INTERNATIONAL COUNCIL FOR CM 2001/J:27 THE EXPLORATION OF THE SEA The Life History, Dynamics and Exploitation of Living Marine Resources: Advances in Knowledge and Methodology

WHERE ARE THE MATURE ANGLERFISH? – THE POPULATION BIOLOGY OF LOPHIUS PISCATORIUS IN NORTHERN EUROPEAN WATERS.

Chevonne Laurenson, I.G. Priede, L.W. Bullough and I.R. Napier

ABSTRACT

The general relationship between length frequency and water depth was investigated for anglerfish (monkfish) Lophius piscatorius Linnaeus 1758 in waters around the Shetland Isles, Scotland. Length and age data were obtained during commercial trawling trips between 1998 and 2000 and correlated with depth. A trend of increasing average length (and age) with increasing depth was found, in accordance with Heincke’s Law. Within the length frequency distributions modes thought to represent year classes correlate with mean lengths-at-age derived from otolith readings. Analysis of maturity stages suggests that the average length at first maturity is 59cm for males and 96cm for females. Such fish represent only 12% and 2% respectively of the commercial catch. The high proportion of immature anglerfish, particularly females, within the fishery is a cause for concern. A Harden-Jones style triangle is presented with immature fish predominating in the inshore and shelf waters and a general movement into deeper waters with increasing size and maturity. It appears however that even in deep water mature anglerfish are relatively scarce. It is speculated that the triangle is completed with a planktonic drift of eggs and larvae towards shallower waters before settlement.

C. Laurenson, L.W. Bullough, I.R. Napier: North Atlantic Fisheries College, Port Arthur, Scalloway, Shetland, U.K. [tel: +44 (0)1595 880328, fax: +44 (0)1595 880549, e-mail: [email protected], [email protected], [email protected]]. I.G. Priede, University of Aberdeen, OceanLab Culterty, Newburgh, Aberdeen, U.K. [tel: +44 (0)1358 789631, fax: +44 (0)7775 866971, email: [email protected]].

Introduction

In the past, anglerfish were taken as a by-catch (and discarded) during bottom trawl groundfish fisheries (1999; Afonso-Dias, 1997; Fahy and Gleeson, 1992). However, a targeted fishery for Lophiid species has developed in ICES Areas IV and VI over the last 10-15 years. The majority of the UK catch of anglerfish is taken in Scottish waters (Afonso-Dias, 1997). The fishing grounds to the north and west of the Shetland Isles (covered during this study) became important within the targeted anglerfish fishery during the 1990’s. Statistics show that in Scotland the landings peaked at 26.1 thousand tonnes, worth £44.8 million at first sale during 1996 but this fell steadily to 12.1 thousand tonnes, worth £28.4 million during 1999 (2000b). To put their value and landings into perspective, during 1996 cod Gadus morhua and haddock Melanogrammus aeglefinus landings were worth £38.9m (42,300 tonnes) and £49.8m (82,300 tonnes) respectively. Anglerfish are species whose maximum value is fresh rather than processed and for which continental Europe has provided the main markets (Fahy and Gleeson, 1992). During the present study, which covered grounds around the Shetland Isles (Figure 1), with additional data from grounds to the west of the Hebrides it was found that Lophius piscatorius Linneaus, 1758, the white-bellied anglerfish was the predominant species within the fishery. This species is sold in Scotland under the trade name of (and is commonly known as) ‘monks’ or ‘monkfish’. L. piscatorius represented 99% of anglerfish catches. The remaining 1% was L. budegassa Spinola, 1807, the black- bellied anglerfish, or monkfish whose distribution is concentrated more in the Mediterranean. Similarly Afonso-Dias, (1997) found that L. budegassa represented not more than 3% of catches to the northwest of Scotland. The species are not separated during selling or processing. Although the fishery for Lophiid species has become of economic importance to the trawling fleet in recent years, much basic information on the biology, ecology and abundance is still lacking. It is considered that for the North Sea and West of Scotland fishing mortality and recruitment are not well estimated (2000a). The purpose of this study was to gather, first hand, information relating to the anglerfish catches on the grounds around the Shetland Isles. From this, their length frequency and age have been investigated in relation to water depth and biological features of the species and its fishery, and are discussed in relation to the possible implications for its future management.

Materials & Methods

Between May 1998 and June 2000 data collection trips were conducted onboard commercial whitefish trawlers belonging to the Shetland fleet. A total of 286 hauls were sampled covering 1,621 hours trawling time. All 11,257 anglerfish caught were measured to the nearest centimetre below (total length). For the purpose of age determination, sagittal otoliths were collected from a representative sample of the catch. Additional otolith samples were obtained from market sampling of L. piscatorius landed in Shetland. A total of 2428 pairs of otoliths were collected, stored in and read under a 1:1 glycerine: water solution following the methodology of Tsimenidis and Ondrias, (1980). Otoliths were used as the ageing structure partly due to their ease of removal, storage and preparation but also because samples were taken from commercial catches and their removal did not affect the market value. As all landings are of gutted fish, determination of sex and maturity stage was done de visu using the scheme of Afonso-Dias and Hislop, (1996). Maturity stage was assigned to 2137 males and 2207 females.

For each tow the shooting and hauling times and positions were recorded, as was the tow track. On most of the sampling trips water temperature and depth were recorded every 2 minutes using a Vemco minilogger attached to the net otherwise depths were recorded from the wheelhouse echosounder.

During the summer of 1999 additional anglerfish data was collected during sandeel (Ammodytes marinus) surveys in inshore waters around Shetland. Data collected by one of the authors’ (L.B.) from grounds to the West of the Hebrides (depth range 150 - 850m) has also been included in the analyses.

Kolmogornov-Smirnov 2-sample tests (Sokal, 2000) were carried out to compare length frequency distributions over the depth ranges.

Results

Geographical area Figure 1 shows both the area covered during observation trips in waters around the Shetland Isles and the area to the west of the Hebrides from where additional data was obtained.

Age determination The mean lengths-at-age determined from otolith readings are shown in Table 1 and the resulting growth curve in Figure 2. As can be seen, the growth curve agrees closely with those from previous studies, confirming the accuracy of age determination in this study.

Table 1. Mean lengths-at-age for L. piscatorius determined from otolith readings.

Age Mean Age Mean (years) length (years) length (cm) (cm) 0 17.9 7 69.2 1 28.9 8 74.0 2 36.4 9 79.7 3 43.3 10 86.3 4 50.0 11 93.0 5 56.6 12+ 109.2 6 62.6

Length frequency in relation to fishing depth Figure 3 represents percent length frequency distributions of L. piscatorius caught in different depth ranges. The mean lengths at ages as determined during the present study are superimposed over the percent length frequency distributions. A progressive shift towards predominantly larger and older fish with increasing depth is apparent. In Table 2 summary data from the length frequency distributions is presented for each depth range, mean age at each depth is also shown. The Kolmogornov-Smirnov tests showed significant differences between the length frequency distributions in each successive depth range (P> 99% in each case). Mean length data from each depth range within the Shetland area (Table 2) are plotted against the mid-point of each depth range and shown in Figure 4. A strong linear relationship exists (y = 5.32x – 116.9, r = 0.995).

Table 2. Summary data from the length frequency distributions at each depth range.

Depth Length Mean Mean Age N Range (m) Range (cm) Length (cm) (years) 1 <50m 4 – 54 27 1.3 132 1 50-99m 16 – 54 35 2.2 626 1 100-149m 16 – 103 47 3.7 9331 1 150-199m 13 – 124 54 4.6 1213

2 150-300m 28 – 71 52 4.4 205 2 600-850m 22 - 125 64 6.1 473 1 Shetland waters, 2 West of Hebrides.

Maturity The sex ratio for each size-class sampled are shown in Figure 5. For anglerfish below about 58 cm the sex ratio was approximately 1:1, but above this size the proportion of females increases with length. Fish above 91 cm in length were exclusively female. Figure 6 shows the maturity ogives for each sex by length (based on macroscopic observations). The L50 for female L. piscatorius is 98cm compared to 58cm for males. From the length frequency distributions at each depth range (Figure 3) and the sex ratio and maturity ogives (Figures 5 and 6) the percentage of mature L. piscatorius (capable of spawning: Stages III-V) has been estimated for each of the depth ranges sampled. This indicates a general trend of increasing percentages of mature fish within the population with increasing depth. Higher proportions of males than females were reproductively active at all depth ranges sampled.

Table 2. Estimated sex ratio of L. piscatorius and percentages of mature males and females in each depth range sampled (based on length frequency data). Depth m Male : Female % Male spawners % Female spawners within total population within total population 1 <50m 1 : 1.00 0.9 0.2 1 50-99m 1 : 1.01 4.6 0.8 1 100-149m 1 : 1.07 11.2 2.2 1 150-199m 1 : 1.10 16.9 3.3

2 150-300m 1 : 1.01 15.8 1.7 2 600-850m 1 : 1.27 25.7 6.5 1 Shetland waters, 2 West of Hebrides.

Discussion

A large amount of data has been collected during this study on the size, age, sex and maturity of L. piscatorius in the waters around Shetland, and in particular of those caught by commercial fishing vessels. Close agreement was found between the average lengths at age obtained in this study and those reported from previous studies, indicating that accurate ages were determined from otoliths in this study. Previous studies have derived ages from other structures, including vertebrae and illicia, as well as otoliths, and illicia have been held to provide the most accurate age readings for this species. Unlike vertebrae or illicia, however, otoliths can be removed without causing external damage to the fish and thus affecting their market value; an important consideration when collecting data in a commercial fishery.

Analysis of the relationship between length (and age) and depth has revealed a strong linear relationship between the average length and age of L. piscatorius and water depth around Shetland. A similar trend was apparent in data collected in deeper water to the west of the Hebrides. The trend for larger (and older) fish to occur at greater depths (Heincke’s Law) was first reported for plaice in the North Sea by Heincke (1913; quoted by Cushing, 1982). It has since been found to hold true for a number of species (reviewed by Merrett and Haedrich, (1997), but has not previously been noted for L. piscatorius or other Lophiid species.

Female L. piscatorius were found to mature at a larger size (and older age) than males. At least partly as a result the sex ratio changes as the fish get larger, with an increasing proportion of females at larger sizes. Above about 91 cm the fish sampled were exclusively female. Similar trends have been reported in previous studies e.g. Afonso-Dias and Hislop, (1996); Duarte et al., (2001); Quincoces et al., (1998). The L50s determined for male and female L. piscatorius in this study (58 cm and 98 cm, respecively) are close to, although slightly larger than, the range of previously reported values; from 49.0 cm to 54.5 cm for males and from 73.0 cm to 93.9 cm for females (Afonso-Dias and Hislop, 1996; Duarte et al., 2001; Quincoces et al., 1998). The present study analysed a substantially larger sample of anglerfish than previous studies, and was focussed on generally more northern waters. The relatively small proportion of mature anglerfish in the populations sampled is also likely to result in variability in L50 values.

It is noteworthy that none of the 2207 commercially caught female L. piscatorius whose maturity stage was determined during the course of this study were ripe, i.e. ready to spawn. Nor were any mature females noted during any of the work on commercial vessels during the study. From the length frequency distributions and maturity ogives it is estimated that the proportion of mature (capable of spawning) females within the sampled population ranged from only 0.2% to 3.3%, with the proportion increasing with depth. The proportion of mature males in the population was higher, ranging from 0.9 to 16.9%, perhaps because males mature at a smaller size. The same trend of increasing proportion of mature males with increasing depth was apparent.

The data obtained during this study suggests a life history pattern for L. piscatorius whereby small (young) individuals predominate in shallow inshore waters and a general migration into deeper water occurs with increasing size and age. Thus highest proportions of large, old and mature anglerfish occurred in the deepest depth range sampled. Assuming that the anglerfish spawn in deep water the juveniles presumably drift towards shallower water before settlement, thus completing the cycle. Larval and juvenile L. piscatorius have been found over deep water to the west and north of Scotland and there is evidence that they could be carried over long distances by ocean currents (Hislop, 2001). These general movements are modelled in Figure 7 as a Harden-Jones style triangle (Harden-Jones, 1968) on the vertical plane.

Although a trend of increasing size, age and proportion mature with increasing depth was apparent in this study, the proportion mature remained relatively low in the deepest waters sampled. This suggests that mature female anglerfish may be concentrated in deeper water still (>200 m). In a recent survey (Hislop et al., 2001) 17 of the 18 pre-spawning mature females recorded to the north and west of Scotland were taken in deep water (220-900m). Much more sampling of deeper waters would be required to increase our understanding of the distribution of mature female anglerfish.

However, even in depths of between 600 and 850 m (West of Hebrides) the proportion of mature females in the population was estimated as still only 6.5%. Given that the maximum depth range of L. piscatorius is normally around 1000 m, it does not seem likely that mature anglerfish (especially females) constitute a high proportion of the population at any depth in the waters to the north and west of Scotland. The relatively small proportion of large, old, mature females (and to some extent males) in the L. piscatorius population sampled could be a result of heavy, targeted fishing pressure over the last 10 to 15 years having removed most large, mature individuals. Given the relatively late maturity of L. piscatorius the chances of individuals reaching maturity in a heavily fished stock must be poor.

Conventional management models, such as those by Beverton, (1957), Ricker (1954, 1975) and Shepherd, (1982) essentially rely on allowing a proportion of the spawning stock biomass (SSB) to be caught, whilst ensuring enough remain to provide an adequate level of recruitment. They must also ensure that an adequate number of young fish survive to maturity, to maintain the SSB.

This study has clearly shown that that the current L. piscatorius fishery in northern Scotland, which occurs mainly in shelf waters, is based almost entirely on immature fish. While it appears that anglerfish tend to move offshore into deeper water as they mature it seems that only a small proportion actually survive to reach maturity. In addition to the trawl fishery on the shelf, which was the focus of this study, a targeted gill-net fishery for anglerfish also takes place along the shelf-edge. The impact of this on the L. piscatorius population is not known, but it again has the potential to interrupt a general offshore migration with growth and maturity.

The results of this study give rise to serious concerns about the long-term sustainability of the fishery for L. piscatorius. Further evidence for possible overfishing of this stock arises from a sharp decline in catches of this species in the Scottish fishery in recent years (with little evidence of any reduction in effort). Much more information is needed, however, to fully understand the biology of L. piscatorius, the current status of stocks in Scottish waters and the impact of the fishery.

Acknowledgements Data collected until July 1999 received funding under Study DG-FISH No. 96/086 Investigation of the monk fishery in Northern European Union Waters. Funding from June 2000 has been under Teaching Company Scheme Project No. 3107 between North Atlantic Fisheries College and Shetland Fish Producers’ Organisation. A sincere thanks goes to all skippers and crew without which observer trips would not have been possible.

References

(1999): Report of the ICES Advisory Committee on fishery management, 1998. Part 1. I.C.E.S. Cooperative Research Report 229, 335-337. (2000a): Report of the ICES Advisory Committee on Fishery Management, 1999. Part 2. I.C.E.S. Cooperative Research Report 236, 210-215. (2000b): Scottish Sea Fisheries Statistical Tables 1999. Scottish Executive Publications. Afonso-Dias, I. (1997): Aspects of the biology and ecology of anglerfish (Lophius piscatorius, L.) off the west-coast of Scotland (I.C.E.S. Sub-area VIa), pp. 192: Department of Zoology, University of Aberdeen, Aberdeen. Afonso-Dias, I., and Hislop, J.R.G. (1996): The reproduction of anglerfish Lophius piscatorius Linnaeus from the north-west coast of Scotland. Journal of Fish Biology 49, 18-39. Beverton, R.J.H. and Holt, S.J. (1957): On the dynamic of exploited fish populations. Ministry of Agriculture, Fisheries and Food, Fisheries Investigations, UK, Series 2 19. Crozier, W.W. (1989): Age and growth of angler-fish Lophius piscatorius L. in the North Irish Sea. Fisheries Research 7, 267-278. Cushing, D.H. (1982): Climate and Fisheries. Academic Press. London. Duarte, R., Azavedo, M., Landa, J. & Pereda, P. (2001): Reproduction of anglerfish (Lophius budegassa Spinola and Lophius piscatorius Linnaeus) from the Atlantic Iberian coast. Fisheries Research 51, 349-361. Duarte, R., Azevedo, M., and Pereda, P. (1997): Study of the growth of southern black and white monkfish stocks. I.C.E.S. Journal of Marine Science 54, 866- 874. Fahy, E., and Gleeson, P. (1992): The exploitation of angler fish Lophius spp. in Irish waters. Irish Fisheries Investigations Series B 40, 17pp. Fulton, T.W. (1903): The distribution, growth, and food of the angler, Lophius piscatorius. Twenty-first annual report of the Fishery Board for Scotland., 186-217. Harden-Jones, R.F. (1968): Fish Migration. Edward Arnold. London. Hislop, J.R.G., Gallegro, A., Heath, M.R., Kennedy, F.M., Reeves, S.A. & Wright, P.J. (2001): A synthesis of the early life history of the anglerfish, Lophius piscatorius (Linnaeus, 1758) in northern British waters. ICES Journal of Marine Science 58, 70-86. Landa, J., Pereda, P., Duarte, R. & Azevedo, M. (2001): Growth of anglerfish (Lophius piscatorius and Lophius budegassa) in Atlantic Iberian waters. Fisheries Research 51, 363-376. Merrett, N. R. and Haedrich, R.L. (1997): Deep-sea Demersal Fish and Fisheries. Chapman & Hall. London. Quincoces, I., Santurtun, M. & Lucio, P. (1998): Biological aspects of white anglerfish (Lophius piscatorius) in the Bay of Biscay (ICES Division VIIIa,b,d), in 1996-1997. I.C.E.S. C.M. 1998/O:48, 1-29. Ricker, S.E. (1954): Stock and Recruitment. Journal of the Fisheries Research Board of Canada. 11, 555-623. Ricker, S.E. (1975): Computation and interpretation of biological statistics of fish populations. Fisheries Research Board of Canada Bulletin 191. Shepherd, J.G. (1982): A versatile new stock-recruitment relationship for fisheries, and the construction of sustainable yield curves. Journal du Conseil, Conseil Internationale pour L'Exploration de la Mer 40(1), 67-75. Sokal, R.R. and Rohlf, F.J. (2000): Biometry: the principals and practice of statistics in biological research. W.H. Freeman and Company. New York. Tsimenidis, N., and Ondrias, J.C.H. (1980): Growth studies on the angler-fishes Lophius piscatorius L., 1758 and Lophius budegassa Spinola, 1807 in Greek waters. Thalassographica 3, 63-94.

62 Faroe

61

Shetland 60 m 200

100 m 59

58

57 Scotland

56 1086420

Figure 1. Map of waters around Scotland showing survey areas around the Shetland Isles and to the west of the Hebrides. 100m and 200m contours also shown.

140

120

100

80

60 Length (cm) Length

40

20

0 024681012141618202224 Age (years) Figure 2. Comparison of mean length-at-ages with those of previously published sources (Afonso-Dias, 1997; Crozier, 1989; Duarte et al., 1997; Fulton, 1903; Landa et al., 2001; Tsimenidis and Ondrias, 1980).

0 1 2 3 4 5 6 7 8 9 10 11 12+ 20 a

16

12

8

<50 m 4

0 6 a 4 2 50 - 99 m 0 4 a 2 100 - 149 m 0 4

equency a r 2 150 - 199 m cent F r 0

Pe 8 b 6 4 2 150-300 m 0 8 b 6 4 600 - 850 m 2 0

0 20 40 60 80 100 120 140 Length cm a Shetland waters b West of Hebrides Figure 3. Percent length frequency distributions of L. piscatorius caught in different depth ranges.

Mean length (cm) 020406080 0

40

80

120 Mean Depth (m) Depth Mean 160

200

Figure 4. Relationship between mean L. piscatorius length at each depth range and mid-point of each depth range for grounds around the Shetland Isles.

1

0.8

0.6 tion Female tion r opo r 0.4 P

0.2 20 40 60 80 100 120 Length cm Figure 5. Sex ratio of L. piscatorius at each size-class sampled.

100

80 e r 60

cent Matu 40 r Pe 20 Female 0

100 e r 80

60 cent Matu r 40 Pe 20 Male 0 0 20 40 60 80 100 120 140 Length cm

Figure 6. Maturity ogives by sex for L. piscatorius. L50 for females is 98cm and 58cm for males.

Depth

0m 50m 100m 150m General migration Inshore 200m towards nursery depth grounds Main fishery over shelf Planktonic

drift 400m

600m

Spawning 800m

1000m

Figure 7. Harden-Jones style triangle modelling the life history pattern of L. piscatorius.