RESEARCH ARTICLE

Reproductive status and body condition of Atlanticbluefin tuna in the Gulf of Maine, 2000–2002

Jennifer Goldstein Æ Scott Heppell Æ Andrew Cooper ÆSolange Brault Æ Molly Lutcavage

Received: 29 September 2006 / Accepted: 1 February 2007

� Springer-Verlag 2007

Abstract The reproductive status and body condition of

195 (‡185 cm curved fork length, CFL; assigned age 7

and above) Atlantic bluefin tuna were assessed in the Gulf

of Maine during the commercial fishing season of June–

October, 2000–2002. Given the distance between known

spawning and feeding grounds, the prevailing paradigm

for Atlantic bluefin tuna (Thunnus thynnus thynnus, L.)

suggests that the most likely histological state for females

arriving in the Gulf of Maine after spawning would be a

resting or quiescent state with little or no perigonadal fat.

Alternatively, the presence of mature or mature-inactive

histological states in some females supports a more varied

or individualistic model for bluefin reproduction. No

relationship was found between body condition and

reproductive status. Males were found in all reproductive

stages, but were more likely to be in spawning condition

(stages 4 and 5) or a mature-inactive state (stage 6) in

June and July. Female bluefin tuna were found in stage 1

(immature or non-spawning) and stage 6 (mature-inac-

tive). Stage 6 females were only present in June and July

and smaller females (<235 cm CFL) were more likely to

be in stage 6 than large females (>235 cm CFL) sampled

during those same months. The presence of smaller fe-

males in stage 6 arriving at the same time as larger fe-

males in stage 1 indicates that Western Atlantic bluefin

tuna may have an asynchronous reproductive schedule

and may mature at a smaller size than the currently ac-

cepted paradigm suggests.

Introduction

The reproductive biology of the western component of the

Atlantic bluefin tuna (Thunnus thynnus) stock remains

incomplete and impaired by large uncertainties, despite

the depleted status and economic importance of this

fishery. When, where, how often and at what size/age

long-lived, highly migratory fish species reproduce are

key life history characteristics needed by fisheries man-

agers to determine the regenerative ability of the stock

(Mather et al. 1995; Quinn and Deriso 1999; Jorgensen

et al. 2006; Fromentin and Powers 2005). Bluefin tuna

feed in energy-rich coastal areas at higher latitudes to

increase somatic fat reserves that fuel reproduction and

migration (Crane 1936; Bigelow and Schroeder 1953;

Dragovich 1970; Chase 2002). Poor body condition

brought about by low quality prey or reduced prey

availability can affect reproductive success through re-

duced fecundity (Hislop et al. 1978) and changes in

reproductive schedule (Burton and Idler 1984, 1987;

Hunter and Macewicz 1985; Larsson et al 1990; Rijnsdorp

Communicated by J.P. Grassle.

J. Goldstein (&) � S. Brault

Biology Department, University of Massachusetts,

Boston, MA 02125, USA

e-mail: jennifer.goldstein@comcast.net

S. Heppell

Department of Fisheries and Wildlife,

Oregon State University, Corvallis, OR 97331, USA

A. Cooper

Department of Natural Resources,

Institute for the Study of Earth, Oceans and Space,

University of New Hampshire, Durham, NH 03824, USA

M. Lutcavage

Large Pelagics Research Center,

University of New Hampshire,

Durham, NH 03824, USA

123

Mar Biol

DOI 10.1007/s00227-007-0638-8

1990; Rajisilta 1992; Rideout et al. 2000; Jorgensen et al.

2006). Seafood brokers’ records of fat and oil grades

indicate that bluefin tuna arriving in the Gulf of Maine are

usually in poor condition (Estrada et al. 2005), and that

overall body condition and quality has declined over the

past 14 years (Golet et al. 2006). Shifts in fat and energy

stores in relation to reproduction have been documented

for the eastern Atlantic bluefin tuna stock (Frade 1937;

Rodriguez-Roda 1963; Medina et al. 2002; Abascal et al.

2004), though there have been no previous studies of

reproduction or energy stores for bluefin tuna that forage

in the Gulf of Maine in summer and fall.

Mature bluefin tuna have been presumed to follow an

annual cycle of foraging from June through March off the

eastern US and Canadian coasts, followed by migration to

the Gulf of Mexico to spawn in April and May, although

Rivas (1978) suggested that some western fish might spawn

in the Mediterranean. The prevailing assumption is that the

Gulf of Maine assemblage is comprised of individuals from

the western Atlantic stock that matures at age 8–10 (�200

to 225 cm CFL, Turner et al. 1991) and shows spawning

site fidelity to the Gulf of Mexico or Florida Straits (Rivas

1954; NRC 1994; Mather et al. 1995; Nemerson et al.

2000; Block et al. 2005). An eastern Atlantic stock, which

primarily spawns in the Mediterranean, achieves sexual

maturity at age 3–5, or 103–110 cm FL (�108–115 CFL)

(Tiews 1963; Rodriguez-Roda 1964; Susca et al. 2000,

2001b; Medina et al. 2002; Corriero et al. 2005).

Recent electronic tagging data from bluefin tuna ini-

tiated in the western Atlantic have been used to support

this interpretation (Stokesbury et al. 2004; Block et al.

2001, 2005), or to call it into question (Lutcavage et al.

1999; Wilson et al. 2005; Fromentin and Powers 2005).

Tag reporting rates from the Gulf of Mexico for mature

sized bluefin tuna from all studies (N = 381) were only

3–11%, including individuals that were present well be-

fore the spawning season of April–June (Lutcavage et al.

1999; Stokesbury et al. 2004; Block et al. 2005; Wilson

et al. 2005; Sibert et al. 2006; F. Royer et al., unpub-

lished data). Most (N � 317) were found in a vast area

spanning from the Gulf Stream margins to the Azores,

where there is substantial mixing of the two purported

stocks (Lutcavage et al. 1999; Block et al. 2001, 2005;

Sibert et al. 2006). These results present the possibility

that (1) individual bluefin tuna do not spawn on an an-

nual cycle as previously assumed (Lutcavage et al. 1999;

Lioka et al. 2000; Corriero et al. 2003; Block et al. 2005;

Fromentin and Powers 2005), (2) a component of the

western stock is spawning somewhere other than the Gulf

of Mexico, e.g., in the central north Atlantic or Gulf

Stream edge (Mather et al. 1995; Lutcavage et al. 1999)

or (3) some of the electronically tagged fish have eastern

Atlantic origins but migrate west as juveniles and share

feeding grounds in US coastal waters (Rooker and Secor

2004; Block et al. 2005). Any of these scenarios impact

the quality of population assessments used to pro-

mote conservation and stock recovery for this depleted

species.

Ideally, reproductive parameters should be measured in

fish collected directly on the spawning grounds (NRC

1994; Farley and Davis 1998; Schaefer 1998, 2001;

Medina et al. 2002) because direct evidence of spawning

activity (migratory nucleus oocytes, post-ovulatory folli-

cles (POFs), and fully hydrated oocytes) are detectable for

£24 h after spawning in tunas (Hunter et al. 1986;

Schaefer 1996, 1998, 2001; Medina et al 2002; Corriero

et al. 2005). However, sampling in the Gulf of Mexico is

difficult due to a moratorium on bluefin tuna fishing there.

Also, if a portion of the stock is spawning elsewhere or if

the population structure more closely resembles a meta-

population (Fromentin and Powers 2005), the sizes of fish

in the Gulf of Mexico in April and May may not accu-

rately represent the spawning size range of the population

as a whole.

Despite their distance from known spawning grounds,

Gulf of Maine bluefin tuna offer alternative information on

size at maturity and timing of spawning. Though direct

evidence of spawning is unlikely to be detected, atretic

(degrading) vitellogenic oocytes, which indicate that

maturity has occurred during the last maturity cycle

(Heppell and Sullivan 1999; Corriero et al. 2003), are

detectable for a longer time period. Atretic follicles in

northern anchovy (Eugraulis mordax) were detectable for

as long as fourteen days after cessation of spawning

(Hunter and Macewicz 1985), but are likely to be resorbed

more quickly in tuna due to their higher metabolism and

relatively warm internal body temperature (Hunter et al.

1986). The presence of vitellogenic and atretic vitellogenic

oocytes in histological samples from Gulf of Maine bluefin

tuna would indicate that maturity had occurred recently,

even if spawning per se cannot be determined (Heppell and

Sullivan 2000).

Given the distance between known spawning and feed-

ing grounds, the prevailing paradigm suggests that the most

likely histological state for females arriving in the Gulf of

Maine after spawning would be a resting or quiescent state

with little or no perigonadal fat. Alternatively, the presence

of mature or mature-inactive histological states in some

females supports a more varied or individualistic model for

bluefin reproduction. The purpose of this study is to (1)

characterize the reproductive status of Gulf of Maine

bluefin tuna using histological techniques and (2) use

general linear models (GLMs) to determine whether the

reproductive characteristics of histological stage and gonad

weight could be separated on the basis of size/age and body

condition.

Mar Biol

123

Materials and methods

Sample collection

We asked 12 commercial fishermen participating in the

seasonal Gulf of Maine fishery for large and large-medium

bluefin (‡185 cm CFL) to collect stomachs, gonads, and

perigonadal fat. The minimum legal size for bluefin tuna

landed in the commercial sector of the fishery is 185 cm

CFL, so smaller sizes could not be sampled for this study.

Perigonadal fat is an adipose fat reserve attached directly to

the gonad, used primarily for the production of gametes but

also for general metabolism (Mourente et al. 2002; Abascal

et al. 2004; Corriero et al. 2003). It can be used as an

indicator of condition and foraging success because it ac-

crues rapidly over the summer and fall if feeding condi-

tions are appropriate. A 1-cm3 sample of muscle tissue was

frozen for hormonal analyses of 11-ketotestosterone and

17ß-oestradiol levels to determine whether a relationship

between hormone levels and maturational status was

detectable, similar to the study by Susca et al. (2000).

Sampling coincided with the commercial fishing season

June 1st through mid October 2000–2002. Fishermen were

asked to record capture location and gear. Either CFL or

dressed length (DL), which is the curved length of the fish

minus the head, was recorded. Dressed weights (DW) were

recorded rather than round weights, as most fishermen re-

move heads from fish at sea prior to obtaining a weight

dockside. DWs and DLs were converted to round weights

and CFLs when necessary by using the conversion factors

of DW · 1.25 = round weight (Anon. 2003) and

CFL = DL · 1.35 (S. Turner, unpublished data). Samples

were obtained from 195 fish (80 females and 115 males),

ranging in size from 185 to 291 cm CFL, and round

weights of 75–314 kg. The study area includes the Gulf of

Maine and some sampling also occurred east of Cape Cod

and south to the Great South Channel, all known foraging

areas for bluefin tuna (Crane 1936; Bigelow and Schroeder

1953; Caddy and Butler 1975; Chase 2002) (Fig. 1).

Histological analysis

Perigonadal fat was trimmed from the gonads and each

weighed separately to the nearest 0.1 g. A gonadosomatic

index was calculated by the following formula:

GSI ¼ gonad weight (kg)

RW (kg)� 100. ð1Þ

A 1.0 cm3 sub-sample from the midsection of the gonad

was preserved for histological analysis in 10% buffered

formalin. Gonads were staged according to Heppell and

Sullivan (1999) and stages were defined as follows:

Females

Stage 0: Largest germ cells are primary oocytes with a

conspicuous nucleus containing chromatin threads and a

single large nucleolus, stage 1: primary (perinucleolar)

stage oocytes; minor atresia may be present, stage 2:

vitellogenin independent growth, stage 3: early vitello-

genesis, stage 4: late vitellogenesis, stage 5: final oocyte

maturation and spawning, stage 6: degredation and pres-

ence of atretic follicles. If yolked, atretic oocytes are not

present, it may be impossible to determine whether the fish

is truly immature, or is mature but has had sufficient time

Fig. 1 Sampling locations for

bluefin tuna, Thunnus thynnus,

in the Gulf of Maine and

adjacent waters. Inset shows

study site in relation to the

western North Atlantic. Filledcircle 2000, filled triangle 2001,

plus symbol 2002

Mar Biol

123

since spawning to resorb evidence of maturation (Schaefer

1998; Corriero et al. 2003). These individuals are classified

as stage 1 fish, and termed ‘‘immature or non-maturing’’.

Males

Stage 1: no signs of spermatogenesis, stage 2: spermato-

cytes present, stage 3: spermatocytes and spermatids

present, stage 4: mature sperm in small quantities, stage 5:

fully mature testis, stage 6: collapsing crypts and tubules.

Stage 0 was not defined for males. Stages 1–3 are con-

sidered to be immature or non-maturing, stages 4–5 are

considered to be mature-active, and stage 6 is considered to

be mature-inactive for both males and females.

Calculation of Wr

To quantify changes in body condition over the season, we

calculated a condition factor, Wr, after Anderson and

Neumann (1996).

Wr ¼Wo

Ws

: ð2Þ

Wr is an index of the relative weight of a fish, where Wo is

the observed weight (in kg) of an individual and Ws (in kg)

is a length-specific standard weight predicted by a weight–

length regression constructed to represent the population.

The weight–length regression was calculated from the

National Marine Fisheries Service (NMFS) landings data

(Bluefin Tuna Landings Database, NMFS Northeast Re-

gional Office, Gloucester, MA, 01930, USA) collected

during 2000–2002. Only landings data from the New

England region were used to ensure that Ws was calculated

from the same assemblage of fish.

Data entry errors in the NMFS database when DLs were

entered as CFLs and vise-versa, were detected from an

examination of the residuals from the regression of DW on

DL. We corrected for this by conservatively removing data

points with deviations greater than ±150 (Fig. 2a). While

not completely removing all outliers, it did improve the

goodness of fit. This resulted in a loss of 96 points (about

2%), leaving an N = 4,700 from which the length-specific

standard weight was obtained through simple linear

regression using log-transformed values for weight

(Fig. 2b). Since round weights were not obtained for most

fish and conversion factors can introduce unnecessary

uncertainty, we chose to develop the Wr index based on

DLs and DWs. The values of sampled fish were compared

to the expected value from the regression of a fish of the

same weight according to Eq. 2. Values for Wr are clus-

tered around 1.0. Fish having a Wr value = 1.0 are of

average weight for their length, fish with a Wr < 1.0 are

relatively thin for their length, and fish with Wr > 1.0 are

relatively rotund for their length.

Statistical analyses

All analyses were performed using Splus 7.06 for Windows

(Insightful Corp., Seattle, WA, USA). A description of

model variables is provided in Table 1. Males and females

were analyzed separately. For analyzing the reproductive

stage of tuna we used logistic regression. For the purposes

of analysis, reproductive stages were broken into two

groups consisting of stages 0–3, indicating fish that are

either immature (juveniles) or non-maturing adults, and

stages 4–6, indicating fish that are in spawning condition or

fish that have matured during the last maturity cycle, but

are currently inactive. We examined the effect of DW,

CFL, month (as an unordered categorical variable and as a

continuous variable), Wr, Wg (in kg), and Wpf. (in g). We

Expected Values

0 100 200 300 400 500 600 700

Reg

ress

ion

Res

idua

ls

-400

-300

-200

-100

0

100

200

DL (cm)

120 140 160 180 200 220 240 260

ln D

W

3.5

4.0

4.5

5.0

5.5

6.0

6.5

y = 0.0162x + 2.3245R2 = 0.7429

(a)

(b)

Fig. 2 Data corrections for the calculation of condition factor, Wr. aPlot of residuals vs. expected values from the regression of bluefin

tuna (Thunnus thynnus) dressed weights (DW) on dressed lengths

(DL) from the NMFS landings database. Dotted lines indicate cutoff

points to exclude outliers. b Regression of lnDW on DL to corrected

NMFS database values

Mar Biol

123

analyzed gonad weight using generalized linear models

(GLMs) (e.g., McCullagh and Nelder 1989), and examined

the effect of DW, CFL, month (as an unordered categorical

variable and as a continuous variable), Wr, and Wpf (in g).

Main effects for the regression and GLMs were tested

using an alpha-level of 0.05, and interaction effects were

tested using an alpha-level of 0.10.

Results

A summary of variables by month (Table 2) revealed that

sex ratios were skewed, with 59% of fish sampled being

male, and 41% female. Mean male CFL and DW were

larger than their corresponding female values in all months

except June, where females tended to be larger. The effect

of month on Wr was significant (P = 0.0001), with June

and July not different from each other, but less than August

and September based on 90% confidence intervals using

the Tukey method. Females had lower Wr overall

(P = 0.027), but the effect of month did not differ by sex

(P = 0.50). Wg was extremely variable, but females tended

to have a higher mean Wg in all months. Wpf did not differ

by sex (P = 0.47), nor did the effect of month differ by sex

(P = 0.26). Mean GSI values were highest in the months of

July and August (0.84 and 0.86) for females, and highest

for males in September (0.52). Females in the mature/

mature-inactive group had GSI values that were higher

than females in the immature /non-maturing group (0.63

vs. 0.47), but the two male functional groups had almost

identical GSI values (0.40 vs. 0.43).

Reproductive stage: males

Males were found in all reproductive stages except stage 0.

Males were more likely to be in a mature or a mature-

inactive state in June and July, with active stages

decreasing as the summer progressed (Fig. 3a). The most

parsimonious model for predicting the reproductive stage

of male bluefin tuna only contained the variable Month, as

an unordered categorical variable, (F4,111 = 7.37,

P < 0.0001). After accounting for month, DW, CFL, Wr,

Wg, and Wpf were each non-significant (P = 0.64, P = 0.52,

P = 0.41, P = 0.28, and P = 0.86, respectively). Month,

however, was always significant with these other variables

in the model. All interactions were similarly not significant.

Diagnostic plots supported the assumption of homogeneous

variance and normally distributed residuals.

Gonad weight: males

Wg was log transformed to correct for heterogeneous sto-

chasticity. The most parsimonious model for predicting Wg

of male bluefin tuna contained only Wpf and DW. Wpf was

negatively correlated with Wg (F1,91 = 24.85, P < 0.0001),

but DW was positively correlated with Wg (F1,91 = 28.8,

P < 0.0001). With Wpf and DW in the model, neither

month, CFL, nor Wr were significant (P = 0.51, P = 0.22,

P = 0.71, respectively). No interactions were significant.

Reproductive stage: females

All females, with the exception of one fish in stage 2, were

found in either stage 1 or stage 6 (Fig. 3b). No length or

weight data was available for the female in stage 2, so it

was excluded from the model. All females landed in Au-

gust, September and October were in stage 1. Month, as an

unordered categorical variable, was a significant factor in

predicting the reproductive stage of female bluefin tuna

(F3,55 = 18.51, P < 0.0001). Females were most likely to

be in a mature-inactive state (stage 6) in June or July. Only

one female was observed in October; it was not in stage 6,

and was not included in this analysis due to the small

sample size. Even after accounting for month and Wg, DW

was also significant (F1,55 = 36.33, P < 0.0001), with lar-

ger females less likely to be in stage 6. When accounting

for month and DW, females with higher Wg were more

likely to be in stage 6 (F1,55 = 40.10, P < 0.0001). With

month, Wg, and DW in the model, Wr was not significant

(P = 0.92); nor was Wpf (P = 0.90). Interactions between

month and Wg, month and DW, and Wg and DW were all

nonsignificant (P = 0.33, P = 0.90, and P = 0.32, respec-

tively). Diagnostic plots supported the assumption of

homogeneous variance and normally distributed residuals.

Table 1 Conditional and

morphometric descriptor

variables for Atlantic bluefin

tuna, Thunnus thynnus, used in

logistic regression and GLM

analyses

Variable Abbreviation Units Description

Dressed wt. DW kg Fish weight—gilled, gutted, head removed

Curved fork length CFL cm Length measured along the contour of the body,

from tip of upper lip to fork of tail, touching

top of pectoral fin

Condition factor Wr None Relative weight of a fish (see text, Eq. 1)

Perigonadal fat wt. Wpf g Weight of perigonadal fat reserve

Gonad wt. Wg g Weight of gonads

Mar Biol

123

Gonad weight: females

Month, DW, and Wpf were all significant predictors of Wg

for female bluefin tuna. Tuna with lower Wpf had higher Wg

(F1,50 = 11.79, P = 0.001). DW varied by month

(F3,50 = 5.33, P = 0.003) such that DW is positively cor-

related with Wg in July and August (P = 0.0006, and

P < 0.0001, respectively), but not correlated with Wg in

June or September (P = 0.95 and P = 0.40). Based on post-

hoc multiple comparisons using the Sidak method (Sidak

1967) with simultaneous 90% confidence intervals after

accounting for DW and Wpf, Wg in June were different

from those in July, August, and September, but Wg in July,

August, and September did not differ from one another.

After accounting for Wpf, DW, and month, neither CFL nor

Wr were significant (P = 0.15 and P = 0.92). No other

interactions were significant. Diagnostic plots supported

the assumption of homogeneous variance and normally

distributed residuals.

Discussion

This is the first study to apply current histological tech-

niques to define the reproductive status of bluefin tuna in a

key western Atlantic foraging ground. Sampling during this

study was limited by several factors, most notably, the

inability to sample fish smaller than the legal commercial

size limit of 185 cm CFL (estimated age 7–8 years, Turner

et al. 1991). Due to the rapid rate of resorption of post-

ovulatory follicles (£24 h), direct evidence of spawning

activity was not detected in females (Fig. 4), but the

presence of atretic vitellogenic oocytes indicated recent

sexual maturity (stage 6: mature-inactive females). Hor-

monal analyses of 11-ketotestosterone and 17ß-oestradiol

levels in muscle from sampled fish showed no clear rela-

tionship between maturational status and steroid concen-

tration (J. Goldstein et al., unpublished data).

Wr increased significantly over the season as fish fat-

tened, but it was not helpful for defining differences in

reproductive states for males or females. This index, which

has a very small range (0.74–1.53), may not be sensitive

enough to detect differences between reproductively dis-

tinct individuals, especially at a time of year when indi-

viduals are expected to have traveled from several hundred

miles away, leaving metabolic lipid reserves in a reduced

state. Wpf and Wg were inversely proportional to each other

in both sexes, suggesting that perigonadal reserves were

being used to produce gametes (Mourente et al. 2002).

The ratio of females to males sampled in this study was

1:1.4, and males were larger, on average, than females in

both length and weight (Table 2), a result also found by

Table 2 Mean and SD for CFL, DW, condition factor (Wr), gonad weight (Wg), perigonadal fat weight (Wpf) and gonadosomatic index (GSI) by

month for Atlantic bluefin tuna (Thunnus thynnus) landed in all 3 years of the study (2000–2002)

Month Sex CFL (cm) DW (kg) Wr Wg (g) Wpg (g) GSI

June Females

N = 15

229.0 (18.8) 143.0 (29.1) 0.98 (0.08)a 1010.2 (257.9) 618.1 (287.9) 0.58 (0.25)

Males

N = 22

218.0 (21.3) 122.7 (37.6) 0.96 (0.08)a 534.6 (604.2) 584.4 (363.5) 0.40 (0.46)

July Females

N = 29

218.0 (22.3) 119.0 (45.0) 0.93 (0.12)a 1243.1 (781.3) 769.3 (457.6) 0.84 (0.55)

Males

N = 33

222.0 (24.6) 128.0 (17.6) 0.96 (0.15)a 758.0 (765.5) 812.1(861.0) 0.50 (0.47)

August Females

N = 15

233.8 (23.8) 150.1 (48.9) 1.00 (0.08)b 1762.5 (1143.6) 978.4 (506.4) 0.86 (0.35)

Males

N = 39

246.0 (17.5) 186.0 (41.8) 1.03 (0.09)b 1171.1 (917.4) 1286.8 (1476.8) 0.48 (0.35)

September Females

N = 20

236.0 (18.0) 167.0 (34.6) 1.05 (0.08)b 1176.4 (686.0) 1399.7 (1032.3) 0.63 (0.48)

Males

N = 16

242.0 (21.7) 177.0 (46.2) 1.03 (0.08)b 1125.1 (1095.0) 1290.9 (1203.0) 0.52 (0.49)

October Females

N = 1

239 NA NA 2712.1 92.9 NA

Males

N = 5

243.0 (16.0) 187.0 (47.9) 1.08 (0.06) 293.8 (78.8) 2521.3 (2226.7) 0.12 (0.03)

Groupings for Wr (a, b) based on 90% CI using the Tukey method

Mar Biol

123

Baglin (1980, 1982) and Schaefer for yellowfin tuna

(2001). Skewed sex ratios were also reported in previous

studies, with more males at high latitudes (e.g., 1:3 in

Canada, Caddy and Butler 1976) and the reverse in low

latitudes (e.g., 3:1 Bahamas, Rivas 1976). There is no way

to determine the sex of bluefin tuna from external charac-

teristics, though it appears that males tend to grow larger

than females for many tuna species (Schaefer 1998, 2001).

The harpoon fishery, which targets surface fish and can

select for size, may be inadvertently selecting for males, or

large females may be less susceptible to the gear types used

in this fishery, though this seems unlikely.

Males

Month was the only significant variable for predicting male

reproductive stage, with early season males more likely to

be in mature/mature-inactive condition. Unlike females,

there was no significant size distinction between mature/

mature-inactive males and immature or non-maturing

males. Males appear to be using a different reproductive

strategy than females, with the majority sampled in June

and July arriving in stages 4 and 5 (Fig. 3a), including 5

males under 200 cm CFL, indicating readiness to spawn,

despite the lack of environmental conditions necessary to

support viable larvae. Histological evidence of spawning in

male yellowfin tuna (Thunnus albacares) was only

detectable for about 12 h in samples collected directly on

the spawning grounds (Schaefer 1996). It is not uncommon

for male teleosts to be ready to spawn earlier than females

(Rajisilta 1992; Mylonas et al. 1997; Abascal et al. 2004)

Fig. 4 Bluefin tuna (Thunnusthynnus) sampling locations.

MODIS Terra 4 km nighttime

mean monthly imagery for

March–April 2001 (combined).

White areas cloud cover. Temp

range 0–26�C. Yellow circlesthis study. Black symbolsWilson’s (1965) MV Delaware

cruise: plus symbol cruise 64-3

(N = 10 fish), filled trianglecruise 65-3 (N = 25 fish), filledcircle cruise 66-2 (N = 12 fish).

Green diamond NEAQ

sampling location (N = 17)

(Belle 1995). Black line 156 km

buffer = 24 h directed

movement at 6.5 km h–1 (Rivas

1978; Lutcavage et al. 1997),

assuming POF

resorption £ 24 h. Dotted line312 km buffer (48 h directed

movement)

Month

June July Aug Sept Oct

Month

June July Aug Sept Oct

Fre

quen

cy (

mal

es)

0

10

20

30

40 Stage 1 Stage 2 Stage 3 Stage 4 Stage 5 Stage 6

N = 115 F

requ

ency

(fe

mal

es)

0

10

20

30

40 Stage 1 Stage 2 Stage 3 Stage 4 Stage 5 Stage 6

N = 80

(a)

(b)

Fig. 3 Male (a) and female (b) bluefin tuna (Thunnus thynnus)

reproductive stage by month for fish sampled in the Gulf of Maine

from 2000 to 2002. Stages 1–3 for both sexes = immature or non-

maturing, stages 4–5 = mature active, stage 6 = mature-inactive

Mar Biol

123

and to continue spermiating after females have ceased

spawning (Burton and Idler 1984), but there is little

information regarding the post-spawning condition of

bluefin tuna males. Whether males producing active sperm

are capable of spawning in the absence of appropriate

environmental cues is unknown.

Females

Females entering the Gulf of Maine in June and July were

more likely to be in stage 6 (mature-inactive) than in stage 1

(immature or non-maturing) (Fig. 3b). After July, no fe-

males were found to be in a mature-inactive state. Females

exhibited two reproductive schedules, with all females

between 235 and 265 cm in the immature or non-maturing

state (stage 1), while smaller females (185–235 cm) were

significantly more likely to be in a mature-inactive state

(stage 6). Given the assigned age of females over 235 cm

(>>10 years), they are most likely mature fish traveling

from distant spawning grounds that have had sufficient time

to resorb oocytes and atretic follicles. The presence of rel-

atively small females (185–235 cm) in the mature-inactive

state is unexpected because (1) it indicates that some bluefin

tuna of assigned age 7–8 years are mature, despite the

apparent absence of this size/age class in the Gulf of Mexico

during the spawning season (Block et al. 2005), and (2)

maturity should not be detectable in animals that have

spawned at such great distances from the Gulf of Maine

(e.g., Gulf of Mexico or Mediterranean Sea). There are

several scenarios that could explain this finding.

Scenario I: natural variation

Large and small bluefin tuna could be arriving from the

same previous location with differences in reproductive

state reflecting normal variation in resorption time for fish

of different sizes/ages. Given that energetic reserves are

likely to be in short supply after spawning and migration,

rapid resorption of oocytes and follicles by all size classes

seems likely. Furthermore, we would expect to see a

greater proportion of larger fish rather than smaller fish

with unresorbed follicles, as the former should have greater

endogenous energy reserves.

Scenario II: arrival from different areas

Alternatively, different size/age classes may be arriving in

the Gulf of Maine from different spawning locations.

Similar results have been found for Pacific bluefin (Thun-

nus orientalis), which segregate to different spawning re-

gions based on size (Itoh 2006). Older, experienced

spawners may be coming from the Gulf of Mexico region

or more remote locations such as the Windward Passage

and other Caribbean areas, where adult bluefin tuna ‘‘in

near spawning condition’’ were documented in the RV

Crawford Cruise 62 of 19 April–8 June 1961 (Rathjen

1961). Smaller mature-inactive fish may have come from a

spawning location closer to the Gulf of Maine, lacking the

time to completely resorb vitellogenic oocytes. Although

the Gulf Stream margin has been dismissed as an important

spawning area for bluefin tuna because few larvae have

been found there (McGowan and Richards 1989), bluefin

spawning on its southern extension, the Loop Current, is

well established (Richards 1976). Mather hypothesized

(1973) that young bluefin tuna reaching maturity for the

first time may spawn on the northern edge of the Gulf

Stream, or in its warm core eddies. In tagging studies ini-

tiated in the Gulf of Maine, F. Royer et al. (unpublished

data) discerned seasonal patterns of behavior, and found

that some bluefin tuna moved from wintering areas off the

northeast continental slope to areas along the Gulf Stream

edge and Sargasso Sea during the spawning season of

April–June. Smaller mature-inactive fish may be coming

from this region rather than the Gulf of Mexico. It is also

possible that some of the sampled fish may have Medi-

terranean origins (Rooker and Secor 2004; Block et al.

2005), which mature at a younger age (3–5 years) than

members of the Western stock. This may explain why 7–8-

year-old fish in our sample were mature, but not why those

signs were detectable so far away from Mediterranean

spawning grounds

Scenario III: skipping a reproductive event

A third scenario may be that not all fish are spawning

annually, a hypothesis advanced to explain the presence of

spawning sized bluefin tuna located in the central north

Atlantic and elsewhere during the presumed spawning

period (Lutcavage et al. 1999; Wilson et al. 2005; Sibert

et al. 2006). Mature sized bluefin tuna sampled at feeding/

wintering grounds during the spawning season in the

Mediterranean had ovaries with no signs of previous or

imminent spawning, but displayed high levels of vitello-

genic atresia (Corriero et al. 2003), similar to mature fish

from our study, which has often been interpreted as a sign

of cessation of spawning or failure to attain final oocyte

maturation (Hunter et al. 1986; Mylonas et al. 1997; Farley

and Davis 1998; Schaefer 1998). Smaller mature-inactive

fish may have skipped spawning and so did not travel to

remote spawning locations.

Recent models on the Northeast Arctic cod stock, also a

long-lived, migratory, iteroparous species, showed that

skipped spawning was quite common, especially among

smaller size classes and younger fish, and was more com-

mon among females, and when feeding conditions were

poor and the energetic cost of migration was high

Mar Biol

123

(Jorgensen et al. 2006). Rideout et al. (2005) lists 21 spe-

cies in which skipped spawning has been documented, and

cites poor nutritional condition of non-spawners as the

most common reason. This phenomenon may be quite

common, but often goes undocumented due to the diffi-

culties in identifying non-reproductive individuals (Rideout

et al. 2005). Evidence from captive breeding experiments

(Lioka et al. 2000) and long-term historical data sets on the

Mediterranean trap fishery (Royer and Fromentin 2006)

suggests that some bluefin tuna may have a 2–3 year

spawning cycle, contrary to the common presumption of an

annual reproductive cycle.

Spatial-temporal patterns

Evidence for a more varied spawning cycle than the cur-

rently accepted paradigm suggests can be seen by exam-

ining historical records for the months of January–June.

Reproductive condition was recorded for 49 bluefin tuna

sampled during exploratory longline cruises conducted by

the MV Delaware in the 1960s (Wilson 1965). Although

qualitative in nature, gonad status estimated by the chief

scientist (P. Wilson, unpublished data, see Appendix 1)

indicates fish sampled along the Gulf Stream edge and

adjacent waters (Fig. 4) in March and April (mean CFL

198 ± 12.3 cm) were found in a mature or mature-inactive

state, including spent, ripening, and running (males, milt)

(Wilson 1965). In contrast, studies on bluefin tuna of

similar size sampled by coastal fisheries (with the excep-

tion of males in this study), have found little evidence of

active spawning. Seventeen fish (164–226 cm CFL,

x = 203 cm, males, 207 cm, females) sampled in January–

March 1995 off coastal North Carolina showed no signs of

spawning activity (Belle 1996), however, most were cap-

tured in winter sea surface temperatures <24�C (Fig. 4).

Baglin’s (1982) sampling in the Mid-Atlantic Bight found

no evidence of spawning activity in June, July and August

but all fish sampled were assigned age 7 or younger.

Conclusions

The range of post-reproductive states present well outside

of known spawning areas from this study and from his-

torical cruise data combined with recent electronic tagging

results lends evidence to a more asynchronous model for

bluefin tuna reproduction than previously assumed. Males

of commercial sizes (185–263 cm CFL) and small females

(185–235 cm CFL) arriving in June and July in mature or

mature-inactive condition may indicate that spawning has

occurred outside of known spawning areas, or spawning

has been omitted during the last maturity cycle. This result

is particularly striking given that the mean age of elec-

tronically tagged bluefin tuna present on the spawning

grounds are ages 11 and above (‡241 cm CFL) (Block

et al. 2005) and recent analyses on longline data in the Gulf

of Mexico estimate the age of 50% maturity to be 12 years

(Diaz and Turner 2006), although this finding may be

highly biased by size selectivity of longline sampling

(Davis and Farley 2001; Corriero et al. 2003). The exis-

tence of oceanic spawning areas remains a possibility, and

must be addressed by more extensive sampling, and a

complete understanding of the bluefin tuna reproductive

schedule. Sampling that includes fish smaller than 185 cm

CFL should be included to determine the lower size/age

limit of this maturity curve.

Modeling approaches on tuna (Fromentin and Fonteneau

2001) and other species (Stearns and Crandall 1984; Gar-

rod and Horwood 1984; Gunderson 1997; Jorgensen et al.

2006) and applied studies (Hearn and Polacheck 2003)

have shown that life history traits like size and age at

maturity shift in response to environmental stress such as

low food availability and fishing pressure. Age 8 (200 cm

CFL) has been assigned as the age of 100% knife-edge

maturity for western Atlantic bluefin tuna based on sizes

observed on known spawning grounds (Turner et al. 1991)

and not on histological evidence, an approach that has been

criticized for its non-quantitative nature (Schaefer 2001).

Determination of size/age at maturity depends first on

accurately assigning age, which has proven difficult for this

species, particularly in the larger size classes (Turner and

Terceiro 1994). A recent study on bluefin tuna sampled in

Canadian waters indicates that the growth curve most

commonly used to assign ages for the western Atlantic

stock may have shifted (Neilson and Campana 2006),

suggesting that growth curves need to be revised for this

stock (Restrepo et al. 2006).

Our data did not allow us to find a significant link be-

tween body condition and reproductive state but condition

should not be ruled out as a possible factor for determining

differences in migration routes or reproductive status. We

are currently developing a more precise index of condition

based on % lipid in muscle tissue to provide a more

accurate measure of energetic state. Future work will in-

clude muscle tissue biopsies and/or blood samples taken

from electronically tagged individuals which could prove

useful in determining whether sex, (Susca et al. 2000;

Heppell and Sullivan 2000) and/or lipid content of muscle

correlates with migratory and reproductive behavior or

spatial range as has been found in herring (Rajasilta 1992)

and European eels (Larsson et al. 1990)

Acknowledgments We thank Mike Blanchard, Matt Bunnell, John

Caldwell, Bill Chaprales, Rocky Chase, Scott Drabinowicz, Mark

Godfried, Eric and John Hesse, Jeff Tutein, Dave and Greg Wa-

Mar Biol

123

linski, Cape Quality Bluefin and Fresh Water Fish for collecting

samples. We also thank Jennifer Bowdoin and Jennifer Albright for

help with sampling, Kurt Schaefer and Antonio Medina for advice

on histology, Chris Bridges for hormonal analysis, Ben Galuardi for

spatial analysis, and Frank Cyganowski and the late Peter C. Wilson

for use of unpublished materials. This work was supported by

NOAA Grant NA04NMF4550391 to M. Lutcavage. All work was

done under compliance with UNH IACUC and NOAA Exempted

Fishing Permits.

Appendix 1

Station results for bluefin tuna, Thunnus thynnus, caught during research longline cruises conducted by the Bureau of Commercial Fisheries from

March 30 to April 23, 1965

Cruise Spec. # Station Lat.

Deg N

Long.

Deg W

Date CFL* (cm) Weight (kg) Sex Condition

64-3 1 1 38.68 67.62 19-Apr 188 109 F Inactive

64-3 2 1 38.68 67.62 19-Apr 157 79 M Inactive

64-3 3 1 38.68 67.62 19-Apr 176 95 M Inactive

64-3 5 2 38.13 67.55 20-Apr 201 109 F Inactive

64-3 7 2 38.13 67.55 20-Apr 185 91 F Inactive

64-3 9 2 38.13 67.55 20-Apr 183 79 F Inactive

64-3 10 3 38.05 67.10 20-Apr 180 91 F Inactive

64-3 11 3 38.05 67.10 20-Apr 184 102 M Inactive

64-3 12 3 38.05 67.10 20-Apr 163 72 F Inactive

64-3 88 22 38.07 68.02 13-May 197 147 F Spent

64-3 142 40 38.63 68.17 31-May 250 234 F Enlarged

65-3 1 1 35.90 72.85 1-Apr 195 112 M Spent

65-3 2 1 35.90 72.85 1-Apr 190 110 M Spent

65-3 3 1 35.90 72.85 1-Apr 169 78 F Immature

65-3 5 1 35.90 72.85 1-Apr 206 142 M Ripening

65-3 6 1 35.90 72.85 1-Apr NA NA F Spent

65-3 7 1 35.90 72.85 1-Apr 194 110 F Spent

65-3 8 1 35.90 72.85 1-Apr 194 112 F Spent

65-3 10 1 35.90 72.85 1-Apr 192 104 M NA

65-3 11 1 35.90 72.85 1-Apr 199 116 F NA

65-3 12 1 35.90 72.85 1-Apr 178 86 F NA

65-3 17 1 35.90 72.85 1-Apr 192 104 M Spent

65-3 18 2 35.55 74.20 4-Apr 198 116 F Spent

65-3 20 2 35.55 74.20 4-Apr 188 101 F Spent

65-3 21 2 35.55 74.20 4-Apr 191 99 M Spent

65-3 42 6 35.53 73.25 6-Apr 224 164 M Ripe

65-3 43 6 35.53 73.25 6-Apr 198 120 F Spent

65-3 44 6 35.53 73.25 6-Apr 209 127 M Ripening

65-3 45 6 35.53 73.25 6-Apr 229 169 F Spent

65-3 46 6 35.53 73.25 6-Apr 223 162 F Spent

65-3 47 6 35.53 73.25 6-Apr 209 137 F Ripening

65-3 48 6 35.53 73.25 6-Apr 199 121 F Spent

65-3 57 8 35.93 72.53 8-Apr 206 119 M Running

65-3 63 8 35.93 72.53 8-Apr 200 117 M Running

65-3 65 8 35.93 72.53 8-Apr 191 114 M Running

65-3 66 8 35.93 72.53 8-Apr 213 140 M Running

65-3 67 8 35.93 72.53 8-Apr 214 138 M Running

65-3 82 9 35.93 72.53 15-Apr 189 105 M Running

66-2 1 1 38.12 70.92 10-Mar 215 145 M Inactive

66-2 7 1 38.12 70.92 10-Mar 212 143 M Inactive

66-2 8 1 38.12 70.92 10-Mar 195 114 NA NA

Mar Biol

123

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