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JOURNAL OF CRUSTACEAN BIOLOGY, 22(4): 762774, 2002

MATURITY AND REPRODUCTIVE CYCLE OF THE FEMALE AMERICAN LOBSTER, HOMARUS AMERICANUS, IN THE SOUTHERN GULF OF ST. LAWRENCE, CANADA Michel Comeau and Fernand Savoie
Department of Fisheries and Oceans, Science Branch, P.O. Box 5030, Moncton, New Brunswick, E1C 9B6, Canada (corresponding author (MC) e-mail: comeaum@dfo-mpo.gc.ca) ABSTRACT
The maturity and reproductive cycle of female American lobsters (Homarus americanus) were investigated in the southern Gulf of St. Lawrence (sGSL), Canada. The onset of sexual maturity of female lobsters can be established by observations of the ovarian condition, either color or weight, and staging of cement glands but cannot be detected by the morphometry of their abdomens. Females reached 50% maturity between 68.7 mm and 73.3 mm carapace length (LC). There was a signicant geographic difference (P , 0.005) in the size at 50% maturity established by the ovarian development techniques but not by the cement-gland staging technique. Also, there were no annual signicant differences (P . 0.005) between the ovarian development techniques used at a single site between 1994 and 1997. To study the reproductive cycle of females, molt stage, ovarian development, and egg spawning were monitored by dissections at the laboratory and by tagging studies in the eld. The majority (80%) of small mature females (LC , 120 mm) in the sGSL had a typical two-year reproductive cycle with molting (with copulation) and spawning in alternating years. However, up to 20% of multiparous females ranging between 65 mm and 109 mm LC could spawn in successive years instead of the generally accepted twoyear cycle, and some could even molt and spawn during the same summer. Similarly, up to 20% of primiparous females could molt and spawn (for the rst time) in the same year instead of spawning the following year. A small percentage (5%) of small mature females could also skip molting or spawning for a year. Temperature data suggested that the length of the female reproductive cycle, and possibility of molting and spawning in the same year, were related to the number of degree-days in a particular season.

The American lobster (Homarus americanus Milne Edwards, 1837) is one of the most valuable commercial species landed in Eastern Canada. One of the key elements to achieve a healthy shery is assuring a good egg production by allowing females to spawn before being captured (Anonymous, 1995). Hence, a good knowledge of the female size at maturity is essential for a sound management of the shery and is often used as one of a suite of references to dene the minimal legal size at capture for the lobster (Campbell, 1985). Lobster mating in the southern Gulf of St. Lawrence (sGSL) occurs between July and September. Small female lobsters (carapace length , 120 mm) are thought to follow a two-year reproductive cycle (Aiken and Waddy, 1982). In a typical cycle, females are molting and mating during the same summer, extruding the eggs the following year, and carrying them attached on pleopods under the abdomen for nearly another year. This

two-year reproductive cycle may be shortened to one year for primiparous females by uctuation of environment factors, mainly temperature (Templeman, 1934, 1936; Waddy and Aiken, 1992; Waddy et al., 1995). The reproductive cycle is also inuenced by the female size, as larger females can spawn in successive years before molting (Waddy and Aiken, 1986). Maturity of female crustaceans can generally be dened as the ability either to produce mature oocytes (gonadal maturity) or to mate and spawn efciently (functional maturity). The size at maturity for female American lobster can be established directly by the presence or absence of eggs under the abdomen (ovigerous or berried females) or indirectly by observations of the ovarian condition, the formation of specialized glands in pleopods needed to attach the eggs after spawning (Aiken and Waddy, 1982), and morphometry (Aiken and Waddy, 1980). Because there is a direct relationship

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Table 1. The year, area, date, and number of female lobsters (Homarus americanus) collected to establish the reproductive cycle, and the onset of sexual maturity based on cement-gland staging, weight, and color of the ovaries.
Number of females dissected Ovaries Year Area Date Total Pleopod Color Weight Berried female

1994 1994 1994 1995 1995 1996 1996 1997

AB CR MI CR ST CR VC CR

May 16July May 11July May 17July May 16July May 18July June 6 June 11 June 4

26 21 12 17 18

263 336 154 309 310 257 324 296

258 330 116 305 310 255 323 296

260 328 153 306 307 257 324 296

261 327 153 306 307 257 324 296

8 18 8 32 5

AB: Anse-Bleue; CR: Caraquet; MI: Miscou; ST: Stonehaven; VC: Val Comeau.

between the maturity of the ovaries and egg laying or mating (Aiken and Waddy, 1982; Waddy et al., 1995), the size of gonadal and functional maturity is the same. Detecting sexual maturity in female lobster by morphometry is achieved by plotting the maturity index against carapace length (LC) (Simpson, 1961). However, Ennis (1980) noted that the inections and asymptotes of the morphometric method were sometimes not very distinct and concluded that considerable caution must be exercised when interpreting the maturity index for females. Conan et al. (1985) examined this technique on females from the sGSL and concluded that the allometry of the abdominal segment was not adequate to detect sexual maturity. In the sGSL, Campbell and Robinson (1983) established the size at which 50% of females reach maturity (50% maturity) at 78.5 mm LC based on the development of cement glands in pleopods, which is higher than the estimates of 70.9 mm and 71.7 mm LC based on the development of cement glands and ovarian observations, respectively, established by Conan et al. (1985). Because knowledge of the size at 50% maturity is essential for the management of the resource, it is essential to investigate the different methods used to establish female sexual maturity, to fully understand their limits, and to select the most appropriate method. The purpose of this paper is to compare the size at 50% maturity being established by the development of cement glands in pleopods, abdominal morphometry, and color and weight of the ovaries for female lobsters from the sGSL. Annual and regional variations of the size at the onset of female maturity and the reproductive cycle of female lobsters were also investigated.

MATERIALS AND METHODS


Study Sites Two thousand, two hundred forty-nine (2,249) female lobsters were captured between 1993 and 1997 (Table 1) at ve sites in northeastern New Brunswick (Fig. 1). Females from the Caraquet locations were collected every year (Table 1). The sites adjacent to Caraquet at Anse-Bleue and Miscou were sampled in 1994, and the sites at Stonehaven and Val Comeau were sampled only in 1995 and 1996, respectively (Table 1). Seventy-one (71) berried females were collected in mid-July (1226 July) in 1994 and 1995 (Table 1) and dissected at the laboratory. Temperature Temperature data were collected by using an electronic recorder from a stationary mooring at 18-m depth in Caraquet between 1995 and 1997. The 1995 temperature data were taken from Lanteigne et al. (1996). Degree-days were calculated as the cumulative sum of daily mean temperatures recorded above 08C. We assumed that the temperatures recorded at Caraquet were representative for Baie des Chaleurs (Fig. 1). Tagging Berried females were tagged on board the vessel immediately after being captured in the area encompassing the sites of Stonehaven to Miscou Island (Fig. 1) between 1993 and 1998 to monitor their reproductive cycle. A total of 118 females with eggs in an early development stage were tagged, as described by Moriyasu et al. (1995) and Comeau et al. (1998), with streamer tags between September and November. These tags are retained between molts. Information on the recaptured female size and presence of eggs was noted during the subsequent shing seasons (MayJune). A total of 209 females with well-developed eggs (or empty eggshell) under the abdomen were tagged in early July. Information on the recaptured female was noted only for the shing season following the tagging. Unlike for tagged females with eggs in an early development stage, only the shing season following tagging for tagged females with well-developed eggs was considered relevant, because any change in their condition (presence of eggs or an increase in LC) observed after more than a year at large cannot be unambiguously attributed to the rst or second year at large.

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Fig. 1. Geographic location of sampling sites in the southern Gulf of St. Lawrence.

Laboratory At the laboratory, the carapace length (LC) of each female collected (Table 1) was measured, and in 1996, the abdominal width (AW) was also measured for females from Caraquet. For all females, the second pleopod on the left side was removed for examination under a stereomicroscope with magnication of 364. The molt stage was established by the pleopod reading method (Aiken, 1973), which is efcient to determine intermolt (C4) and premolt stages (D0 to D3). Maturity of females was estimated by examining developmental stages of cement glands in the pleopod (Aiken and Waddy, 1982). Females in postmolt and intermolt with well-developed cement glands (stages 2 to 4), indicating imminent egg extrusion during the current

spawning season, were considered as mature. Females in premolt stages with well-developed cement glands were not considered as mature because they will molt before spawning, which results in an erroneous assessment of the size at maturity. The ovaries of females measured were weighed to the nearest 0.0001 g, and the color was noted to establish maturity. The ovary condition was divided into six development stages based on their color (Aiken and Waddy, 1980): 1) immature (white); 2) immature developing (beige, yellow, olive); 3) developing (light green); 4) developing (medium green); 5) developing (dark green); 6) ripe (dark green with free oocytes) (Table 2). The color standardization was done on fresh ovary samples using the Pantone Color

Table 2. Developmental stages of female lobster (Homarus americanus) ovaries based on color.
Developmental stage Maturity stage Color Pantone color*

1-Immature 2-Immature developing 3-Developing** 4-Developing** 5-Developing** 6-Ripe**

Immature Immature Immature Immature Mature Mature

White Beige Yellow Olive Light green Medium green Dark green Dark green with free oocytes

1205c, 125c 120c, 121c, 122c, 123c, 116c 111c, 583c 576c 575c, 574c 350c, 553c, 5535c 5535c

* Color standardization using the Pantone Color Formula Guide 1000 (Pantone, Inc. New Jersey, 07072-3098, U.S.A.). ** Observed from stages 3 to 6, residual oocytes from previous egg extrusion characterized by yellow patches in the ovaries. These yellow patches are identied by Pantone color 108c. Females with yellow patches in the ovaries are considered as mature.

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compared for annual and regional variations using a deviance analysis implemented in SAS (PROC GENMOD; SAS Institute, Inc., 1996). The results of the maturity status determined by two different techniques, i.e., the cement-gland staging technique and the ovarian development technique, were compared. The latter technique is thought to be more accurate (Waddy et al., 1995).

RESULTS Temperature The accumulation of degree-days was different between 1995 and 199697 (Fig. 2). Degree-days from May 21 to October 2 reached 1,190, 955, and 924 in 1995, 1996, and 1997, respectively. Weekly accumulation of degreedays was not similar between years, as the spring was colder, and the summer-fall was warmer in 1995 compared to the following two years (Fig. 2). Reproductive Cycle Based on the tag-recapture experiment of berried females, it was possible to observe the sequence of molting and spawning of these females. A total of 41 females tagged in the fall while carrying eggs in an early development stage were recaptured in MayJune the following years. As anticipated, females recaptured during the year following their fall tagging (their rst recovery period, n 36) were still carrying eggs, because they would have released their larvae only in July. Five females were recaptured in MayJune during their second year at large, and four (LC ranging from 71 mm to 88 mm) had released their larvae and molted without extruding another batch of eggs. Only one female (66 mm LC) released her larvae, molted, and spawned. Of the females tagged in July and carrying well-developed eggs, a total of 40 were recaptured in MayJune of the following year. Thirty-two (80%) females (LC ranging from 69 mm to 89 mm) had molted immediately after being tagged without extruding eggs. Two (5%) small females of 69 mm and 77 mm LC tagged in July of 1994 and 1996, respectively, had neither molted nor extruded eggs. Six females (LC ranging between 65 mm and 82 mm) were recaptured while berried. The size information was available for only two of these berried, multiparous females (69 mm and 76 mm LC), and it revealed that they had also molted before spawning. A total of 34 and 37 berried females collected in 1994 and 1995, respectively, were

Fig. 2. Degree-days relationship of temperature recorded at a depth of 18 m in Caraquet between 1995 and 1997 starting on May 21. Temperature data from 1995 were taken from Lanteigne et al. (1996).

Formula Guide 1000 (Pantone Inc. New Jersey, 070723098, U.S.A.). Females in postmolt and intermolt with gonads in stages 5 and 6 were considered mature. For the same reason as for the cement-gland staging technique, premolt females in stages 5 and 6 were not considered as mature. Females were considered mature independently of their molting stage if an indication of a previous spawning, characterized by residual oocytes (yellow patches) within the ovaries (Aiken and Waddy, 1980; M. Comeau, personal observation), was observed. Statistical Analysis The allometry of the female abdomen was investigated by tting a linear regression to the AW vs. LC plot. The morphometric maturity was established using the maturity index (AW/LC ratio) plotted against LC (Aiken and Waddy, 1980). The female maturity status was also established using the ovary factor (Of) based on the weight of the ovaries (Aiken and Waddy, 1980). The Of is the ratio between the ovary weight in mg and the cube of LC in cm multiplied by a factor of 10 ([ovary weight (mg)/[LC (cm)]3] 3 10). A female was considered mature if 1) the Of value was superior to the Ofm in a given year, and 2) the female was in postmolt or intermolt stage. For a given year, the Ofm value used to establish maturity was set at the 5% percentile of the observed Of from females in stage 5 based on the color of the ovaries. As mentioned for the color of the ovaries, a female was considered mature if an indication of a previous spawning was observed. The S-shaped curves representing the proportion of mature female within each size class of 1 mm LC established by cement gland staging, the color of the ovaries, and the Of were modeled by the logistic equation: P 1 1 expabLC

where P is the proportion, LC the carapace length, a and b are tted parameters. The logistic equation was tted using the maximum likelihood implemented in SAS (PROC GENMOD; SAS Institute, Inc., 1996). The logistic curves generated for different area and maturity criteria were

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Table 3. Condition of primiparous and berried female lobsters (Homarus americanus) collected in the southern Gulf of St. Lawrence and dissected at the laboratory between 1994 and 1997. Ovaries in stages 5 and 6 were an indication of imminent spawning. The incidence of molting was established by pleopod reading.
Primiparous females Year Spawning Molting and spawning Number dissected Molting Berried females Spawning Molting and spawning

1994 1995 1996 1997

408 229 202 190

9 9 37 25

34 37

15 26

5 6

3 4

dissected to evaluate their molt stage and ovarian development (Table 3). The ovaries of all the berried females showed oocyte reabsorption (Aiken and Waddy, 1980), characterized by yellow patches. Up to 50% (n 17) in 1994 and 24% (n 9) in 1995 of the berried females were not preparing to either molt or extrude another batch of eggs. Approximately 15% of the berried females (LC ranging between 67 mm and 109 mm) were preparing to extrude another batch of eggs (Table 3). Approximately 65% of the berried females preparing to spawn were also preparing to molt (Table 3). The duration of the reproductive cycle does not seem to be related to size for females ranging between 65 mm and 109 mm LC (Fig. 3). For primiparous females, the reproductive pattern is quite different between years

(Table 3). In 1994 and 1995, 2% and 4% of the primiparous females were preparing to molt before spawning compared to 18% and 13% in 1996 and 1997 (Table 3). Size at Maturity The relationship of the AW against the LC is linear, and there is no indication of an abrupt change in the allometric relationship to establish the size at the onset of sexual maturity (Fig. 4A). Furthermore, the maturity index does not permit us to establish a size at maturity because the swarm of points from the immature and mature female lobsters (established by ovarian observations) was not discrete (Fig. 4B).

Fig. 3. Relationship between the condition of berried female lobsters (Homarus americanus) and their carapace size. Their condition is dened by the following criteria: 0) without indication of imminent molting or eggs extrusion; 1) in premolt condition (molt stage D) indicating imminent molting; 2) with ripe ovaries (stages 5 and 6), indication of imminent eggs extrusion; and 3) that will both grow and spawn. Conditions 0 and 1 indicate females with a two-year reproductive cycle (at least), and conditions 2 and 3 indicate females with a one-year reproductive cycle.

Fig. 4. Morphometric relationship of female lobsters (Homarus americanus) between A) the abdomen width (AW) and carapace length (LC) (AW 0.94LC 19.47; n 323) and B) the maturity index, dened by the AW/LC ratio and LC (n 323). The maturity of females is established by observations of their ovaries. Correlation coefcients (r) are indicated on the graphs.

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Table 4. Size at 50% maturity for female lobsters (Homarus americanus) collected in northeastern New Brunswick located in the southern Gulf of St. Lawrence. The size at 50% maturity was established using cement-gland staging, color, and weight of the ovaries. Parameters a and b are calculated from the logistic curve modeled by P 1=1 expabLc .
Year Site Method a b Size at 50% maturity

1994

Caraquet Anse-Bleue Miscou

Cement gland Ovary color Ovary weight Cement gland Ovary color Ovary weight Cement gland Ovary color Ovary weight Cement gland Ovary color Ovary weight Cement gland Ovary color Ovary weight Cement gland Ovary color Ovary weight Cement gland Ovary color Ovary weight Cement gland Ovary color Ovary weight

16.24 16.83 13.74 13.70 19.02 18.96 17.00 17.63 15.72 14.97 24.45 19.54 17.76 20.49 16.29 17.36 20.85 17.79 18.73 26.42 25.00 20.93 21.85 17.82

0.2260 0.2392 0.1999 0.1885 0.2632 0.2672 0.2325 0.2437 0.2191 0.2117 0.3453 0.2840 0.2514 0.2797 0.2264 0.2464 0.2977 0.2545 0.2607 0.3657 0.3456 0.2974 0.3101 0.2543

71.9 70.4 68.7 72.7 72.3 71.0 73.1 72.4 71.8 70.7 70.8 68.8 70.6 73.3 71.9 70.4 70.0 69.9 71.8 72.3 72.3 70.4 70.5 70.1

1995

Caraquet Stonehaven

1996

Caraquet Val Comeau

1997

Caraquet

The size at the onset of sexual maturity was established by using pleopod reading for cement gland development, and by the color and weight of ovaries. In northeastern New Brunswick, the size at 50% maturity calculated from the logistic model ranged between 68.7 mm and 73.3 mm LC (Table 4). No signicant geographic differences (P . 0.005) were observed for the size at maturity established by cementgland staging (Table 5). There was no signicant difference (P . 0.005) between areas in

the size at maturity established by ovarian condition for the three sites examined in 1994 (Table 5). There were signicant geographic differences (P , 0.005) in the size at maturity established by the ovarian condition for the sites examined in 1995 and 1996 (Table 5). Both measures of ovary condition (weight and color) indicated that the size at maturity of lobsters from Caraquet was smaller than that of the ones from Stonehaven (1995) and Val Comeau (1996). For each year, there was no

Table 5. Geographical comparison of the probability for a female lobster (Homarus americanus) to be mature based on a single method for a given year. Female lobsters were collected in the southern Gulf of St. Lawrence. The comparison was done using the deviance analysis.
Year Sites Method P-value

1994

Caraqeut vs. Anse-Bleue vs. Miscou

Cement gland Ovary color Ovary weight Cement gland Ovary color Ovary weight Cement gland Ovary color Ovary weight

0.6671 0.0984 0.0884 0.6228 0.0028 0.0004 0.2150 0.0014 0.0002

1995

Caraquet vs. Stonehaven

1996

Caraquet vs. Val Comeau

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Table 6. Comparison of the probability for a female lobster (Homarus americanus) to be mature at a particular site for a given year based on pleopod reading, color, and weight of the ovaries. The comparison was done using the deviance analysis.
P-value Year Site All three methods Ovary color vs. ovary weight

Table 7. Consistency of the cement-gland staging technique compared to the ovary-color technique to determine the maturity status of each female lobster (Homarus americanus).
Year Area n* Total matched Percentage

1994 Caraquet Anse-Bleue Miscou 1995 Caraquet Stonehaven 1996 Caraquet Val Comeau 1997 Caraquet

0.0060 0.1093 0.1997 0.0014 0.0056 0.7960 0.0872 0.7601

0.3043 0.9858 0.6232 0.1772 0.2007 0.3628 0.7186 0.2150

1994 1994 1994 1994 1995 1995 1995 1996 1966 1996 1997 Grand total

Anse-Bleue Caraquet Miscou All Stonehaven Caraquet All Val Comeau Caraquet All Caraquet

247 310 108 665 302 273 575 323 255 578 296 2,114

193 214 84 491 230 213 443 274 206 470 263 1,677

79 69 78 74 76 78 77 85 80 81 89 79

signicant difference (P . 0.005) in the size at maturity established by the ovarian condition for a particular site (Table 6). Comparisons of the three techniques showed signicant differences (P , 0.005) in three cases (Table 6). However, when the cement-gland staging technique was removed, there was no signicant difference (P . 0.005), suggesting that this technique was inconsistent. Thus, the estimated size at 50% maturity for female lobsters could depend on both the geographic location and the technique being used. The consistency of the cement-gland staging technique when compared to the ovary-color technique varied between 69% and 89% (Table 7). The yearly level increased steadily from 74% in 1994 to 89% in 1997 (Table 7). The discrepancy between the determination of the maturity status of a female was related not to the time of the sampling in our study but rather to whether the female had already spawned at least once and to the subjectivity of the cement-gland staging technique. Female lobster data collected in Caraquet from 1994 to 1997 were pooled for each method because there were no interannual signicant differences (P . 0.005). The size at 50% maturity for each method was calculated using the logistic curve model (Fig. 5) and ranged between 69.4 mm and 70.9 mm LC for females from Caraquet. DISCUSSION Reproductive Cycle The one-year reproductive cycle of mature females, involving molting and spawning in the same year, may seem to be more wide-

*n is the total number of females examined by both techniques.

spread than it has been believed (Aiken and Waddy, 1980; Waddy et al., 1995) in the sGSL lobster population. Available data suggest that female lobsters smaller than 120 mm LC will produce eggs every two years, whereas larger females could alternate between a one- and a two-year reproductive cycle (Aiken and Waddy, 1980; Waddy and Aiken, 1986; Waddy et al., 1995). However, Aiken and Waddy (1982) reported a variation from the typical two-year reproductive cycle based on aquarium observations of small primiparous females from the sGSL. Aside from the normal two-year cycle with molting and egg laying occurring in alternate years, they reported that up to 20% of primiparous females could also molt and then extrude eggs in the same year (they called these females Adult-Ib). Similarly, Robinson (1979) reported molting and spawning in the same year for around 20% of the primiparous females based on tagging studies carried out in the sGSL. Our ndings also indicate that between 2% and 18% of primiparous females could molt and spawn in the same year. Outside the sGSL, Ennis (1980, 1984) and Briggs and McGroarty (1985) also reported that small primiparous females from Newfoundland and Long Island Sound, respectively, could molt and extrude eggs in the same year. Thus, a substantial fraction (20%) of primiparous females show a one-year reproductive cycle. Except for female lobsters from the Long Island Sound area (Briggs and McGroarty, 1985), the occurrence of molting and spawning

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Fig. 5. Relationship (P 1=1 expabLc ) between the proportion of female lobsters (Homarus americanus) reaching maturity and their carapace length used to establish the size at 50% maturity. The female maturity was established by (A) cement-gland staging (a 16.94; b 0.239; 50% maturity at 70.9 mm LC); (B) the color of the ovary (a 20.75; b 0.2945; 50% maturity at 70.5 mm LC); and (C) the weight of the ovary (a 17.17; b 0.2475; 50% maturity at 69.4 mm LC) dened as the ovary index (Of). Females were collected between 1994 and 1997 in Caraquet.

in the same summer is generally accepted as unusual and rare for multiparous females in the wild (Aiken and Waddy 1982; Waddy et al., 1995). However, based on our ndings from tagging studies and observations of the ovarian condition of berried females, molting and spawning in the same year is not restricted to small primiparous females, nor is the one-year reproductive cycle limited to larger females (LC . 120 mm) in the sGSL. We found that 15% to 20% of tagged berried females ranging between 65 mm and 82 mm LC were observed with eggs for two consecutive years, indicating a one-year reproductive cycle. Moreover, there were also indications that some multiparous females had also molted between spawning. Around 15% of the berried females dissected (LC ranging between 67 mm and 109 mm) were ready to spawn, indicating a one-year reproductive cycle, and 10% showed signs of molting before spawning. Hence, females from the sGSL have the opportunity to produce over the years a larger quantity of eggs than females observed in areas restricted to a two-year reproductive cycle. Temperature seems to be an important environmental factor inuencing the reproductive cycle of both primiparous and multiparous fe-

males in the sGSL. Aiken and Waddy (1982) suggested that Adult-Ib females in areas with higher summer water temperatures would have the opportunity to both molt and spawn in the same year. In our study, the sharp increase in the incidence of primiparous females with indications of molting and spawning in the same year was observed between 1995 (4%) and 1996 (18%). The lower incidence observed in 1995 could be due to cold spring temperatures observed that year. Also, the degree-day proles were quite similar in 1996 and 1997, and the incidence of primiparous females with indications of molting and spawning were similar. In Newfoundland, Ennis (1980) also observed that the variation in the incidence of molting and spawning in the same summer for primiparous females studied over several years in different locations was related to temperature. In addition, Robinson (1979) reported that in the cold water off the coast of Nova Scotia (NS) less than 1% of primiparous females molted and spawned in the same year. Thus, the temperature regime of warm temperatures (. 208C) observed in the sGSL during the summer might explain primiparous females molting and spawning in the same year. Furthermore, the high temperature regime in the sGSL could also explain the one-year reproductive cycle, with or without molting, of small (LC , 120 mm) multiparous females. The only other area where multiparous females were reported to release their larvae, molt, and spawn in the same year was in the Long Island Sound (Briggs and McGroarty, 1985), which is close to the southern limit of the American lobster distribution. The Long Island Sound is also characterized by warm water temperature in the summer. Hence, it seems that a common factor determining a one-year reproductive cycle for multiparous females could be the high water temperatures experienced by females during the summer and the fall seasons at those two locations. Small berried females in the sGSL could also skip both molting and spawning for a year during their reproductive cycle. As indicated by Waddy and Aiken (1986) for large females (LC . 120 mm), we observed that a few (5%) small berried females (LC , 80 mm) with welldeveloped eggs did not molt or extrude eggs over the summer after releasing their larvae. However, we do not have any information about whether these females would have molted and/or spawned the following summer. Hypothetically, if those females spawned the

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following summer, with or without molting, they could still be considered to be on a twoyear reproductive cycle. The alternative is that they only molted the following summer and waited another year before spawning, indicating a three-year cycle (three years before producing larvae). We also observed that berried females (up to 50%) dissected in July 1994 and 1995 with well-developed eggs or empty egg shells were not preparing to molt or extrude eggs. Because cold seasonal water temperatures could inuence the reproductive cycle of primiparous females, it could perhaps also inuence berried females for their next egg extrusion. It is possible that they could have accumulated enough energy during the warmer summer months to molt later in the molting season. However, it is very unlikely that they could have developed their ovaries for spawning, because ovaries require a large amount of energy to develop (Aiken and Waddy, 1982). Hence, skipping a molt and not spawning for an entire year is perhaps caused by interannual variation in environmental conditions for a small number of small females in the sGSL. Size at Maturity The onset of female American lobster sexual maturity, dened by the possibility to carry eggs, cannot be established based on the maturity index using the morphometry of the abdomen. The relationship between AW and LC was linear in our study. Squires (1970) and Conan et al. (1985) also observed a linear relationship in their studies. Furthermore, Ennis (1980) has indicated that the inections and asymptotes needed to establish the size at maturity are not very distinct based on the LC/AW vs. LC graphs. Similarly, Tully et al. (2001) was unable to match maturity based on the maturity index (morphometric maturity) with maturity based on ovarian condition for the European lobster (H. gammarus Linnaeus, 1758). Given negative results in this and other studies, we do not recommend that the maturity index based on the morphometry of the abdomen be used to detect the onset of female sexual maturity in lobsters of the genus Homarus. Our results on the size at 50% maturity are similar to the ones reported by Conan et al. (1985) for female lobster collected in the sGSL (northern Prince Edward Island). Judging by the ovarian condition, they reported that females reach 50% maturity at a size of 70.9 mm LC, compared to between 69.4 mm and 70.5

mm LC in this study. Similarly, the size at 50% maturity determined by cement-gland staging was reported to be 71.7 mm LC by Conan et al. (1985) compared to 70.9 mm LC in this study. These sizes are, however, smaller than the one reported by Campbell and Robinson (1983) for female lobster from the sGSL (Northumberland Strait). They reported a size at 50% maturity of 78.5 mm LC based on cement-gland staging. This difference could be explained, however, by the criterion used to determine the size at maturity. Conversely to Campbell and Robinson (1983), Conan et al. (1985) used the cement-glands developmental stage 2 to identify a mature female instead of the stage 3. We also used the stage 2. It is clear that using stage 3 will underestimate the number of mature females observed, thus giving a larger size at 50% maturity. We believed that with the cement-gland staging technique, female maturity should be established using stage 2 because the estimated size at 50% maturity is closer to the ones established with the ovarian techniques. Although an accurate comparison is difcult because of the different techniques used to determine maturity, female lobsters from the sGSL seem to reach maturity at smaller sizes compared to females from other areas, and the difference could be due to high summer water temperature. Females from the eastern shore of Nova Scotia (Campbell and Robinson, 1983), the Bay of Fundy (Campbell and Robinson, 1983), the coast of Maine (Krouse, 1973), and Massachusetts (Estrella and McKiernan, 1989) were reported to reach 50% maturity at a size of 90 mm LC or larger (LC up to 108.1 mm) in a cold summer water temperature environment. Briggs and Mushacke (1979, 1980) reported that females from the warm summer water temperature of Long Island Sound reach 50% maturity at sizes ranging between 70 mm and 74 mm LC compared to 86 mm and 90 mm LC for females from the colder summer temperature of the Atlantic Ocean off Long Island. Similarly, Estrella and McKiernan (1989) observed that females from Buzzards Bay, Massachusetts, reach 50% maturity at a size of 76 mm LC compared to 89 mm to 97 mm LC for females in nearshore colder summer water temperature of the Gulf of Maine. Although the Long Island Sound is geographically far from the sGSL (some 1,400 km south), female lobsters seem to share a similar characteristic in terms of size at maturity, probably because of com-

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Fig. 6. Schematic illustrating the characteristics used to establish maturity for the female American lobster (Homarus americanus) based on pleopod reading, color, and weight (ovarian factor) of the ovaries.

parable environment especially in the summer season, i.e., warm summer water condition. The only exception to this apparent pattern is that females inhabiting waters colder than sGSL in Newfoundland reach 50% maturity between 71 mm and 76 mm LC (Squires, 1970; Ennis, 1971, 1980). Our ndings showed that although the development of cement glands in the pleopods could be used to determine female maturity, techniques using the ovarian condition were more reliable and accurate. We found that there are two sources of error with the cement-gland staging technique. Firstly, this technique uses an arbitrary criterion rather than a measurement to determine female sexual maturity. It is based on a subjective evaluation of the level of cement gland engorgement in the pleopods. In addition, we observed that the accuracy level increased with time as the reader became more familiar with the technique. Secondly, this technique, based solely on the pleopod observation, cannot accurately identify females that have already spawned at least once. Nevertheless, the cement-gland staging technique has the advantage of being fast and nondestructive. We agree with Waddy et al. (1995) that re-

ported that the cement-gland staging technique does not provide results as accurate as the ovarian condition techniques. The most accurate ovarian condition techniques, however, require dissecting females to determine the degree of ovarian development. It also allows determination of whether a female has already spawned at least once. Based on our ndings, the color of the ovaries is an accurate and objective technique if a color standardization of fresh ovary samples is done. It gives the same results as the Of technique, but it does not require a high precision scale. The technique using the color of the ovaries is recommended to accurately determine the onset of female lobster sexual maturity. That the maturity status of a female lobster be determined using both growth and maturity characteristics is imperative. We have illustrated a binary identication key for establishing whether a female lobster is immature or mature (Fig. 6). In order to efciently use this key, a wide size-range of nonberried females is needed, and the female dissections should take place approximately one month prior to egg laying. The cement-gland staging technique is a nondestructive technique that can easily be

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done on a large quantity of samples, despite its subjectivity. First, the molting status of the female has to be established. If a female is in premolt stages (D0D3), then at least one more molt is anticipated before the female extrudes a batch of eggs, and she has to be identied as immature. In the case of a nonpremolt female, well-developed cement glands would be an indication of a mature female. However, a truly accurate assessment of the maturity status of a female requires additional physiological information in terms of the color and weight of the ovaries. The identication of females that have already spawned at least once is important because, independently of their molt or ovarian condition, they are mature females. Thus, the rst step for establishing the maturity status of a female using the ovarian techniques is to determine whether a previous spawning has occurred. The reabsorption of unused oocytes is characterized by yellow patches in the ovaries (especially, but not exclusively, in the oviduct area: Aiken and Waddy, 1980), and the female is classied as mature. If no sign of reabsorption is observed, the molting status of the female has to be assessed as mentioned above. A nonpremolt female will be considered mature if the ovary is in stages 5 or 6, if the color of the ovary is the criterion used, or if the Of is superior to a pre-established value (Ofm). We suggest establishing the Ofm value by using the 5% percentile of the observed Of from females in stage 5 based on the color of the ovaries. The schematic illustration presented in Fig. 6 would accurately establish the state of female maturity by using different techniques based on maturity and growth characteristics. Management Implications One of the most important regulations of a lobster shery is the minimal legal size (MLS). Based on elasticity indices derived from matrix projection models, the survival of juvenile and young adult lobsters is critical to efciently manage all American lobster sheries (S. Twombly and S. Cobb, personal communication, University of Rhode Island, Kingston, RI 02881, U.S.A.). Hence, for conservation purposes, the MLS should be set to allow an acceptable number of young mature lobsters to be protected from the shery. Unfortunately, the MLS of 63.5 mm LC imposed in 1957 for the entire sGSL (Lanteigne et al., 1998) protected only 11% of young mature females. However, because the MLS was considered to

be an important conservation issue by the scientic and shing communities, it was increased in most of the Lobster Fishery Areas (LFA) between 1987 and 1991. The most recent changes were put in place between 1998 and 2001 (Lanteigne et al., 1998) to increase the MLS to 67.5 mm LC in four of the ve LFA, which will protect 29% of young mature females. One LFA located off the west coast of Cape Breton has already increased the MLS to 70 mm LC since 1990, which protects 47% of young mature females. Based on our observations, to allow 50% of young mature females to be protected, the MLS should be set at a minimum of 70.5 mm LC. To permit more than 90% of young mature females to be protected from the shery, the MLS should be set at 79 mm LC. There is, however, an uncertainty concerning the quality of the eggs produced by young mature females. Attard and Hudon (1987) reported that eggs produced by large females in the GSL are larger, have a higher energy content, and hatch earlier than the ones produced by small females. Laboratory observations suggest that high yolk reserves will increase larval survival (Anger et al., 1985), and therefore, larvae from eggs produced by larger females could have an advantage. However, larvae from eggs that develop at a high temperature also have a high energy content (Sasaki et al., 1986). A detailed knowledge of the egg viability and, more importantly, larval ecology (survival in the natural environment) is required before assessing the real contribution of small mature females to the lobster population recruitment. Meanwhile, based on the precautionary approach (FAO, 1996), a restriction on the capture of large animals (maximum legal size) could be a good preventive conservation measure. Another important regulation of the lobster sheries in the sGSL is the protection of berried females (landing berried females is prohibited). In the sGSL, four of the ve LFA have a spring season (May 1 to June 30) prior to the annual molting and spawning (JulyAugust). With such timing, primiparous females with a one-year reproductive cycle, and multiparous females that spawn in successive years, which can represent up to 20% of the females, are fully protected from the shery. However, in one LFA (LFA 25: early August-early October), shermen can catch females with a oneyear reproductive cycle in early postmolt, but

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before they extrude their eggs (i.e., in the same year before they become primiparous females), and multiparous females that have the ability to spawn in successive years before they can release another clutch of eggs. Hence, a portion of the potential egg-producing females are caught and kept before they have the time to extrude their eggs and get legal protection. This situation specic for LFA 25 may require an adjustment to the present management regime. Recently, an egg-per-recruit model (E/R) designed for the United State sheries (Fogarty and Idoine, 1988) has been proposed to manage the Canadian lobster sheries (Anonymous, 1995). The E/R model focuses on the egg production based on parameters from a particular stock relative to the egg production of an unshed population, and a target of egg production for that stock could be set. Although the E/R model was adapted to the Canadian sheries, the uncertainties of some parameters created difculties in adequately assessing the status of each LFA to recommend a target (Lanteigne et al., 1998). Based on our observations, it would be imperative before setting a target for the sGSL lobster sheries to investigate the sensibility of the E/R model by incorporating the one- and two-year reproductive cycles with or without molting for small primiparous and multiparous females. ACKNOWLEDGEMENTS
The authors thank T. Brideau, B. Comeau, E. Landry, and the captain and crew of the C.S.S. Opilio for technical assistance in the eld and the laboratory and thank Dr. M. Mallet for her assistance and for constructively criticizing the statistical analysis. We also thank M. Lanteigne, Drs. J. M. Hanson and M. Moriyasu, and two anonymous reviews for thoughtful suggestions that improved the quality of this manuscript.

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