ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on July 2, 2008
ICES Journal of Marine Science: Journal du Conseil 2008 65(7):1281-1290; doi:10.1093/icesjms/fsn114
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Biological features of the Lophius piscatorius catch in Scottish waters
1 NAFC Marine Centre, Port Arthur, Scalloway, Shetland ZE1 0UN, UK
2 Fisheries Research Services, Marine Laboratory, PO Box 101, 375 Victoria Road, Torry, Aberdeen AB11 9DB, UK
Correspondence to C. H. Laurenson: tel: +44 1595 772306; fax: +44 1595 772001; e-mail: chevonne.laurenson{at}nafc.uhi.ac.uk
Laurenson, C. H., Dobby, H., McLay, H. A., and Leslie, B. 2008. Biological features of the Lophius piscatorius catch in Scottish waters. – ICES Journal of Marine Science, 65: 1281–1290.Here, data on 50 265 Lophius piscatorius sampled between 1998 and 2006 on board commercial fishing vessels during observer trips and chartered surveys at Shetland, west of Scotland, and Rockall are analysed. In each area, length differed significantly with depth (p < 0.001), there was an increase in modal size with increasing depth down to 450 m, and large fish dominated hauls in deeper water. The sex ratio of all data combined was 0.88 females:1 male, but it varied by area, depth, and season, with males greatly outnumbering females in deep water west of Scotland during the first quarter of the year. The proportion at length that were female differed significantly with depth, and the highest proportions of mature fish were in deep water at Rockall and west of Scotland. L50% maturities, for all data combined, were 102.4 cm for females and 58.3 cm for males.
Keywords: anglerfish, L. piscatorius, monkfish, Rockall, Scotland, Shetland
Received 30 November 2007; accepted 3 June 2008; advance access publication 2 July 2008.
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Introduction |
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Anglerfish, commonly known as monkfish (Lophius piscatorius), are widely distributed in the waters around Scotland, but their range extends from Iceland, the Faroe Islands, and Norway (Ofstad and Laurenson, 2007; Solmundsson et al., 2007) in the north to the Straits of Gibraltar and the Mediterranean in the south (Caruso, 1989). The fishery for anglerfish by Scottish vessels is mainly concentrated on the shelf around Shetland (ICES Division IVa), the shelf edge to the west and northwest of Scotland (ICES Division VIa), and at Rockall (ICES Division VIb; ICES, 2007b). Catches are principally of the white-bellied anglerfish, L. piscatorius, although the black-bellied anglerfish Lophius budegassa is also taken, accounting for between 0.1% and 17% of landings (Laurenson et al., 2008).
In the early 1980s, anglerfish landings from ICES Subareas IV and VI were 
5000 t, but exploitation then increased and they peaked in the mid-1990s, reaching more than 30 000 t (Eurostat/ICES, 2007). Precautionary TACs were introduced in 1984 for Subarea VI and in 1998 for Subarea IV. However, both assessment and management of the northern shelf stock have proved problematic (Dobby et al., 2008) and currently the stock status is considered by the International Council for the Exploration of the Sea (ICES) to be "unknown" (ICES, 2007a).
In Scotland, there has been a concerted effort to improve knowledge of both the fishery and the stock dynamics. The economic importance of the fishery to the Scottish whitefish fleet has been reflected in industry support for a number of Scottish scientific initiatives, including an enhanced observer programme in 2005/2006, joint science industry surveys to estimate anglerfish biomass over the northern shelf (Fernandes et al., 2007), and a tally book scheme in which fishers record catches and fishing effort on a haul-by-haul basis (Dobby et al., 2008).
In parallel with the increase in commercial importance of the species in Scotland, several biological studies have been undertaken, e.g. those of Afonso-Dias and Hislop (1996), Hislop et al. (2001), Laurenson et al. (2004, 2005), Laurenson and Priede (2005), and Laurenson (2006). Some key results demonstrate that L. piscatorius is an ichthyophagous species, with a diet that reflects temporal prey availability, that they probably spawn in deep water during late winter and spring, that they have an average growth rate of 10 cm year–1, and that the pelagic larval stage may allow large-scale passive drift but that some larger fish also actively migrate long distances, e.g. between Shetland and Iceland.
There are, however, aspects of the biology and stock structure that are not yet fully understood, but which may affect its assessment. For each of the studies where maturity has been recorded, females in spawning condition are rarely caught. It is believed that these fish are concentrated in deep water (Hislop et al., 2001) and that these areas may act as a refuge for a spawning stock. If such a refuge exists, then the assessment methods traditionally used that make dynamic pool assumptions are likely to be inappropriate.
Here, we describe the characteristics of catches of L. piscatorius in the northern North Sea (Division IVa), west of Scotland (VIa), and at Rockall (VIb), based on length, sex, and maturity data collected by scientific observers on commercial vessels. We also discuss the implications of various aspects of the biology for assessment of the stock.
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Material and methods |
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The data were collected by scientific observers on demersal trawlers during both chartered surveys and commercial fishing trips in waters around Shetland, west of Scotland, and at Rockall between 1998 and 2006. The locations, based on the calculated midpoints between shooting and hauling positions, and the depths of the hauls are shown in Figure 1. The distribution of samples covers the main fishing areas of the stock.
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The number of trips in each area, year, and quarter (Q) are shown in Table 1. Catches were examined on a haul-by-haul basis, and 1041 hauls were sampled. The total length (TL) of 50 265 L. piscatorius was measured to the nearest centimetre, and sex and maturity stage were recorded for 12 589 females and 14 381 males. The maturity stages were as defined by Afonso-Dias and Hislop (1996).
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Tests for homogeneity of variance (Levene's statistic) indicated that the non-parametric Kruskal–Wallis test was appropriate for the following comparisons: comparing the lengths of L. piscatorius caught in 50-m depth strata in each area, between-areas comparison of the same parameter in the 100–149, 150–199, and 200–249 m strata and, for data from Shetland, between-season and between-year comparisons of quarterly data. Post hoc Nemenyi tests (Zar, 1999) were used to identify between which samples the differences were significant. Mann–Whitney U-tests were used to investigate whether lengths differed between west of Scotland and Rockall in the 250–299, 300–349, and 350–399 m strata.
To further investigate the mean lengths of anglerfish caught, a generalized additive model (GAM) was used to model trends in mean length relative to four predictors; year, depth, latitude, and longitude in the form of the equation: Length = s(Year) + s(Depth) + s(Latitude) + s(Longitude). The scatterplot smoother used was the cubic spline, s (Hamming, 1973). A stepwise removal of terms was carried out and interpreted using an ANOVA to determine the factors that had a significant effect on the model, using S-PLUS 7 (MathSoft©) software.
G-tests were used to investigate differences in sex ratio between areas. Paired-sample t-tests and two-way ANOVA (without replication) were considered appropriate to compare the proportion female-at-length between areas, depths, seasons, and years.
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Results |
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Length
Lengths of the anglerfish sampled ranged from 11 to 139 cm, but 57% of the fish were in the 40–60-cm size range and the modal length was 50 cm. By area, modal length was 50 cm at both Shetland and west of Scotland, and 56 cm at Rockall (Figure 2). West of Scotland, 9% of L. piscatorius were small (<40 cm), compared with 24 and 34% at Rockall and Shetland, respectively. The percentage of large (>60 cm) fish was greatest at Rockall, 31%, and just 14% west of Scotland and at Shetland, respectively.
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Length frequency distributions of catches in each area and in each sampled 50-m depth stratum are shown in Figure 3. In general, modal size increased with depth. Significant differences related to depth were detected in all areas (all p < 0.001). Post hoc Nemenyi tests on data from the Shetland area indicated that, of the possible 28 between-stratum comparisons, 18 resulted in significant differences at p < 0.05 and that all those involving the <50 and 50–99-m strata had fish significantly smaller than those in deeper strata (each at p < 0.05). West of Scotland, lengths in each of the 50-m depth strata <350 m differed significantly from those at depths >350 m, fish being smaller in shallower strata (post hoc Nemenyi tests, each at p < 0.01), and at Rockall, lengths in depth strata <450 m were significantly smaller than those from depth strata >500 m (post hoc Nemenyi tests, each at p < 0.01).
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For most depth strata, significant between-area differences in length were detected. At 100–149, 150–199, and 200–249 m, there were differences between all areas (each at p < 0.0001). Post hoc Nemenyi tests indicated differences at p < 0.001 between each of the area comparisons at 100–149 m, with larger fish at Shetland and smaller fish at Rockall. At 150–199 m, fish at Shetland were significantly larger than those in the other areas (p < 0.001 in each case), and at 200–249 m, anglerfish from west of Scotland were significantly smaller than those at Shetland (p < 0.001) or Rockall (p < 0.05). At 250–299, 300–349, and 350–399 m, comparisons between west of Scotland and Rockall could be made (Figure 3). Although we found differences at p < 0.01 and p < 0.001, respectively, in the shallower strata, there was no significant difference in length at 350–399 m.
Over the period investigated, the dataset from Shetland was most complete, and the length distributions are shown on a quarterly basis for each year for both the 100–149 and 150–199 m strata (Figure 4). From this, we found significant annual differences in lengths for each quarter in both strata (p < 0.001 in each case), except for Q4 data at 150–199 m. The proportions of fish <40 cm in catches were variable, with a very strong cohort of small fish evident from Q4 1999 persisting through 2000 (Figure 4). Data were available in each quarter in both 1999 and 2000 for the 100–149 m strata (Figure 4), and although there were significant quarterly differences in lengths in 1999 (Kruskal–Wallis: 
2 = 687, d.f. = 3, p < 0.0001), this was not detected in 2000 (2 = 2.796, d.f. = 3, p = 0.424). A much larger proportion of fish <40 cm was recorded during Q4 than at other times in 1999.
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Scatterplots of the variables used in the GAM are shown in Figure 5. The relationships of mean anglerfish length with latitude and longitude reflect the geographic areas in which the samples were collected (Figure 5), and the concentration of samples from Shetland is also reflected in the higher density of data points in depths <200 m. The GAM plots are shown in Figure 6 and show the best fitting smoothers (and 95% confidence intervals, CIs) for the effect of time, depth, latitude, and longitude on mean length of anglerfish caught. The density of samples for each covariate value is shown in the rug under each covariate effects plot. The lower the number of samples, the wider is the spread in the CIs. Water depth, latitude, longitude, and time were all very significant covariates (p < 0.001). The smallest response range was observed in the spline plot for year, which indicated that, of the four factors, year exerted the least effect on the mean length of anglerfish catches. Water depth provided the greatest reduction in residual deviance, explaining 57% of it (Table 2). The spline plot of time revealed a non-linear response pattern, with a minimum at the end of 1999 and during 2000. This probably reflects the large recruitment of small fish then, mentioned above (Figure 6). The spline plot of depth shows a strong positive relationship between length and depth, particularly to
450 m. The spline plots of latitude and longitude show positive and negative relationships with mean length, respectively.
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Sex ratio
Overall, the sex ratio was 0.88 female:1 male (Figure 7). However, in waters <450 m, there were significant between-area differences (G-test: Gadj = 102.7,
20.001[2] = 13.812, p < 0.001), with 0.78, 0.94, and 1.06 females:1 male west of Scotland, at Rockall, and Shetland, respectively. In depths >450 m, there were 0.27 females:1 male west of Scotland and 1.55 females:1 male at Rockall, with a G-test revealing a significant between-area difference (Gadj = 208.5, 20.001[1] = 10.828, p < 0.001). Note that no data were collected from >450 m at Shetland.
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At depths <450 m, there were approximately equal numbers of males to females at fish lengths <65 cm, at >65 cm the proportion of females increased, and at 100+ cm males were rare (Figure 8). Despite this general pattern, differences in the proportion female-at-length were found between Shetland and west of Scotland (t = 4.15, d.f. = 84, p = 0.00004), and between west of Scotland and Rockall (t = –2.29, d.f. = 88, p = 0.012; Figure 8). In contrast, at depths >450 m, the available data from west of Scotland and Rockall showed that males dominated at lengths <80 cm and females at lengths
80 cm (Figure 8). However, the proportion of females-at-length differed between these areas (t = –5.523, d.f. = 65, p < 0.001).
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For water <450 m, no evidence was found of seasonal differences in the proportion female-at-length. The comparisons made for the Shetland area were between September/October 2000, and January–March 2001 (t = 1.18, d.f. = 35, p = 0.246), and between October/November 2005, December 2005/January 2006, and February/March 2006 (F67,2 = 0.683, p = 0.507). West of Scotland, Q4 2005 and Q1 2006 were compared (t = 1.68, d.f. = 49, p = 0.49). Data from Rockall did not allow seasonal comparison. For water >450 m, only data from west of Scotland allowed seasonal comparison, and there was a significant difference in the proportion female-at-length between Q4 2005 and Q1 2006 (t = 3.14, d.f. = 37, p = 0.003). Between those times, the overall sex ratio decreased from 0.31 females:1 male in Q4 to 0.19 females:1 male in Q1.
The data on proportion female-at-length were also analysed to determine whether there were any annual differences. At Shetland, there were no significant differences in Q1 between 1999–2001 and 2006 (t = –0.94, d.f. = 65, p = 0.35), or in Q3 between 2001 and 2006 (t = 1.23, d.f. = 60, p = 0.22), but there was a difference in Q4 between 2000 and 2005 (t = –2.80, d.f. = 51, p = 0.007). West of Scotland, there was no significant between-years difference in Q4 data from 1999–2001 and 2005 at depths <450 m (F37,2.404 = 2.761, p = 0.059, using a Greenhouse–Geisser correction for sphericity). At Rockall, there were no significant differences in the proportion female-at-length between years in depths <450 m (t = 0.28, d.f. = 83, p = 0.78). Data were insufficient to investigate annual differences at depths >450 m and were also not available to allow seasonal comparisons.
Maturity
Overall, the L50% maturity was 102.4 cm for females and 58.3 cm for males (Figure 9). By area, the L50% values were similar at 97.5, 100.7, and 104.4 cm for females, and 60.5, 52.7, and 57.3 cm for males at Shetland, west of Scotland, and Rockall, respectively. At Shetland for the period 1998–2001, the L50% values were 99.4 cm for females and 57.9 cm for males, and in 2005 and 2006, L50% values were 92.6 cm for females and 61.5 cm for males.
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Maturing females (stage 3) were mainly caught between August and December, ripe females (stage 4) were caught between November and March, and recently spent females mainly from February on. Mature males were caught mainly from October to March, and the proportion of recently spent males increased during late February. Although mature males were widely distributed and were relatively many, the number of mature females was relatively low (overall <6% of females), with the highest numbers recorded in deep water west of Scotland (12% of females) and at Rockall (15% of females).
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Discussion |
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Over the areas and periods studied here, we found a consistent increase in mean fish length in the catches with depth, substantiating fisher reports for our study area. In the GAM analysis, depth explained 57% of the residual deviance. Although anglerfish of a wide range of lengths are found over all depths, we can generalize that on the shelf (<200 m), most are <60 cm, on the upper slope (200–450 m) the dominant size increases to 40–80 cm, and in deeper water those caught west of Scotland are mainly 50–80 cm long, and at Rockall between 60 and 100 cm. This pattern would suggest a general migration into deeper water with growth over time. Our data on seasonal changes in sex ratio at length, along with evidence from a tagging study at Shetland (Laurenson et al., 2005) and from fisher reports of seasonal changes in abundance in parts of our study area, indicate that patterns of movement are more complex than generally recognized, particularly at a seasonal level, but that those complexities are not yet fully understood.
Outside our study area, only Ungaro et al. (2002) noted that L. piscatorius caught on the continental shelf in the Mediterranean Sea (<200 m) were smaller than those caught in deeper water. For L. budegassa in the Mediterranean Sea, Maravelias and Papaconstantinou (2003) reported size-specific aggregation patterns, but in contrast to what has been observed for L. piscatorius, they reported that small and large fish both congregated in areas 300 m deep, whereas fish of intermediate size aggregated in shallower water.
In addition to a general increase in length with depth, we found significant differences in anglerfish lengths in catches between areas and within areas over time. Some variation is to be expected, particularly when there are cohorts of differing strength entering a fishery, as observed. During late 1999, a strong cohort of small anglerfish which persisted through 2000 was evident at Shetland, and our data confirm anecdotal evidence from fishers then. Strong cohorts have also been reported from Iceland (Jónsson, 2007). A strong cohort with a modal length of 26 cm was recorded at Iceland in May 1999 and was assumed to represent the 1998 year class. By May 2000, the cohort dominated the length distribution, with a strong mode at 40 cm (Jónsson, 2007), similar to the modal length of the strong cohort observed at Shetland then. Although the geographic extent of this strong cohort is unknown, an increase in abundance of anglerfish has been widely reported by the local industry since the early 2000s (Dobby et al., 2008). We suggest that the cohort in our data had a broader distribution and likely contributed towards this strong recruitment.
The largest proportions of anglerfish <30 cm were in catches in <50 m of water at Shetland, and we believe that certain shallow inshore areas around Shetland may act as nursery grounds. It has been reported previously that small anglerfish are abundant on some inshore areas at Shetland, related to the seasonal abundance of sandeels (Ammodytidae), a main prey item (Laurenson and Priede, 2005). Nursery areas west of Scotland are yet to be identified. At Rockall, although anglerfish caught between 100 and 200 m were mostly smaller, further investigation in relation to nursery areas is required. Should such areas be identified, routine surveys could provide an early indication of the relative strengths of cohorts entering the fishery, and in the longer term contribute towards improved management of the fishery.
The pattern of approximately equal ratios of females to males, rising to almost exclusively females at the largest sizes in waters <450 m, is similar to that reported for the same species by Afonso-Dias (1997) and Duarte et al. (2001), for L. budegassa in our study area (Laurenson et al., 2008), and for L. americanus (Richards et al., 2008). Although both EC (2001) and García-Rodríguez et al. (2005) showed that the overall percentage of males increased with depth in Scottish waters and in the Spanish Mediterranean, respectively, the marked difference in the proportion female-at-length between depths <450 and 450 m has not been documented previously.
We suggest that the dominance of males <80-cm long that we recorded in deeper water, together with the seasonal increase (from Q4 to Q1) in the proportion of males in deep water west of Scotland reflects spawning activity, which is between November and May in that area (Afonso-Dias and Hislop, 1996). Although we recorded a seasonal increase in males in deep water, we did not detect any seasonal changes in the proportion in shallower water, which could have suggested migration of spawning males into deeper water. However, further research into the change in the proportion of females-at-length, before and during the spawning season, and on a finer geographical scale, may better define both the timing and the locations of spawning.
It was first suggested by Fulton (1903) that anglerfish spawn in deep water. Our data indicated that the proportions of mature females caught in deep water are higher, so the deep water areas west of Scotland and at Rockall are believed to be the most significant in our study area for spawning. Even with the large size of our dataset, mature (stages 3–5) females were few, and ripe (stage 4) females noticeably scarce. Such an apparent scarcity of mature females has been highlighted in previous studies, e.g. by Quincoces et al. (1998), Duarte et al. (2001), and EC (2001), and this has hindered the confirmation of spawning locations and the estimation of spawning-stock size. We suggest that the apparent scarcity of ripe females could reflect either a lowering of their catchability or a short duration of that stage. Evidence from strandings in Norwegian fjords of large females in ripe condition (O. Bjelland, IMR, Bergen, pers. comm.) has led to speculation that females may migrate into shallow water as part of their spawning behaviour. Evidence from data storage tags taken from L. piscatorius (E. Jónsson, MRI, Iceland, unpublished data; I. Gibb, FRS, Aberdeen, unpublished data) and from L. americanus (Rountree et al., 2006) has shown that anglerfish can make short-duration near-surface migrations. However, a migration into shallow water to spawn would appear to be contradictory to the seasonal increase in the proportion of males-at-length that we observed in deep water during the spawning season. Clearly, many questions associated with spawning locations, depths, and behaviour remain unanswered and require further investigation.
The lengths at first maturity for females found here exceed those reported by other authors (Table 3), but this may reflect the larger length range and greater numbers of large fish in this study than in most of those studies, but again even in this study, the number of mature females was relatively small. The lengths at first maturity for males in this study are within the range of those listed in other publications (Table 3). All studies agree that the length at maturity of females is much larger than for males, and this, combined with the variation in length distribution with depth and in some cases with area, and with the proportion female-at-length by depth and season highlights the complexities within the anglerfish stock structure. These factors should be both understood and considered when estimating the proportion of mature males and females in catches.
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To conclude, the data presented here suggest considerable heterogeneity in the biological characteristics of the anglerfish stock on the northern shelf related to area, season, and depth. Although this may to some extent reflect migratory behaviour of the species, it highlights the need to obtain representative samples of the landings for stock assessment purposes. Findings in relation to the proportion female-at-length suggest that fishing mortality may differ by sex, dependent on depth and season, and although we have demonstrated this trend, its patterns are not yet fully understood.
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Acknowledgements |
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We thank the scientific observers from FRS and NAFC Marine Centre, the skippers and crews of vessels that accommodated observers, and K. Peach for collating FRS datasets.
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References |
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