 –5.39 3.10 27865.5 0.0001Female 1223 1.19 56 –5.41 3.12 24277.1 0.0001Contrasts

GOM vs. MID 9.28 0.002GOM vs. SNE–GB 9.13 0.003MID vs. SNE–GB 0.01 0.904

Winter skateRegions

NE coast 1713 10.28 111 –5.73 3.33 84371.0 0.0001Mid 121 7.21 94 –5.70 3.33 5236.9 0.0001SNE–GB 1555 10.28 111 –5.73 3.33 80215.5 0.0001GOM 37 8.81 99 –5.75 3.35 881.5 0.0001

Male 676 10.28 111 –5.65 3.28 43340.4 0.0001Female 1035 6.53 93 –5.82 3.39 44381.2 0.0001Contrasts

GOM vs. MID 0.090 0.762GOM vs. SNE–GB 0.010 0.909MID vs. SNE–GB 0.110 0.735

Note: n, sample size; Wmax, largest individual weight; Lmax, longest skate (total length, TL); F, estimated Fstatistic; p, test probability. Also provided in the table are orthogonal contrasts for tests for regional differencesin weight–length relationships. NE coast, region-wide estimates; Mid, mid-Atlantic; SNE–GB, southern NewEngland – Georges Bank; GOM, the Gulf of Maine.

Table 1. General linear model results for little skate (Leucoraja erinacea) and winter skate(Leucoraja ocellata) regional weight vs. length relationships.

precision estimate across readers was 18% (n = 40; R1, onereading; R2, one reading; R3, one reading) and 8.0% withinreader (n = 46; R3, three readings). There was no significantreader bias between R1 and R2 (reader–fish interaction,F[1,106] = 0.86, p = 0.71).

Little skate growth models were estimated for the north-east coast, mid-Atlantic, southern New England – GeorgesBank, and the Gulf of Maine (Fig. 5; Table 2). Parameters ofthe von Bertalanffy model were highly correlated (Table 3).Because no age-0 little skate were caught in the Gulf ofMaine, growth curves for this region were fit with a t0 fixedto correspond to the hatch size estimated for the northeastcoast overall (11.2 cm TL). Growth rates (k) declined andasymptotic length (L∞) increased with latitude for little skate

(Fig. 6). However, only the pairwise comparisons betweenthe Gulf of Maine and the Mid-Atlantic were significantbased on the Chen et al. (1992) residual sum of squares test(Gulf of Maine vs. mid-Atlantic, F[3,146] = 2.87, p = 0.04;Gulf of Maine vs. southern New England – Georges Bank,F[3,137] = 2.30, p = 0.08; southern New England – GeorgesBank vs. mid-Atlantic, F[3,189] = 0.19, p = 0.90).

Male little skate appear to grow slower and reach a largersize than females (Fig. 7; Table 2). However, there were nosignificant differences between sex-specific curves (residualsum of squares: male vs. female, F[3,219] = 2.14, p = 0.10).Comparisons of the results presented here with those of pre-vious studies on little skate are shown in Fig. 8. Work con-ducted in Long Island and Block Island sounds and the

© 2006 NRC Canada


Fig. 4. Sample images of sections of vertebral centra: (a) a winter skate (Leucoraja ocellata) with total length (TL) = 55 cm, age =4 years, readability = 6; (b) a winter skate with TL = 63 cm, age = 9–10 years, readability = 5; and (c) a little skate (Leucorajaerinacea) centrum section (TL = 53 cm, age = 11–12 years, readability = 4).

southern New England – Georges Bank regions all showhigher growth rates and shorter longevities (Richards et al.1963; Johnson 1979; Waring 1984). However, a more recentstudy (Natanson 1993), which included lab validation ofgrowth bands, found ages and growth rates that were moresimilar to those of the present study.

Winter skate growth was estimated for the northeast coastonly (Fig. 9; Table 2) because sample coverage was notadequate for region-specific models. Parameter estimates ofthe von Bertalanffy model were highly correlated (Table 3).

Males were significantly larger at age than females(Fig. 10). Significant differences were found between thegrowth models for male and female winter skate (residualsum of squares: male vs. females, F[3,198] = 2.78, p = 0.042).

von Bertalanffy growth estimates for winter skate usingthe conservative read approach provided similar results tothose obtained with the liberal read approach (Fig. 11; Ta-ble 2). The maximum observed age from conservative read-ings (Tmax = 15) was lower than that from liberal readings(Tmax = 20.5), although the sizes at age were generally simi-

© 2006 NRC Canada


Fig. 5. von Bertalanffy growth model fit to length (cm total length, TL) and age (years) data for little skate (Leucoraja erinacea). Thefigure shows data for the US northeastern coast (solid line), mid-Atlantic (circles), southern New England – Georges Bank (triangles),and Gulf of Maine (diamonds) regions.

L∞ (cm) k (year–1) t0 (years) F p n

Little skateNE coast 56.10 0.19 –1.17 694.18 0.0001 236Male 60.13 0.17 –1.16 271.98 0.0001 94Female 53.94 0.20 –1.22 326.61 0.0001 125Mid 53.26 0.22 –1.04 274.12 0.0001 99SNE-GB 54.34 0.20 –1.22 233.83 0.0001 90GOMa 59.31 0.18 –1.15 3806.0 0.0001 47Winter skateNE coast 122.10 0.07 –2.07 289.5 0.0001 229Malea 115.92 0.08 –1.88 1345.8 0.0001 75Femalea 114.10 0.07 –2.10 2604.0 0.0001 126HRa 111.43 0.09 –1.80 2016.8 0.0001 75Conservative 109.78 0.10 –1.50 5120.2 0.0001 239GOMb 131.40 0.064 –1.53 209

Note: NE coast, region-wide estimates; L∞, asymptotic size; k, growth coefficient; t0, theoretical sizeat hatch; F, estimated F statistic; p, test probability; n, sample size. Regions: Mid, mid-Atlantic; SNE–GB, southern New England – Georges Bank; GOM, the Gulf of Maine. HR, higher readability; Conser-vative, conservative read. Note that the liberal read approach was used to estimate NE coast and allmodel fits except the conservative approach.

aModel was fit with t0 set to equal sizes at hatch of 11.2 and 16 cm (total length, TL) for little skateand winter skate, respectively.

bValues were not provided. Instead, r2 = 0.95 and standard error (SE) = 0.001 were provided (datafrom Sulikowski et al. 2003).

Table 2. Little skate (Leucoraja erinacea) and winter skate (Leucoraja ocellata) growthparameters.

lar. The growth curve for the conservative readings fit didnot flatten out as much as the model for the liberal readingsfit. Differences between the conservative reading fit and the

liberal reading fit were significant (residual sum of squares:conservative vs. liberal, F[3,465] = 22.4, p = 0.0001).

A growth curve for specimens ranked as high readability(HR = 4–6) was estimated for winter skate. There was not asignificant difference between higher readability and the NEcoast readings (Fig. 11; Table 2; residual sum of squareresults: HR vs. NE coast, F[3,301] = 1.83, p = 0.14). vonBertalanffy model parameters estimated were similar betweencurve fits for high readability (4–6) and data for all readabil-ity rankings (0–6). All three interpretations of annuli providesimilar growth and asymptotic size estimates.

Discussion

Little skate follows a latitudinal gradient of increased sizeand longevity and decreased growth rate with increasinglatitude (Taylor 1958; Beverton and Holt 1959; Beverton1992). Little skate from northern regions were larger butgrew more slowly than little skate from more southern

© 2006 NRC Canada


L∞ t0 k

Little skateL∞ 1.00 –.67 –0.96t0 1.00 0.81k 1.00Winter skateL∞ 1.00 –0.83 –0.99t0 1.00 0.90k 1.00

Note: L∞, asymptotic length; t0, theoretical age atzero length; k, growth coefficient.

Table 3. Correlations between parameter esti-mates of the von Bertalanffy growth equationfor the northeast region.

Fig. 6. Relationships between von Bertalanffy asymptotic size (L∞, broken line) and Brody growth coefficient (k, solid line) shown forlittle skate (Leucoraja erinacea) from three regions.

Fig. 7. von Bertalanffy growth model fit to length (cm total length, TL) and age (years) data. The figure shows data for male (opencircles, broken line) and female (closed circles, solid line) little skate (Leucoraja erinacea) for the US northeastern coast.

regions. Richards et al. (1963) reported that total length inlittle skate increased with increasing latitude. Their resultsindicated that little skate from southern New England andDelaware Bay averaged 47 cm TL and 43 cm TL, respec-tively (Richards et al. 1963). Other elasmobranchs haveshown similar variation in vital rates among localities andlatitudes. Parsons (1993) compared populations of thebonnethead shark (Sphyrna tinburo) from temperate (morenortherly) and tropical regions and found that individuals

from the temperate population grew slower but reachedlarger sizes. Yamaguchi et al. (1998), studying the star-spotted dogfish (Mustelus manazo), reported significant dif-ferences in vital rates between regions in the Japan Sea andPacific Ocean. Although starspotted dogfish populationsfrom areas with the greatest temperature differences showedthe greatest differences in growth rate, the populations fromgeographically intermediate sites showed evidence against atemperature effect.

© 2006 NRC Canada


Location k t0 L∞ Lmax Tmax Author

BIS and LIS 0.27 –0.98 52.69 54 8 Richards et al. 1963LIS 0.31 –0.29 60.88 52 5 Johnson 1979SNE-GB 0.36 –0.43 52.32 53 8 Waring 1984NE coast 0.20 –1.11 55.79 57 12.5 Present study

Fig. 8. Comparison of current estimates of growth rates for little skate (Leucoraja erinacea) with previous studies. Growth models areshown for US northeastern coast (solid line) (present study) compared with studies on little skate from southern New England –Georges Bank (dotted line) (SNE-GB), Block Island Sound (dashed line) (BIS), Long Island Sound (dashed-dotted line) (LIS),and Natanson’s (1993) laboratory data. Comparison of growth models of little skate:

Fig. 9. von Bertalanffy growth model fit to length (cm total length, TL) and age (years) data for winter skate (Leucoraja ocellata).The figure shows data for the US northeast coast (solid line), mid-Atlantic (circles), southern New England – Georges Bank (triangles),and Gulf of Maine (diamonds) regions.

Large size, longevity, and slow growth are common indi-cators that a species is vulnerable to overexploitation and oflow population productivity (Frisk et al. 2001, 2002). Withinelasmobranchs, low productivity has been associated withpopulation declines. For example, the more productivegummy shark appeared resilient, whereas the less productiveschool shark experienced a population decline in the samefishery (Stevens 1999). We suggest that as little skate popu-lations at higher latitudes likely have slower growth, in-creased longevity, and lower productivity, these populationsare likely more susceptible to declines under exploitation.

Winter skate specimens were relatively few in comparisonwith little skate, and as a result, we were unable to conductregional growth analyses for the former. A comparison ofthe growth curves estimated for winter skate in this studywith those of Sulikowski et al. (2003) provide some evi-dence that winter skate may grow slower and attain a largersize in higher latitudes. Additionally, McEachran and Martin(1977) reported that larger individuals of winter skate are

more common in higher latitudes. However, Simon andFrank (1996) provide conflicting evidence. They reported agrowth rate of k = 0.14 year–1 and asymptotic size of L∞ =114 cm for winter skate off Nova Scotia (Simon and Frank1996; Sulikowski et al. 2003). Simon and Frank’s (1996)growth estimates are considerably higher than those fromthe present study and those reported by Sulikowski et al.(2003). However, Sulikowski et al. (2003) cites personalcommunication with Simon that the oldest individuals mayhave been underaged by 4 or more years in the Simon andFrank (1996) study. This may explain the apparent anomaly.The potential for latitudinal trends in winter skate deservesmore study.

Why might there be different responses to latitude in thetwo species? Although the trends are not clear, a review ofmaps of juvenile and adult winter skate regional distribu-tions and abundances reveals that adults and juveniles arefairly mobile (Parker et al. 2003). Adult and juvenile winterskate occur, or gather, in great numbers on Georges Bank,

© 2006 NRC Canada


Fig. 10. von Bertalanffy growth model fit to length (cm total length, TL) and age (years) data for winter skate (Leucoraja ocellata). Thefigure shows data for male (open circles, broken line) and female (closed circles, solid line) winter skate for the US northeastern coast.

Fig. 11. Comparison of growth models for winter skate (Leucoraja ocellata) fit to “liberal read” (solid line), “conservative read” (cir-cles, broken line), and high readability (triangles, smaller broken line) data.

whereas juveniles appear to occur in the mid-Atlantic re-gion at disproportionately higher abundances than adults(Parker et al. 2003). Further, all genetically identified, newlyhatched winter skate were caught on Georges Bank. A possi-ble explanation for these patterns is that Georges Bank is theprincipal spawning ground for winter skate. In contrast, re-cently hatched specimens of little skate were caught in allregions in the northeast coast. Thus winter skate may repre-sent a single biological population with restricted spawning,whereas little skate spawn more widely and thus express lat-itudinal differences more fully. However, sample size wasnot large and the abundance maps are not conclusive; thusthese results are speculative in nature.

Our findings, like those of Natanson (1993), indicate thatthe observed maximum age for little skate is older than theprevious estimates of Tmax = 5 (Johnson 1979) and Tmax =8 years (Richards et al. 1963; Waring 1984). The oldestfemale and male little skate were 12.5 and 12 years,respectively. Additionally, previous growth curves did notexhibit asymptotic behaviour, suggesting that larger, olderindividuals were not adequately sampled or that age esti-mates were biased low (Richards et al. 1963; Waring 1984).Assuming that longevity can be estimated as the fraction(95%) of L∞ attained in a life span (Taylor 1958), the theo-retical life span (Tmax) for little skate would equal 13 yearsin the mid-Atlantic, 14 years in southern New England –Georges Bank, and 15 years in the Gulf of Maine.

Previous work conducted on winter skate in the Gulf ofMaine indicates that the species may grow slightly slowerand reach a larger size than our data suggest (Sulikowski etal. 2003). The slightly lower growth rate of Sulikowski et al.(2003) may explain the higher L∞ as a result of the strongcorrelation among von Bertalanffy parameters. However, thelargest individual that Sulikowski et al. (2003) aged wasTL = 94 cm. The present analysis included 13 winter skatethat were 94 cm TL or larger and all samples above 90 cmTL were male. The largest individual caught on the NMFS’sannual surveys (1963 to present) was TL = 111 cm. This isin agreement with the size of L∞ for southern New England –Georges Bank, high readability, and conservative growthmodels.

The oldest female and male winter skate were 19.5 and20.5 years, respectively. Previous workers found maximumages of 16 and 19 years for females and males, respectively(Simon and Frank 1996; Sulikowski et al. 2003). Althoughthe vertebral centra from juvenile winter skate (0–10 years)were relatively easy to read, adult winter skate were harderto age. Difficulty ageing older fish may have produced thegrowth curves that do not fully reach an asymptote. How-ever, it is relatively common in Rajidae species to see growthcurves that do not flatten out (Sulikowski et al. 2003). Untilthe age of larger individuals can be verified, estimates oflongevity based on aged individuals should be interpretedwith caution and may be underestimates. Assuming that lon-gevity can be estimated as the fraction (95%) of L∞ attainedin a life span and the uncertainty discussed above, the theo-retical life span (Tmax) for winter skate is 35 years (Taylor1958).

In some adult winter skate, the first 8–10 annuli wereclear, with false rings or check marks becoming more com-

mon in subsequent annuli. One potential confounding factoris the possibility that check marks are formed as a result ofspawning, which has been proposed in the viviparous Austra-lian sharpnose shark, Rhizoprionodon taylori (Simpfendorfer1993). Defining spawning time in a serial spawner wouldlikely be a difficult process with egg case production occur-ring many times each year. A second ageing problem thatoccurred in some individuals was that the distance betweensuccessive annuli increased towards the edges of the centra,indicating that we may be undercounting annuli. Ultimatelythe liberal read approach, in which we counted every markthat could be a potential annulus, was used as the standard.In this method, readers still avoided counting obvious checkmarks that were not annuli. However, in some cases, thetask of distinguishing between check marks and annuli re-mained difficult.

Ultimately, the conservative read approach provided simi-lar growth rates but a lower maximum age (Tmax = 15 years)for winter skate, and the high readability fit was very similarto the liberal read fit. However, the life history of winterskate suggests that the conservative read approach is likelyinaccurate. Age at maturity estimates for this species rangefrom 10 to 14 years (Frisk 2004). If these estimates are cor-rect, then the conservative read would provide a reproductiveperiod too short for a species with low to moderate fecundity(Frisk 2004). von Bertalanffy growth curves fit with speci-mens with high confidence in annuli interpretation providedmaximum age and growth rates nearly identical to those ofthe liberal read. However, the high readability fit lackedmany of the largest specimens and may have excluded manyof the oldest specimens. Here again, underestimation ofadult ages may be occurring. Validation of the age of oldspecimens of winter skate is needed to better understand themaximum age and growth in older fish. Until then, a precau-tionary management philosophy and the lessons fromNatanson’s (1993) work on little skate argues for a liberalinterpretation of annuli.

Precision between readers was relatively high at 20% and18% for little skate and winter skate, respectively. Within-reader precision was lower at 11.6% and 8.0% for little skateand winter skate, respectively. Precision estimates in elasmo-branchs tend to be lower than those in teleost fish and areoften not reported (Campana 2001; Cailliet and Goldman2004). Some little skate specimens that were 19–20 cm TLwere estimated to be age 0. It was unclear if this was an age-ing error or a result of date of birth. Little skate is a continu-ous spawner and hatching can occur at any time of the year,whereas the formation of annuli is a seasonal process (John-son 1979; Natanson 1993).

It has long been known that elasmobranchs, especiallylarge, late-maturing, long-lived, slow-growing species, arevery susceptible to overexploitation and even local extinc-tion (Walker and Hislop 1998; Dulvy et al. 2000; Stevens etal. 2000). Further, species in the family Rajidae have beenranked as one of the marine fishes most susceptible to over-exploitation (Dulvy et al. 2000). Previous analyses have in-dicated that moderate to low exploitation rates could lead tothe decline of little skate (Leucoraja erinacea) and winterskate (Leucoraja ocellata) populations in the western Atlan-tic (Frisk et al. 2002). Although skates are likely candidates

© 2006 NRC Canada


for overexploitation, a lack of knowledge of vital rates of lit-tle skate and winter skate have hindered effective manage-ment policies (NEFSC 2000). Here critical life history ratesof age and growth have been estimated over large propor-tions of both species’ ranges that reinforce concerns over thepotential for overexploitation in these species.

Acknowledgments

There are too many people to thank than space would al-low. However, we thank all the people who worked or volun-teered aboard the NOAA R/V Albatross IV, Woods Hole,Massachusetts, for helping collect samples and providingmany good times. We especially thank Kris Ohleth andKathy Sosebee for advice and assistance in collecting sam-ples. We thank Lisa Natanson and James Gelsleichter fortechnical assistance with ageing skates. We also thank tworeviewers who provided comprehensive and professionalcomments on drafts of this manuscript. The project wasfunded by the National Marine Fisheries Service / Sea GrantFellowship in Population Dynamics. This is contributionNo. 3916 from the University of Maryland Center for Envi-ronmental Science Chesapeake Biological Laboratory.

References

Alvarado Bremer, J.R.A., Frisk, M.G., Miller, T.J., Turner, J., Vinas,J., and Kwil, K. 2005. Genetic identification of cryptic juvenilesof little skate and winter skate. J. Fish Biol. 66: 1177–1182.

Beverton, R.J.H. 1992. Patterns of reproductive strategy parametersin some marine teleost fishes. J. Fish Biol. 41: 137–160.

Beverton, R.J.H., and Holt, S.J. 1959. A review of the life-spansand mortality rates of fish in nature, and their relationship togrowth and other physiological characteristics. CIBA Found.Colloq. Age, 54: 142–180.

Cailliet, G.M., and Goldman, K.J. 2004. Age determination andvalidation in Chondrichthyan fishes. In Biology of sharks andtheir relatives. Vol. 14. Edited by J.C. Carrier, J.A. Musick, andM.R. Heithaus. CRC Press, Boca Raton, Fla. pp. 339–447.

Campana, S.E. 2001. Accuracy, precision and quality control inage determination, including a review of the use and abuse ofage validation methods. J. Fish Biol. 59: 197–242.

Chen, Y., Jackson, D.A., and Harvey, H.H. 1992. A comparisonof von Bertalanffy and polynomial functions in modeling fishgrowth data. Can. J. Fish. Aquat. Sci. 49: 1228–1235.

Conover, D.O., and Present, T.M.C. 1990. Countergradient varia-tion in growth-rate — compensation for length of the growing-season among Atlantic silversides from different latitudes.Oecologia, 83: 316–324.

Dulvy, N.K., Metcalfe, J.D., Glanville, J., Pawson, M.G., andReynolds, J.D. 2000. Fishery stability, local extinctions, and shiftsin community structure in skates. Conserv. Biol. 14: 283–293.

Fogarty, M.J., and Murawski, S.A. 1998. Large-scale disturbanceand the structure of marine system: fishery impacts on GeorgesBank. Ecol. Appl. 8: S6–S22.

Frisk, M.G. 2004. Biology, life history and conservation of elasmo-branchs with an emphasis on western Atlantic skates. Ph.D. dis-sertation, University of Maryland, College Park, Md.

Frisk, M.G., Miller, T.J., and Fogarty, M.J. 2001. Estimation andanalysis of biological parameters in elasmobranch fishes: a com-parative life history study. Can. J. Fish. Aquat. Sci. 58: 969– 981.

Frisk, M.G., Miller, T.J., and Fogarty, M.J. 2002. The populationdynamics of little skate Leucoraja erinacea, winter skateLeucoraja ocellata, and barndoor skate Dipturus laevis: predict-ing exploitation limits using matrix analyses. ICES J. Mar. Sci.59: 576–586.

Johnson, G.F. 1979. The biology of the little skate, Raja erinaceaMitchill 1825, in Block Island Sound, Rhode Island. MS thesis,University of Rhode Island, Kingston, R.I.

Kimura, D.K. 1980. Likelihood methods for the von Bertalanffygrowth curve. Fish. Bull. NOAA, 77: 765–776.

Link, J.S., Garrison, L.P., and Almeida, F.P. 2002. Ecological inter-actions between elasmobranchs and groundfish species on thenortheastern US continental shelf. I. Evaluating predation. N.Am. J. Fish. Manag. 22: 550–562.

McEachran, J.D. 2002. Skates. Family Rajidae. In Fishes of the Gulfof Maine. 3rd ed. Edited by B.B. Collete and G. Klein-MacPhee.Smithsonian Institution Press, Washington, D.C.

McEachran, J.D., and Martin, C.O. 1977. Possible occurrence ofcharacter displacement in the sympatric skates Raja erinacea andR. ocellata (Pisces: Rajidae). Environ. Biol. Fishes, 2: 121–130.

McEachran, J.D., and Musick, J.A. 1973. Characters for distin-guishing between immature specimens of sibling species, Rajaerinacea and Raja ocellata (Pisces-Rajidae). Copeia, 1973:238–250.

Murdy, E.O., Birdsong, R.S., and Musick, J.A. 1997. Fishes ofChesapeake Bay. Smithsonian Institution Press, Washington, D.C.

Natanson, L.J. 1993. Effect of temperature on band deposition inthe little skate, Raja erinacea. Copeia, 1993: 199–206.

National Marine Fisheries Service. 2002. Annual report to con-gress on the status of U.S. fisheries — 2001. US Department ofCommerce, NOAA National Marine Fisheries Service, SilverSpring, Md.

Nelson, G.A. 1993. The potential impacts of skate abundance uponthe invertebrate resources and growth of yellowtail flounder(Pleuronectes ferruginea) on Georges Bank. Ph.D. dissertation,University of Massachusetts, Amherst, Mass.

Northeast Fisheries Science Center. 2000. [Report of the] 30thNortheast Regional Stock Assessment Workshop (30th SAW)Stock Assessment Review Committee (SARC) consensus sum-mary of assessments. Northeast Fisheries Science Center Ref.Doc. No. 00-03.

Parker, D.B., Zetlin, C.A., and Vitaliano, J.J. 2003. Essential fishhabitat source document: winter skate, Leucoraja ocellata, lifehistory and habitat characteristics. NOAA Tech. Memo. NMFSNE, 79: 72.

Parsons, G.R. 1993. Geographic variation in reproduction between2 populations of the bonnethead shark, Sphyrna tinburo. Envi-ron. Biol. Fishes, 117: 23–31.

Richards, S.W., Merriman, D., and Calhoun, L.H. 1963. Studies onthe marine resources of southern New England IX. The biologyof the little skate, Raja erinacea, Mitchill. Bull. BinghamOceanogr. Collect. Yale Univ. 18: 5–67.

SAS Institute Inc. 2001. SAS version 8.2 [computer program].SAS Institute Inc., Cary, North Carolina.

Shine, R., and Charnov, E.L. 1992. Patterns of survival, growth,and maturation in snakes and lizards. Am. Nat. 139: 1257–1269.

Simon, J.E., and Frank, K.T. 1996. Assessment of the division4VsW skate fishery. DFO Atlantic Fisheries Research DocumentNo. 96/105. p. 51.

Simpfendorfer, C.A. 1993. Age and growth of the Australiansharpnose shark, Rhizoprionodon taylori, from North Queens-land, Australia. Environ. Biol. Fishes, 36: 233–241.

© 2006 NRC Canada


Stevens, J.D. 1999. Variable resilience to fishing pressure in twosharks: the significance of different ecology and life history pa-rameters. In Life in the slow lane. Edited by J.A. Musick. Am.Fish. Soc. Symp. 23: 11–14.

Stevens, J.D., Bonfil, R., Dulvy, N.K., and Walker, P.A. 2000. Theeffects of fishing on sharks, rays, and chimaeras (chon-drichthyans), and the implications for marine ecosystems. ICESJ. Mar. Sci. 57: 476–494.

Sulikowski, J.A., Morin, M.D., Suk, S.H., and Howell, W.H. 2003.Age and growth estimates of the winter skate (Leucorajaocellata) in the western Gulf of Maine. Fish. Bull. 101: 405–413.

Taylor, C.C. 1958. Cod growth and temperature. J. Cons. Int.Explor. Mer, 23: 366–369.

von Bertalanffy, L. 1957. Quantitative laws in metabolism andgrowth. Q. Rev. Biol. 32: 217–231.

Walker, P.A., and Hislop, J.R.G. 1998. Sensitive skates or resilientrays? Spatial and temporal shifts in ray species composition inthe central and north-western North Sea between 1930 and thepresent day. ICES J. Mar. Sci. 55: 392–402.

Waring, G.T. 1984. Age, growth, and mortality of the little skateoff the northeast coast of the United States. Trans. Am. Fish.Soc. 113: 314–321.

Yamaguchi, A., Taniuchi, T., and Shimizu, M. 1998. Geographicvariation in growth of the starspotted dogfish Mustelus manazofrom five localities in Japan and Taiwan. Fish. Sci. 64: 732–739.

© 2006 NRC Canada


age, growth, and latitudinal patterns of two rajidae ...frisk/frisk and miller, 2006.pdf ·...

Documents