Growth and reproduction of the introduced crayfish Pacifastacus leniusculus in a British lowland river

Fisheries Research 42 (1999) 245±259

Growth and reproduction of the introduced cray®sh Pacifastacus leniusculus in a British lowland river Rui-Zhang Guana,*, Peter Roy Wilesb a

Aquaculture Department, Fisheries College, Jimei University, Xiamen, 361021 Fujian, China The Clore Laboratory for Life Sciences, The University of Buckingham, Buckingham MK18 1EG, UK

b

Received 14 October 1998; received in revised form 31 March 1999; accepted 18 April 1999

Abstract Signal cray®sh, Pacifastacus leniusculus (Dana), a native of North America, were introduced into the River Great Ouse, the major lowland river in mid- to eastern England in 1984. The present paper reports the growth and reproduction of a naturalised signal cray®sh population in the river. Cray®sh moulted between April and October. Males of individuals >55 mm carapace length (CL) and females of individual >45 mm CL moulted only once a year while younger ones moulted more than once. Mature males grew faster than mature females by a larger per moult increment (MI) and more frequent moult. For cray®sh >30 mm CL, the MI increased with CL and then decreased as cray®sh grew larger, while the percentage moult increment (PCMI), the annual moult increment (AMI), and the annual percentage moult increment (APCMI) decreased with increase in CL. The mean AMI of males (36±70 mm CL) ranged from 11.7 to 5.1 mm in CL, that of females (41±70 mm CL) 8.4 to 3.4 mm. Both males and females matured in their third year. The smallest ovigerous female was 36.3 mm CL. In 1994, the mean number of pleopodal eggs per ovigerous female sampled at the end of April was 158. A recruitment of 70 juveniles per m2 was estimated in the original pool of cray®sh introduction. # 1999 Elsevier Science B.V. All rights reserved. Keywords: Signal cray®sh; Pacifastacus leniusculus; Growth; Reproduction; England; River Ouse; Introduction of cray®sh

1. Introduction Growth and reproduction are two important characteristics expressing ®tness and adaptation of a species to its habitat. A good understanding of these is important in aquaculture and the ®shery management of a species in nature. A good ®shery can be expected from fast growth and successful reproduction. *Corresponding author. Tel.: +86-592-6180973; fax: +86-5926181476 E-mail address: [email protected] (R.-Z. Guan)

Signal cray®sh, Pacifastacus leniusculus (Dana), is a native of North America, introduced widely into British waters since 1976. Some have established breeding populations (Holdich and Lowery, 1988); the River Great Ouse, a major lowland river in mid- to eastern England, is one such water. The river used to be inhabited by the native white-clawed cray®sh, Austropotamobius pallipes (Lereboullet), but its last veri®ed sighting was in 1981 according to locals. The present P. leniusculus population has established since its introduction in 1984 with the release of 100 summerlings and 40 adults from a cray®sh farm in England at the river section in

0165-7836/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 5 - 7 8 3 6 ( 9 9 ) 0 0 0 4 4 - 2

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Thornborough, Buckinghamshire (Map Reference: OS 738355). The growth of cray®sh is usually estimated by per moult increase (MI), percentage per moult increase (PCMI) or mean carapace length of each year class. The growth of signal cray®sh has been studied in various waters worldwide, mainly in America (Flint, 1975b; Flint and Goldman, 1977; Goldman and Rundquist, 1977; Mason, 1978; McGriff, 1983; Westman and Savolainen, 1995) and European continent (Abrahamsson, 1971; Brinck, 1975; Kossakowski, 1988; Westman et al., 1993). Studies showed various growth rates of the species from the different environments. Little is known, however, about growth of introduced signal cray®sh in British waters, except in a small lake in southern England where it was reported to have an exceptionally fast growth in the ®rst four years following its introduction (Richards, 1983; Hogger, 1986). Information on the fecundity has been provided by a number of researchers (e.g., McGriff, 1983; Shimizu and Goldman, 1983; Lowery, 1988; SoÈderbaÈck, 1995). There is less information on the reproduction of P. leniusculus in British rivers. In the River Great Ouse, it is known that large number of mature cray®sh were trapped commercially in 1989, ®ve years after introduction. For these reasons the present study was

undertaken from 1992 to 1994. The results on the growth and reproduction of signal cray®sh in the river are presented in this paper. 2. Study site The River Great Ouse is a lowland river with its greatest altitude less than 135 m. It has a total length of approximately 240 km starting in Northamptonshire, running northeastwards through clay land into The Wash, where it enter the North Sea. During the study period (1992±1994), the mean annual water temperature was 10±128C, with higher temperatures (14± 228C) between April and October (Fig. 1). At the study site (Fig. 2), the catchment area was 389 km2, the annual rainfall was generally 500±600 mm, and the mean water ¯ow from 1980 to 1990 was 2.67 m3 sÿ1 (range 0.14±36.40 m3 sÿ1). The mean pH value and dissolved oxygen of the river water in 1993 were 8.08 and 8.94 mg lÿ1, respectively. Within the study site, macrophytes (mainly Phragmites spp.) were abundant along the most of the river banks and extended to the waterlogged area of some shallow sections with a mud bottom. The water moss (Fontinalis antipyretica Hedw.) was abundant on some

Fig. 1. Annual water temperature of the River Great Ouse at Thornborough (the NRA Cambridge Division Data).

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Fig. 2. Sampling sites and distribution of Pacifastacus leniusculus in the River Great Ouse. The river section within the dashed lines was occupied by the crayfish in the May of 1994. P1±P7: Pool 1±Pool 7; R1±R6: Riffle 1±Riffle 6; B1: Brook; P2: the original site of crayfish introduction. Map reference (Ordnance Survey): P1 (OS 719343), P2 (OS 735353), P3 (OS 735354), P4 (OS 736354), P5 (OS 740356), P6 (OS 752364), P7 (OS 727343), R1 (OS 697338), R2 (OS 725343), R3 (OS 738353), R4 (OS 752363), R5 (OS 762375), R6 (OS 774382).

river bed. In summer, the macroalga (Cladophora spp.) grew on the surfaces of stones in all rif¯es. Twelve species of ®sh were recorded during a ®sh survey, 1988±1994, with total ®sh biomass ranging from 42 to 47 g mÿ2. Pike (Esox lucius (L.)) was the absolute dominant by biomass while roach (Rutilus rutilus L.) was always dominant in number (data provided by the NRA Anglian Region, England). 3. Materials and methods 3.1. Growth The growth of cray®sh was estimated by two methods, capture-mark-recapture (CMR) method and Bhattacharya (1967) method. Cray®sh samplings were conducted bimonthly both in the pool P2 and the rif¯e R3 (about 300 m downstream from P2) (Fig. 2) from October 1992 to April 1994 (December 1992 was missed due to ¯ooding). In P2 cray®sh were sampled with cylindrical, plastic cray®sh traps (50 cm long and 20 cm in diameter). Traps, including the inverted entry

cones at both ends, were covered with polyethylene nets of 44 mm2 mesh to prevent the small cray®sh entered from escaping. Traps, baited with ®sh heads, were put into the river and anchored at intervals of 45 m in eight locations along the bank. Traps were set in the late afternoon and emptied early the following morning. In R3, a modi®ed large Surber sampler (505015 cm3) and directly hand capture were used for collecting cray®sh. The front and both sides of the sampler were enclosed with nets, the back was connected with a 1.2 m long net bag (net mesh 44 mm2), and the frame was made of iron. Additional samples were taken in May 1994 in R3 (for observing the ®rst moult of the year as no newly moulted soft-shelled cray®sh was observed in April) and in November 1994 in both P2 and R3 to provide the winter data of cray®sh length frequency for 1994. During the sampling, the carapace length (CL, from the rostral apex to the posterior median edge of the cephalothorax) and total body length (TL, from the rostral apex to the posterior median edge of the telson) of cray®sh were measured to the nearest 0.1 mm with callipers, and the wet weight (WW) to the nearest

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0.1 g. The relationship between the WW and CL of cray®sh with normal chelipeds was estimated by arithmetic and logarithmic plots and a simple linear regression analysis. The ®rst moult of the year was determined by the observation on the ®rst appearance of newly moulted soft-shelled cray®sh of different sexes and sizes in the samples from both P2 and R3. In P2, cray®sh were trapped and marked by a modi®ed marking method (clipping pleurons and punching holes in the telson and uropods) developed by Guan (1997). The data of recaptured marked cray®sh between October 1992 and November 1994 was used for CMR method to estimate the MI, PCMI, annual moult increment (AMI), annual percentage moult increment (APCMI) and annual instantaneous growth rates of CL (gl) and wet weight (WW) (gw). The following equations were used to calculate the MI and PCMI of cray®sh CL from the recaptured marked cray®sh which had one moult indicated by an increase of 2.0±6.5 mm in CL (any increase >5 mm in CL from the cray®sh recaptured more than two months after the mark-release was omitted as it may consist of more than one moult). MI ˆ CL1 ÿ CL0 ; PCMI ˆ ……CL1 ÿ CL0 †=CL0 †  100; where CL0 and CL1 were the CL of cray®sh before (at ®rst capture) and after (at recapture) a moult, respectively. The AMI and APCMI of cray®sh CL for each size class were estimated from the recaptured marked cray®sh in P2 that spent approximately one year or a whole growing season (April±October) in the river after marking. Those cray®sh were sorted into size classes at 5 mm CL intervals and mean AMI and APCMI of each size class were estimated from the difference in CL between ®rst capture and recapture, similar to the calculations of MI and PCMI. The gl and gw for each size class were estimated using equations: gl ˆ ln…CLb =CLa †; gw ˆ ln…Wb =Wa †; where CLa was midlength of a size class, and CLb was CLa ‡ mean AMI of the size class CLa; Wa and Wb were the wet weights, corresponding to CLa and CLb, respectively, calculated from the estimated equation describing the relationship of WW and CL.

The annual winter data of cray®sh length frequency from both P2 and R3 during 1992 and 1994 were used to estimate the number of cray®sh cohorts (age classes) and the mean CL of each age class by Bhattacharya's method, using the modal class progression analysis (MPA) in the Compleat ELEFAN (electronic length frequency analysis for ®sh and aquatic invertebrates) computer program (version 1.10). Then, the AMI and APCMI, and the annual instantaneous growth rates of CL (Gl) and WW (Gw) were estimated. Since cray®sh do not moult during October and March and in order to increase the sample size, the winter data of cray®sh length frequency for 1992 were pooled from the October sample in 1992 to the February samples in 1993 and those for 1993 were pooled from the October samples in 1993 to the February samples in 1994, while those for 1994 were only from November samples in 1994. The AMI and APCMI of each age class were estimated by the difference between the mean CL of age class i and age class i‡1 (in the next year) estimated by Bhattacharya's method from the consecutive three years data (1992±1994). Then, the Gl and Gw for each age class were estimated using equations: Gl ˆ ln…CLi‡1 =CLi †; Gw ˆ ln…Wi‡1 =Wi †; where CLi and CLi‡1 were the mean CL of each age class at year i and year i‡1, respectively, and Wi and Wi‡1 were the mean WW of each age class at year i and year i‡1, calculated from the estimated equation describing the relationship of WW and CL. The AMI of each age class was calculated from the difference in the mean CL of a age class between year i and year i‡1. 3.2. Reproduction Periods of spawning and egg hatching were observed in laboratory by keeping about 200 adults cray®sh outdoor (in tanks) and in the river by weekly checking in rif¯es and trapping in pools between May and October. The number of pleopodal eggs of 90 ovigerous cray®sh collected at the end of April 1994 from the river was directly counted. The number of recruits (R) of young-of-the-year (YOY) cray®sh per m2 for P2 in 1994 were estimated

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using equation: R ˆ DPrE; where D was the annual mean density of females in P2, which equalled to half the total density, assuming equal numbers of sexes, P the proportion of adult females to total females, r the ratio of ovigerous females and total adult females (>39 mm CL), and E was the mean number of pleopodal eggs per ovigerous female estimated at the end of April, assuming all these eggs hatched. The P, r, and E were all calculated from the April samples in P2 and were used to represent those in the population. All data in the present study were analysed by analysis of variance (ANOVA) unless otherwise indicated. 4. Results 4.1. Morphology, moulting and growth The CL of signal cray®sh was approximately half the TL. The CL : TL was 1 : 1.9988 for males of 23.4± 74.8 mm CL (n ˆ 479) and 1 : 2.1262 for females of 23.6±75.3 mm CL (n ˆ 675). Females had a longer abdomen than males of the same TL. The relationship between WW and CL of cray®sh with normal chelipeds was estimated separately for both sexes and size as the ratios of CL and TL are different between sexes and for juveniles and adults due to the allometric growth. The separation of juveniles and adults (mature cray®sh) was determined at 39 mm CL as a majority of ovigerous females was >39 mm CL and it was assumed that mature males were the same size. The exponential relationship (plot log WW against log CL and ®t by a straight line) was the best description of the relationship (correlation coef®cient, R ˆ 0.99±1.00) (p < 0.001, t-test on the correlation coef®cient, R) (Lee and Lee, 1982) between WW and CL of cray®sh (Fig. 3(a) and (b)) compared to simple linear regression and semi-logarithmic plot relationships, which gave lower correlation coef®cients. There was no signi®cant difference (p > 0.05, Fig. 3(a) in the relationship of WW and CL of juveniles between males and females but a signi®cant difference (p < 0.01, Fig. 3(b)) in that of adults between males and females.

Fig. 3. The relationship between WW and CL of crayfish from the River Great Ouse. The pre-mature and mature crayfish (>39 mm CL) were estimated separately. (a) 39 mm CL; (b) >39 mm CL.

The cray®sh in R3 started their ®rst moult of the year in the mid April of 1993 but in the early May of 1994. Males in P2 started their ®rst moult between 23rd of April and 23rd of June (Fig. 4) and some of those <55 mm CL moulted again at least once in the same year, but those >55 mm CL did not moult again (Fig. 5); juvenile and non-ovigerous females started the ®rst moult in the same period as males (Fig. 4) but ovigerous females took their ®rst moult of the year between 23rd of June and 18th of August after the release of their offsprings; females >45 mm CL moulted only once a year while the younger ones moulted once or more (Fig. 5). In P2, 8274 cray®sh were sampled, of which, 7619 were marked and 1186 were consequently recaptured. The MI, PCMI, AMI, and APCMI of both male and female estimated from recaptured moulted cray®sh

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decreased with increase in CL (Tables 1 and 2). The mature males grew much faster than mature females, by not only larger MIs (Table 2) but also more frequent moulting (Fig. 5). The mean CL and WW of each age class of cray®sh in three consecutive years, estimated by Bhattacharya's method, were shown in Tables 3 and 4 and Figs. 6 and 7. The annual growth rate of CL at each age class in 1994 was signi®cantly (p < 0.05, paired data comparison on the growth rates of cray®sh of 0‡ to 3‡ between 1993 and 1994) (Ryan et al., 1985) slower than that in 1993, 22% less in both CL and WW for males and 25% in CL and 21% in WW for females. The AMI of each age class, from October 1992 to October 1993, calculated by the mean CL of cohorts estimated from the CL frequency distribution using the Bhattacharya's method, was much higher than that estimated by the mark-recapture method even when the latter was adjusted to accommodate the effects of marking (Guan, 1997) (Fig. 8). 4.2. Reproduction

Fig. 4. Moulting periods of crayfish >30 mm CL in the River Great Ouse.

were binomially correlated (p < 0.05, t-test on the correlation coef®cient, R) with their initial CL. The MI increased with CL and then decreased as cray®sh grew larger, while the PCMI, AMI, and APCMI

According to the observations in the laboratory, the mating activity of signal cray®sh kept in tanks outdoors started in September when the water temperature dropped to 13±148C and lasted until November. The polygyny type of sexual relations were observed. Spawning occurred within one week, usually 2±3 d, after mating. In the river, eggs hatched between early May and the beginning of July. Both males and females matured in their third year, according to observations on the smallest males and females

Table 1 Mean per MI and PCMI of Pacifastacus leniusculus of different size classes from the River Great Ouse estimated from marked recaptures (CL: carapace length; n: number of crayfish;  standard deviation) CL (mm)

31±35 36±40 41±45 46±50 51±55 56±60 61±65 66±70

Male

Female

n

MI (mm)

PCMI

n

MI (mm)

PCMI (%)

1 7 47 63 69 78 29 9

3.8 4.8  0.9 4.1  1.0 4.4  1.1 5.2  1.3 5.1  0.8 5.3  1.0 5.5  0.8

10.9 12.4  2.3 9.5  2.6 9.2  2.3 9.9  2.4 8.9  1.5 8.5  1.5 8.1  1.1

2 5 26 51 34 20 2 ±

4.1 3.4  0.6 3.6  0.8 3.8  0.8 3.7  1.2 3.4  0.8 4.2 ±

11.7 8.8  1.7 8.5  1.9 8.1  1.7 7.2  2.4 6.0  1.4 6.8 ±

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Fig. 5. Number of annual moults of crayfish of different CL in the River Great Ouse.

(38 mm CL) seen mating and/or spawning in the laboratory and the smallest size (36.3 mm CL) of ovigerous females from the river (CL size corresponding to age, see Table 4 and Fig. 7).

That the smallest female spawning in the laboratory was 38 mm CL, while all females >42 mm CL, whether mated or not, spawned. The unmated females carried their unfertilised eggs for up to three months.

Table 2 Mean AMI and APCMI of Pacifastacus leniusculus of different size classes from the River Great Ouse estimated from marked recaptures (CL: carapace length; n: number of crayfish;  standard deviation) CL (mm)

36±40 41±45 46±50 51±55 56±60 61±65 >65

Male

Female

n

AMI (mm)

APCMI (%)

n

AMI (mm)

APCMI (%)

17 31 19 29 26 5 2

11.7  2.9 9.3  2.4 7.3  3.1 7.2  2.9 5.3  1.0 5.1  0.9 5.3

30.6  7.5 21.9  5.7 15.2  6.5 13.6  5.7 9.3  1.7 8.5  1.6 7.9

± 10 20 20 17 3 1

± 8.4  3.4 3.5  0.6 3.4  0.8 3.4  0.9 4.2  0.4 4.1

± 19.8  8.1 7.3  1.2 6.4  1.5 6.0  1.6 6.8  0.6 6.0

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Table 3 Mean CL (standard deviation) of cohorts estimated by Bhattacharya's method based on the CL frequency distribution, and annual instantaneous growth rates of CL of Pacifastacus leniusculus in the River Great Ouse (0‡, 1‡, . . ., and 6‡ correspond to year 1, year 2, . . ., and year 7, respectively. Gl is the growth rate of each cohort during two consecutive years, e.g., 0.72 is the growth rate of CL from male 0‡ in 1992 to male 1‡ in 1993, and 0.70 is the growth rate of CL from male 0‡ in 1993 to male 1‡ in 1994, and so on) Sex

1992

Gl

Age

CL (mm)

Male

± ± 0‡ 1‡ 2‡ 3‡ 4‡ 5‡ 6‡

± ± 16.6  1.8 31.2  5.4 41.6  4.4 52.0  2.4 57.8  3.0 64.2  1.6 69.2  1.3

Female

± ± 0‡ 1‡ 2‡ 3‡

± ± 15.4  2.6 28.5  3.9 39.7  3.3 49.8  3.7

1993

Gl

Age

CL (mm)

± ± 0.72 0.42 0.29 0.19 0.18 ± ±

± 0‡ 1‡ 2‡ 3‡ 4‡ 5‡ ± ±

± 14.0  1.9 34.0  4.6 47.3  3.6 55.6  3.6 62.8  2.3 69.0  1.9 ± ±

± ± 0.77 0.42 0.21 0.12

± 0‡ 1‡ 2‡ 3‡ 4‡

± 14.3  2.0 33.3  5.5 43.2  2.4 49.0  2.2 56.4  3.1

The smallest ovigerous female recorded from the river was 38.5 mm CL in 1992, 39 mm CL in 1993 and 36.3 mm CL in 1994 with a majority of more than 99% ovigerous females >39 mm CL.

1994 Age

CL (mm)

± 0.70 0.29 0.15 0.13 ± ± ± ±

0‡ 1‡ 2‡ 3‡ 4‡ ± ± ± ±

15.6  1.8 28.3  4.2 45.4  4.7 55.1  2.6 63.5  4.4 ± ± ± ±

± 0.72 0.23 0.13 0.12 0.09

0‡ 1‡ 2‡ 3‡ 4‡ 5‡

15.1  2.3 29.5  3.1 41.9  3.5 49.1  2.6 55.1  3.0 61.7  2.1

More mature females carried eggs and fewer of these ovigerous females partly lost their eggs in 1993 than in 1994. This was shown by 28% (55 in 198) of mature females (>39 mm CL) in the February sample

Table 4 Mean WW of cohorts converted from mean CL in Table 3 and annual instantaneous growth rates of wet weight (Gw) of Pacifastacus leniusculus in the River Great Ouse (0‡, 1‡, . . ., and 6‡ correspond to year 1, year 2, . . ., and year 7, respectively. Gw is the growth rate of the WW of each cohort during two consecutive years, e.g., 2.19 is the growth rate of WW from male 0‡ in 1992 to male 1‡ in 1993, and 0.75 is the growth rate of WW from male 0‡ in 1993 to male 1‡ in 1994, and so on) Sex

1992 Age

Gw WW (g)

1993 Age

Gw WW (g)

1994 Age

WW (g)

Male

± ± 0‡ 1‡ 2‡ 3‡ 4‡ 5‡ 6‡

± ± 1.3 8.6 20.4 42.8 60.9 86.4 110.9

± ± 2.19 1.29 0.97 0.63 0.59 ± ±

± 0‡ 1‡ 2‡ 3‡ 4‡ 5‡ ± ±

± 0.8 11.2 31.2 53.6 80.3 109.8 ± ±

± 0.75 0.89 0.51 0.44 ± ± ± ±

0‡ 1‡ 2‡ 3‡ 4‡ ± ± ± ±

1.0 6.4 27.3 51.9 83.3 ± ± ± ±

Female

± ± 0‡ 1‡ 2‡ 3‡

± ± 1.0 6.6 17.4 35.4

± ± 2.32 1.24 0.74 0.39

± 0‡ 1‡ 2‡ 3‡ 4‡

± 0.8 10.5 22.7 36.6 52.2

± 2.17 0.67 0.40 0.28 0.28

0‡ 1‡ 2‡ 3‡ 4‡ 5‡

1.0 7.3 20.6 33.9 48.6 69.2

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Fig. 6. Cohorts of male crayfish, Pacifastacus leniusculus, from the River Great Ouse, estimated by Bhattacharya's method based on the CL frequency distribution data. The separation index was >2 for all cohorts and the expected distributions of cohorts were not significantly different (2-test, degrees of freedom 10) from the observed ones at 95% level of confidence. Dotted lines connected the mean CL of the cohort in three consecutive years.

and 59% (101 in 172) in the April samples in 1993 carrying eggs while only 21% (13 in 61) in the February sample and 48.1% (90 in 187) in the April sample in 1994 carrying eggs, and by 22% of ovigerous females being partly lost their eggs in the April sample of 1993 while 34% in the April sample of 1994. Almost all larger females (>60 mm CL) partly lost their eggs. The average number of eggs carried per female (n ˆ 90), including the ones that partly lost their eggs, at the end of April 1994 was 158  104 (standard deviation), and the estimated number of ovigerous females was 0.44 mÿ2 (ˆannual mean density of cray®sh (2.2 mÿ2) divided by two (assuming half were females), then, times the proportion of ovigerous females to total female in the April sample (40%)) (see Guan, 1995), therefore, the recruitment of juvenile in 1994 was about 70 mÿ2 (ˆ0.44158, assuming all eggs hatched).

5. Discussion 5.1. The comparison and estimation of growth The earlier moult of cray®sh in R3 in 1993 was apparently related to the water temperature which rose earlier and was higher in the spring of 1993 than in the spring of 1994 (Fig. 1). The higher AMI of each age class calculated by the mean CL of cohorts estimated from the CL frequency distribution than that estimated by the CMR method (Fig. 8) suggests that marking may also affect the number of moults in a year. It was shown clearly that the growth of P. leniusculus was faster than that of the native cray®sh, A. pallipes, which used to inhabit the River Great Ouse (Pratten, 1980). The growth of P. leniusculus (nine years after introduction) in the river was also faster than those from much older populations (>30 years

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Fig. 7. Cohorts of female crayfish, Pacifastacus leniusculus, from the River Great Ouse, estimated by Bhattacharya's method based on the CL frequency distribution data. The separation index was >2 for all cohorts and the expected distributions of cohorts were not significantly different (2-test, degrees of freedom 10) from the observed ones at 95% level of confidence. Dotted lines connected the mean CL of the cohort in three consecutive years.

after introduction) in American lakes and rivers (Flint, 1975b; Flint and Goldman, 1977; Goldman and Rundquist, 1977; Shimizu and Goldman, 1983), and was similar to that from the older population (17±20 years after introduction) in Lake Slickolampi in southern Finland (Westman et al., 1993) but slower than those from younger population (<5 years after introduction) in a lake at Strat®eld Saye in southern England (Hogger, 1986) and in Swedish waters (Abrahamsson, 1973; Brinck, 1975). The faster growth of P. leniusculus together with its larger size, greater aggression, higher reproductivity (Lowery, 1988) and resistance to cray®sh plague Aphanomyces astacti Schikora (Unestam and Soderhall, 1977; Persson and Soderhall, 1983; Alderman, 1993) suggest that it could support a good cray®sh ®shery in British freshwater. Many factors in¯uence growth including density, temperature, and food availability. The density-depen-

dent growth of cray®sh in enclosed water systems is commonly observed (Avault et al., 1975), and several stunted cray®sh populations from lakes or ponds have been reported (SvaÈrdson, 1949; Abrahamsson, 1966; Flint, 1975b; Huner and Lindqvist, 1986). The density-dependent growth of cray®sh in these enclosed water systems may be easily explained by the limited resources, such as food and space. However, it could be also signi®cant in relatively open water systems like rivers because a high density could built up due to the burrowing and homing behaviour. For example, in the River Great Ouse, cray®sh occupied only a limited part of the river and was still expanding into new areas, they dug extensive borrows in the mud banks and lived at a high density (Guan, 1994; Guan and Wiles, 1997). They often stayed near and returned to their burrows. The consequence of this behaviour may be a stunted cray®sh population when the density reaches a max-

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Fig. 8. Comparison of AMI of crayfish in the River Great Ouse estimated from the mark-recapture data (MR) (adjusted to accommodate the effects of marking, see Guan, 1997) and CL frequency distribution (CL-FD) data.

imum. Therefore, growth may be rapid when cray®sh ®rst inhabit new habitats with rich resources, but slows down when density increases and resources may be limiting. An exceptionally high growth was reported for the cray®sh in the ®rst two years after introduction to a lake in southern England (Richards, 1983; Hogger, 1986) while a slow growth occurred in the old population in Lake Tahoe (introduced in 1895) (Flint, 1975a), in which the mean CL of the new hatchlings and largest captured cray®sh were only 3.25 and 57.0 mm, respectively, compared to 4.54 and 78.0 mm in the present study. The growth estimated from those newly introduced cray®sh, or a young population with an extreme low density, should be treated cautiously to avoid leading to any misunderstanding of the general growth of a stable population in nature. The annual water temperatures may be an important factor affecting the growth of cray®sh. France (1985) reported that the higher temperatures and longer growing season during 1980 increased growth by an

average of 12% over that of the preceding year. However, water temperature in this study appeared not to be the main factor, as the accumulated annual water temperature of 1993 (4080 day degrees) was similar to that of 1994 (4050 day degrees) (Fig. 1). Therefore, the slower growth and smaller mature size of cray®sh in P2 in 1994 than 1993 may be more likely due to other factors, e.g., the increase in the cray®sh density, and the removal of the 229 largest cray®sh (>55 mm CL; about 5% of total population) in October 1992 for laboratory burrowing experiments. The latter might promote the growth of young age classes in 1993, as large cray®sh may affect the growth of young age classes through the mechanism of possible intimidation and out-competition for food and space. The present study provided detailed estimates on the growth of signal cray®sh in nature, not only the MI, but also the AMI and the number of moults in a year for different sizes, ages and sexes of cray®sh. The estimations of MI and PCMI only re¯ect part of the growth pattern while the estimations of AMI and

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APCMI are better descriptions of the growth of cray®sh (Guan and Wiles, 1996). The AMI of size classes estimated from the marked recaptures in this study was very laborious while the AMI of age classes were easier estimated based on the length frequency distribution using Bhattacharya's method, which has been considered to be useful for estimating cray®sh cohorts and hence their mean lengths and growth rates (Hogger, 1986; Guan and Wiles, 1996). The higher AMI estimated by Bhattacharya's method than that from marked recaptures may be because marking affects the annual number of moults of the marked cray®sh, or the inaccuracy estimations of cohorts by Bhattacharya's methods. However, the latter is less likely, since young cohorts CL distribution did not overlap (Figs. 7 and 8) and could be used to compare the growth rates between years. Hence, Bhattacharya's method could give more accurate estimates of AMI than the mark-recapture method. However, for an old population consisting of old cohorts which may heavily overlap in the CL frequency distribution, the correspondence of the separated size groups to cohorts needs to be veri®ed with other information, such as the MI, moult number of a year, and AMI of each size class which were used to help in positioning the cohorts in this study. Computer programmes for Bhattacharya's method enable the quick identi®cations of cohorts, hence the estimation of growth. The ®rst two cohorts were easy to identify as there was little or no overlap in the CL frequency distributions. This is very useful information for comparing the growth of cray®sh from different populations and for positioning the older cohorts. The experience gained from this study suggests that it is important that the sample for analysis should be of suf®cient size to obtain a representative length frequency distribution of all cohorts. This point should be taken into considerations at the stage of collection and compilation of data. From personal experience a total some 500 individuals for each sex would be suf®cient. 5.2. Maturation size and reproductivity The season and activity of the reproduction of P. leniusculus in the River Great Ouse were similar to those of the same species in other waters (Mason, 1970; Abrahamsson, 1971; Flint, 1975a) and also similar to that of native species A. pallipes (Pratten,

1980; Rhodes, 1981; Thomas, 1991). The polygyny type of sexual relations in P. leniusculus observed in this study is in agreement with the observations by Doroshenko (1988). P. leniusculus in the River Great Ouse matured at age 3 similar to those in Castle Lake, California (Elser et al., 1994). The various ages at maturity of this species have been reported by many researchers and summarised by McGriff (1983). The difference on the age at maturity from various waters could be attribute to the different growth rates but may also be due to the error of ageing. Cray®sh of the same age could have very different sizes because of different growth rates. In the present study, for example, the smallest ovigerous female in 1993 was 39.0 mm CL compared to 36.3 mm CL in 1994 during which cray®sh grew slower, but they were the same age class (age 3, Table 3 and Fig. 7). Further comparisons of the present data with other data support this hypothesis, the smallest ovigerous female was larger in Swedish ponds (40 mm CL) where cray®sh grew faster (Abrahamsson, 1971), and was similar in Finish lakes (39 mm CL) where cray®sh grew similarly fast (Westman et al., 1993), but was smaller in Lake Tahoe (27 mm CL) (Flint, 1975a) where cray®sh grew slower, though females were all reported to be mature at age 3. Therefore, the maturation size of cray®sh from different waters could be a useful index of growth rate because the maturation depends more on age than on size. The number of pleopodal eggs among cray®sh of various species has been widely studied (Momot, 1984). For P. leniusculus, the mean number of pleopodal eggs per female over several waters ranged from 120 to 466 (Miller, 1960; Abrahamsson, 1971; Flint, 1975a; Mason, 1975; Shimizu and Goldman, 1983; Savolainen et al., 1996; the present study). However, it is unreasonable to compare the reproductivity of cray®sh by those estimated number of pleopodal eggs because they were measured at various cray®sh size ranges and at different times, e.g., the number measured at the end of April in the present study would be considerably lower than that if measured in November (few berried cray®sh could be trapped in this early egg hatching period) or from the females kept in culture because some eggs would lost during hatching, especially in nature (Mason, 1977; Shimizu and Goldman, 1983).

R.-Z. Guan, P.R. Wiles / Fisheries Research 42 (1999) 245±259

The pleopodal eggs estimated at the end of April in this study showed that a high percentage (22±34%) of ovigerous females partly lost their eggs. The percentage of egg loss was not estimated in the present study but in Astacus the number of pleopodal eggs was observed to be 30±55% lower than the number of ovarian eggs (Lahti and Lindqvist, 1983; Cukerzis, 1988; Skurdal et al., 1993; Savolainen et al., 1996). A 44.0±69.8% egg loss was also estimated from potential reproduction (ova in ovary) to actual production (early stage III larva) for nine Orconectes propinquus (Girard) populations in Ontario rivers in Canada (Corey, 1987). Corey (1987) considered that current velocity, increased volume of larval stages and parasitism accounted for the greatest losses. He stated that the loss of eggs while being carried on the abdomen was caused by such factors as predation by brooding females and other cray®sh, and also by abrasion and water currents. For P. leniusculus in this study, the increasing aggressive encounters of cray®sh due to the increased density were probably one of the main factors causing egg losses, e.g., 22% ovigerous females measured in April 1993 (mean density ˆ 0.8 mÿ2 in 1992) (Guan and Wiles,1996)partlylosteggswhile34% measured in April 1994 (mean density ˆ 2.2 mÿ2 in 1993) (Guan, 1995). There could be several factors actingtogetherresultinginthe eggloss,suchaspredators which could mainly be pikes (in this case), burrowing behaviour (Guan, 1994), and environmental shelters. The reproduction ef®ciency or fecundity of P. leniusculus is often indicated by the number of pleopodal eggs per female as indicator (Miller, 1960; Abrahamsson, 1971; Flint, 1975b; Mason, 1975; Shimizu and Goldman, 1983). However, two important features have been often ignored. One is the proportion of mature females that produce eggs, which may be approximately measured by the proportions of adult females carrying eggs in early hatching season, but these berried females may carry unfertilised eggs as shown in aquaria where some females did not mate but did spawn, and eggs would lost totally later; the other is the proportion of mature females actually carrying their eggs until hatching time as many females may, either totally or partly, miscarry their eggs. The latter provides a better representation of the actual reproductivity or recruitment of the population. The proportion of adults involved in reproductive activity, the number of eggs produced and the size at

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maturity are very important reproductive strategies for ®sh populations in response to a variable environments (Wootton, 1984). This may be the same for cray®sh, that is, when the environment becomes less favourable, fewer adults are reproductively active, fewer eggs were produced, and the growth decreases, hence the size at maturity decreases (Momot, 1967; Momot et al., 1978). To estimate the proportions of mature females that produce eggs and that actually carry eggs until hatching time was dif®cult as ovigerous females were too inactive to be trapped. Therefore, the proportions in samples may not adequately represent those in the population, because a higher proportion of nonovigerous mature females may be trapped. However, if assuming such trap selectivity keeps constant in samples from the same seasons of two years, the proportions of females that carried eggs in samples could be used for a comparison of the difference in the reproductivity between two years. In the present study, the results revealed fewer mature females carrying eggs in the samples of 1994 (21% in February, 48% in April) than in those of 1993 (28% in February, 59% in April) from P2. Also more ovigerous females in the April sample of 1994 (34%) partly lost their eggs than in the April sample of 1993 (22%). Such reductions in the abilities of reproductivity and egg carrying of females could re¯ect the less favourable environmental conditions of 1994 compared to 1993. The increased cray®sh density may be one of the main factors deteriorating the living conditions for cray®sh, and hence, may result in decreased growth and decreased fecundity. Acknowledgements Our grateful thanks go to Dr. D. Holdich, and Prof. A.J. Brook for their invaluable help in many ways; Mr. R. Buckley for his help in the sampling; Mr. and Mrs. Atherton, Mr. and Mrs. Moore and Mr. and Mrs. Gurney for cray®sh rights to the River Great Ouse.

References Abrahamsson, S.A.A., 1966. Dynamics of an isolated population of the crayfish Astacus astacus Linne. Oikos 17, 96±107.

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Abrahamsson, S.A.A., 1971. Density, growth and reproduction in populations of Astacus astacus and Pacifastacus leniusculus in an isolated pond. Oikos 22, 373±380. Abrahamsson, S.A.A., 1973. The crayfish, Astacus astacus in Sweden and the introduction of the American crayfish Pacifastacus leniusculus. Freshwater Crayfish 1, 29±40. Alderman, D.J., 1993. Crayfish plague in Britain, the first twelve years. Freshwater Crayfish 9, 266±272. Avault Jr., J.W., de la Bretonne, L.W., Huner, J.V., 1975. Two major problems in culturing crayfish in ponds: oxygen depletion and overcrowding. Freshwater Crayfish 2, 139±144. Bhattacharya, C.G., 1967. A simple method of resolution of a distribution into Gaussian components. Biometrics 23, 115± 135. Brinck, P., 1975. Crayfish in Sweden. Freshwater Crayfish 2, 77± 85. Corey, S., 1987. Intraspecific differences in reproductive potential, realised reproduction and actual production in the crayfish Orconectes propinquus (Girard 1852) in Ontario. Am. Midland Naturalist 118, 424±432. Cukerzis, J.M., 1988. Astacus astacus in Europe. In: Holdich, D.M., Lowery, R.S. (Eds.), Freshwater Crayfish. Croom Helm., London, pp. 742±775. Doroshenko, J., 1988. Socioethological aspects of sexual behaviour of the signal crayfish Pacifastacus leniusculus Dana introduced in the Lithuanian SSR. Freshwater Crayfish 7, 351±356. Elser, J.J., Junge, C., Goldman, C.R., 1994. Population structure and ecological effects of the crayfish Pacifastacus leniusculus in Castle Lake, California. Great Basin Naturalist 54, 162±169. Flint, R.W., 1975a. The Natural History, Ecology and Production of the Crayfish, Pacifastacus leniusculus, in a subalpine Lacustrine environment. Ph.D. Dissertation, University of California Press, Davis. Flint, R.W., 1975b. Growth in a population of the crayfish Pacifastacus leniusculus from a subalpine lacustrine environment. J. Fish. Res. Board Can. 32, 2433±2440. Flint, R.W., Goldman, C.R., 1977. Crayfish growth in Lake Tahoe: Effects of habitat variation. J. Fish. Res. Board Can. 34, 155± 159. France, R.L., 1985. Relationship of crayfish (Orconectes virilis) growth to population abundance and system productivity in small oligotrophic lake. Can. J. Fish. Aquat. Sci. 42, 1096± 1102. Goldman, C.R., Rundquist, J.C., 1977. A comparative ecological study of the California crayfish P. leniusculus (Dana) from two subalpine lakes. Freshwater Crayfish 3, 51±80. Guan, R.Z., 1994. Burrowing behaviour of signal crayfish, Pacifastacus leniusculus (Dana), in the River Great Ouse, England. Freshwater Forum 4, 155±168. Guan, R.Z., 1995. Ecological Studies on the Crayfish Pacifastacus leniusculus (Dana). Ph.D. Thesis, The University of Buckingham. Guan, R.Z., 1997. An improved marking method for crayfish. Crustaceana 70(6), 641±652. Guan, R.Z., Wiles, P.R., 1996. Growth, density and biomass of crayfish, Pacifastacus leniusculus, in a British lowland river. Living Aquat. Resources 9, 587±596.

Guan, R.Z., Wiles, P.R., 1997. Home range of the crayfish, Pacifastacus leniusculus in a British lowland river. Freshwater Forum 8, 45±54. Hogger, J.B., 1986. Aspects of the introduction of signal crayfish, Pacifastacus leniusculus (Dana), into the southern United Kingdom. 1. Growth and survival. Aquaculture 58, 27±44. Holdich, D.M., Lowery, R.S., 1988. Crayfish ± an introduction. In: Holdich, D.M., Lowery, R.S. (Eds.), Freshwater Crayfish: Biology, Management and Exploitation. Croom Helm., London, pp. 1±7. Huner, J.V., Lindqvist, O.V., 1986. A stunted crayfish Astacus astacus population in central Finland. Freshwater Crayfish 6, 156±164. Kossakowski, J., 1988. Some remarks on the biology of the crayfish Pacifastacus leniusculus. Freshwater Crayfish 7, 369±376. Lahti, E., Lindqvist, O.V., 1983. On the reproductive cycle of the crayfish Astacus astacus L. in Finland. Freshwater Crayfish 5, 18±26. Lee, J.D., Lee, T.D., 1982. Statistics and Numerical in BASIC for Biologists. Van Nostrand Reinhold, Wokingham, UK. Lowery, R.S., 1988. Growth, moulting and reproduction. In: Holdich, D.M., Lowery, R.S. (Eds.), Freshwater Crayfish: Biology, Management and Exploitation. Croom Helm., London, pp. 83±113. Mason, J.C., 1970. Egg-laying in the western north American crayfish Pacifastacus trowbridgii (Stimpson) (Decapoda, Astacidae). Crustaceana 19, 37±44. Mason, J.C., 1975. Crayfish production in a small woodland stream. Freshwater Crayfish 2, 449±479. Mason, J.C., 1977. Reproductive efficiency of Pacifastacus leniusculus (Dana) in culture. Freshwater Crayfish 4, 83±92. Mason, J.C., 1978. Effects of temperature, photoperiod, substrate, and shelter on survival, growth, and biomass. Freshwater Crayfish 4, 73±82. McGriff, D., 1983. Growth, maturity, and fecundity of the crayfish, Pacifastacus leniusculus, from the Sacramento-San Joaquin delta. California Fish and Game 69, 227±242. Miller, R.S., 1960. Pattern and process in competition. Adv. Ecol. Res. 4, 1±74. Momot, W.T., 1967. Population dynamics and productivity of the crayfish, Orconectes virilis, in a Marl lake. Am. Midland Naturalist 78, 55±81. Momot, M.T., 1984. The crayfish production: a reflection of community energetics. J. Crustacean Biol. 4, 35±54. Momot, W.T., Gowing, H., Jones, P.D., 1978. The dynamics of crayfish and their role in ecosystems. Am. Midland Naturalist 99, 10±35. Persson, M., Soderhall, K., 1983. Pacifastacus leniusculus Dana and its resistance to parasitic fungus Aphanomyces astact Schikora. Freshwater Crayfish 5, 292±298. Pratten, D.J., 1980. Growth in the crayfish Austropotamobius pallipes (Crustacea: Astacidae). Freshwater Biol. 10, 401± 412. Rhodes, C.P., 1981. Artificial incubation of the eggs of the crayfish Austropotamobius pallipes (Lereboullet). Aquaculture 25, 129± 140.

R.-Z. Guan, P.R. Wiles / Fisheries Research 42 (1999) 245±259 Richards, K.J., 1983. The introduction of the signal crayfish into the United Kingdom and its development as a farm crop. Freshwater Crayfish 5, 557±563. Ryan, B.F., Joiner, B.L., Ryan, T.A., Jr., 1985. Minitab Handbook, 2nd ed. Pes-kent Publishing Company. Savolainen, R., Westman, K., Pursiainen, M., 1996. Fecundity of Finnish noble crayfish, Astacus astacus L., and signal crayfish, Pacifastacus leniusculus, in various natural habitats and in culture. Freshwater Crayfish 11, 319±338. Shimizu, S.J., Goldman, C.R., 1983. Pacifastacus leniusculus (Dana) production in the Sacramento River. Freshwater Crayfish 5, 210±228. Skurdal, J., Qvenild, T., Taugbol, T., Gamas, E., 1993. Long term study of exploitation, yield and stock structure of noble crayfish Astacus astacus in Lake Steinsfjorden, SE Norway. Freshwater Crayfish 9, 118±133. SoÈderbaÈck, B., 1995. Replacement of the native crayfish Astacus astacus by the introduced species Pacifastacus leniusculus in a Swedish lake: possible causes and mechanism. Freshwater Biol. 33, 291±304.

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SvaÈrdson, G., 1949. Stunted crayfish populations in Sweden. Rep. Inst. Freshwater Res. Drottingholm 29, 135±145. Thomas, W., 1991. Aspects of egg attachment in Austropotamobius pallipes (Lereboullet, 1858) (Decapoda, Astacidae). Crustaceana 61, 287±293. Unestam, T., Soderhall, K., 1977. Soluble fragments from fungal cell walls elicit defence reactions in crayfish. Nature 267, 45± 46. Westman, K., Savolainen, R., Pursiainen, M., 1993. A comparative study on the growth and moulting of the noble crayfish, Astacus astacus (L.), and the signal crayfish Pacifastacus leniusculus (Dana) in a small forest lake in southern Finland. Freshwater Crayfish 9, 451±465. Westman, K., Savolainen, R., 1995. The development of a signal crayfish Pacifastacus leniusculus (Dana) population in a small forest lake in central Finland. Freshwater Crayfish 10, 451±465. Wootton, R.J., 1984. Introduction: tactics and strategies in fish reproduction. In: Potts, G.W., Wootton, R.J. (Eds.), Fish Reproduction: Strategies and Tactics. Academic Press, New York, pp. 1±12.