Abstract

The indirect effects of demersal fisheries, such as habitat degradation, are currently thought to be impacting gadoid stocks. Maerl fulfils nursery area prerequisites for several invertebrate species, so its role in similar ecosystem service provision for gadoids has been addressed. Juvenile cod ( Gadus morhua ), saithe ( Pollachius virens ), and pollack ( Pollachius pollachius ) in shallow (<7 m) inshore waters were surveyed with fykenets and scuba off western Scotland over a period of 12 months. Juvenile densities were highest from September to November, and at that time, significantly more were present during the day and associated with maerl (that lacked macroalgal cover) than with heavily vegetated rocky and gravel substrata. Juvenile cod were present throughout the year, whereas saithe appeared in July, and pollack from September to January. With its abundance of food, maerl probably has a high holding capacity for juvenile gadoids, and thus is an important part of the inshore nursery system.

1 Introduction

Maerl grounds, which vary in size from tens to thousands of square metres, consist of loose-lying, coralline red algae ( Giraud and Cabioch, 1976 ), and are in areas characterized by extensive water movement (tidal and/or wave action) in the photic zone ( Woelkerling, 1988 ). Live maerl grounds are highly biodiverse ( BIOMAERL team, 2003 ; Steller et al ., 2003 ), and have significantly greater heterogeneity than common adjacent substrata, including gravel, sand, and impacted dead maerl ( Kamenos et al ., 2003 ). A single physical impact event may significantly reduce the heterogeneity of maerl thalli to that of a gravel substratum, by breakage, and may lead to subsequent death of the maerl ( Hall-Spencer and Moore, 2000b ; Kamenos et al ., 2003 ). To date, no data are available on the effects of maerl on juvenile gadoid distributions, a topic addressed herein.

Recently, owing to realization that fishing pressure is exceeding sustainable limits on a global scale, there has been mounting pressure to reduce fishing capacity ( Pauly et al ., 2002 ; Schiermeier, 2002 ). Traditional controls such as reduction of quotas have been implemented in an effort to curb such pressures and to conserve spawning stocks. However, the indirect effects of demersal fisheries, such as habitat degradation, are now thought also to be affecting gadoid stocks ( Lindholm et al ., 1999 ).

To survive, pelagic populations of most gadoids are dependent on the recruitment of juvenile fish to shallow coastal areas that offer physical refuge and protection from predation ( Pihl, 1982 ). Recruitment of 0-group cod, for example, occurs over a short period (2–4 months) following metamorphosis from the larval stage, prior to settling on demersal habitats ( Campana et al ., 1994 ). Cod settlement begins in early summer ( Tupper and Boutilier, 1995a ) and, in western Scottish waters, peaks in July and declines to nothing in late November ( Magill and Sayer, 2004 ). Newly settled cod inhabiting rocky reefs establish and defend territories in a size-specific social hierarchy. 0-group fish, however, lose their site fidelity before their first winter, when they move offshore. During that interval, survival of 0-group cod is habitat-dependent ( Tupper and Boutilier, 1995b ).

In the absence of predators, juvenile gadoids forage over less complex substrata, including sand and gravel, but also over more complex maerl ( Hall-Spencer and Moore, 2002 ). However, when predators threaten, they utilize more complex substrata and vegetation for protection including: interstitial spaces of cobble substrata ( Gotceitas and Brown, 1993 ; Gotceitas et al ., 1995 ; Fraser et al ., 1996 ; Lindholm et al ., 1999 ); camouflage against pebble substrata ( Lough et al ., 1989 ); and hiding in unnamed vegetation ( Wheeler, 1980 ; Gregory et al ., 1997 ; Rangeley and Kramer, 1998 ; Lindholm et al ., 1999 ), or in stands of Desmarestia sp. ( Keats et al ., 1987 ), kelp ( Gotceitas et al ., 1995 ), eelgrass ( Borg et al ., 1997 ; Gotceitas et al ., 1997 ; Linehan et al ., 2001 ), Fucus sp. ( Borg et al ., 1997 ), or Cladophora sp. ( Borg et al ., 1997 ).

Distribution, foraging activity, and predator avoidance are also reflected in diel changes of fish location. More 0-group cod are caught at night, independent of the sampling gear used ( Methven and Bajdik, 1994 ; Methven and Schneider, 1998 ; Pihl and Wennhage, 2002 ), which Methven and Schneider (1998) attribute to inshore movement at night (or dusk) rather than to increased catchability then. Juvenile gadoids undertake such inshore migrations, either as they shoal, forage, and feed during the day, then disperse at night to protective inshore bottom cover, so avoiding predation by older conspecifics, which takes place mainly at night ( Pihl, 1982 ; Keats and Steele, 1992 ; Grant and Brown, 1998a , b ; Pihl and Wennhage, 2002 ), or as they feed nocturnally in shallow waters, but aggregate on the bottom by day in deeper water, seeking protection during times of higher predation ( Lough et al ., 1989 ; Olsen and Soldal, 1989 ; Linehan et al ., 2001 ). Keats and Steele (1992) suggest that, because there are so many conflicting reports of feeding times, juvenile cod exhibit great flexibility in diel activity patterns.

This study aims to investigate the diel, shallow-water (<10 m Chart Datum, CD) distribution of juvenile cod ( Gadus morhua ), saithe ( Pollachius virens ), and pollack ( Pollachius pollachius ) in relation to live maerl and adjacent common substrata.

2 Material and methods

Investigations were carried out in Caol Scotnish, Loch Sween (56°01.99′N 05°36.13′W), southwest Scotland. Caol Scotnish is characterized by three key sites/substrata, live Lithothamnion glaciale maerl, rocky substrata with ∼95% Halidrys siliquosa cover, and gravel covered with Chorda filum from June to November. All sites were in depths of 4–7 m CD, and subject to moderate tidal flows (max: 0.29–0.45 m s −1 ). The substrata were mapped using scuba, and gadoids were sampled on five occasions between April 2002 and February 2003, with non-uniform absolute temporal differences between each successive bi-monthly survey, so avoiding temporal pseudo-replication ( Underwood, 1997 ), i.e. sampling events coinciding with behavioural cycles in the organisms being sampled.

Maerl grounds are slow-growing and easily damaged ( Hall-Spencer and Moore, 2000a ; BIOMAERL team, 2003 ; Kamenos et al ., 2003 ) and are protected under the EC Habitats Directive, so mobile gears were not used for sampling purposes. Static gear trials have shown that fykenets are successful at catching juvenile gadoids ( Nostvik and Pedersen, 1999 ). They also have the advantage of not becoming entangled in loose-lying surface maerl, which tangles gill and trammel nets within a few hours of deployment.

Eight double-ended, square-otter-guarded fykenets (mesh size: 14 mm [leader], 10 mm [net]; height: 53 cm; leader length: 6 m) were deployed by hand from a 5-m dory. Nets were deployed during daylight, and emptied and redeployed at night. Dusk and dawn are here defined as falling within the hours of night/darkness. All nets were deployed with the same orientation, placing the leader perpendicular to the tidal flow and >150 m from the nearest net. Each of the five sampling periods lasted for 4 days, during which 12× night and 8× daylight samples were obtained from maerl and gravel, and 9× night and 6× daylight samples from rock. After each day/night cycle, nets were moved to another site/substratum to minimize net effects. Catch number and species, and length measurements were recorded each time the nets were hauled. All fish were retained for further analysis. Larger size classes of gadoid stomach content were determined as described in Bowen (1996) within 1 h of the fish being caught.

Additionally, visual estimates of gadoid numbers were made using scuba. Transects were swum by two divers at 9–10 m min −1 for 5 min (n varied between 7 and 21). All transects were surveyed at slack water (±2 h) to minimize current effects on the divers' swimming distances, and in randomly selected directions. Shoals, or individual fish, observed crossing or in a strip 2-m wide were recorded along each 50-m transect (transect volume = 100 m 3 ). At the size/age at which fish or shoals (e.g. cod) were observed, they do not exhibit territoriality ( Tupper and Boutilier, 1995b ), so the same fish or shoal may have been encountered more than once on the same transect.

2.1 Data analysis

Fykenet catches were adjusted to catch h −1 assuming a linear relationship, because catch rate relationships only become non-linear after extended (>1 day) net deployment ( Austin, 1977 ; Hamley and Howley, 1985 ; Nostvik and Pedersen, 1999 ).

Total numbers of juvenile and larger size class gadoids caught during each sampling session were compared using multiple comparison Kruskal–Wallis tests. Reciprocally (x′=1/(x+0.5)) transformed (to fit parametric assumptions) juvenile catch data from September–November were analysed as a repeated measure ANCOVA because, although the nets were deployed in different locations during each repetitive sample, and gadoids are highly mobile, the size of the population was not known. Therefore, depletion may have been taking place during the sampling period (i.e. successive days during the 4-day sampling session). Numbers of fish of larger size classes in each net were used as a covariate, because adult and larger conspecific presence affects juvenile abundance either through predation or local juvenile avoidance ( Helfman, 1989 ; Rangeley and Kramer, 1998 ). Post hoc comparisons were investigated with a Tukey test. Univariate comparisons of catch composition within each substratum/diel period were made using six a priori multiple comparison Kruskal–Wallis tests with Dunn–Šidák adjusted p values. Additionally, an individual Kruskal–Wallis test was used to compare the numbers of larger size classes of gadoids during each diel period.

Although there were only a few species and size classes of fish present, multivariate analyses were used to aid in the differentiation of species/size compositions associated with each substratum and month. Multivariate analyses were performed using PRIMER ® ( Clarke and Warwick, 1994 ; Clarke and Gorley, 2001 ). Multivariate data analysis was by non-metric multi-dimensional scaling ordination (MDS), using the Bray–Curtis similarity matrix. Analyses used untransformed data, because only a few species/size combinations were present. Two-way crossed pairwise analyses of similarity (ANOSIMs) (assumptions met), were carried out to test for significant differences in assemblage composition between substrata. Similarity percentage (SIMPER) analyses were used to examine the contribution of individual species towards the dissimilarity between the different substrata. This analysis was selected because the samples were in well-defined groups (substrata), and not described by more continuous distributions. SIMPER analysis also examined the contribution each species made to the average similarity within a group.

3 Results

3.1 Temporal abundance

Juvenile gadoids (<12 cm (the upper size limit of juveniles caught)) were found at Caol Scotnish during all months sampled. However, there were significantly bigger catch rates in September and November, which did not differ significantly from each other (H 4 =32.30, p>0.0001; Figure 1 ). Visual observations using scuba also indicated increased numbers of juvenile gadoids during the period September–November, with highest densities over maerl and rocky substrata ( Figure 2 ).

Figure 1

Mean number of juvenile gadoids (<12 cm) caught per hour at Caol Scotnish (data combined for maerl, rocky, and gravel substrata) using fykenets at bi-monthly sampling events. Error bars = s.d. Horizontal lines at the same level indicate substrata that did not differ significantly from each other.

Figure 1

Mean number of juvenile gadoids (<12 cm) caught per hour at Caol Scotnish (data combined for maerl, rocky, and gravel substrata) using fykenets at bi-monthly sampling events. Error bars = s.d. Horizontal lines at the same level indicate substrata that did not differ significantly from each other.

Figure 2

Mean number of juvenile gadoids observed associated with maerl, gravel, and rocky substrata in Caol Scotnish using scuba during bi-monthly sampling events. Error bars = s.d. Straight lines do not indicate linear progressions between data points, but are given to aid trend determination.

Figure 2

Mean number of juvenile gadoids observed associated with maerl, gravel, and rocky substrata in Caol Scotnish using scuba during bi-monthly sampling events. Error bars = s.d. Straight lines do not indicate linear progressions between data points, but are given to aid trend determination.

Large size class fish (all cod, >32 cm, the lower size limit of large size class fish caught) were present only from May to November, and were significantly more numerous in September than in all months other than November (H 4 =15.07, p=0.005; Figure 3 ). All larger size class cod had empty stomachs. Further analysis was therefore concentrated on the period September–November, which appears to be the period when juvenile gadoids utilize the shallow waters of Loch Sween.

Figure 3

Mean number of gadoids of the larger size classes (>32 cm) caught per hour at Caol Scotnish (data combined for maerl, rocky, and gravel substrata) using fykenets at bi-monthly sampling events. Error bars = s.d. Horizontal lines at the same level indicate substrata that did not differ significantly from each other.

Figure 3

Mean number of gadoids of the larger size classes (>32 cm) caught per hour at Caol Scotnish (data combined for maerl, rocky, and gravel substrata) using fykenets at bi-monthly sampling events. Error bars = s.d. Horizontal lines at the same level indicate substrata that did not differ significantly from each other.

3.2 Juvenile density, September–November

Interaction effects between substratum and diel period were not significant (F 2 =2.78, p=0.068). Significantly more juvenile gadoids were caught over maerl than over rock and gravel, and significantly more over rock than over gravel (F 2 =35.41, p<0.0001; Figure 4 ). Significantly more juvenile gadoids were caught during daylight than during darkness (F 1 =15.42, p<0.0001; Figure 4 ). The presence of larger gadoids had no effect on the numbers of juvenile gadoids caught (F 1 =3.45, p=0.067). Gadoids of the larger size classes were caught over rocky and gravel areas only during daylight, and over maerl and rock only at night during the period September–November. Similar numbers of gadoids in the larger size classes were caught during both diel periods (H 1 =4.14, p=0.127; Figure 5 ).

Figure 4

Mean number of juvenile gadoids (<12 cm) caught over maerl, rock, and gravel using fykenets by day and by night, September–November. Error bars = 95% C.I.

Figure 4

Mean number of juvenile gadoids (<12 cm) caught over maerl, rock, and gravel using fykenets by day and by night, September–November. Error bars = 95% C.I.

Figure 5

Mean number of gadoids of the larger size classes (>32 cm) caught over maerl, rock, and gravel using fykenets by day and by night, September–November. Error bars = s.d.

Figure 5

Mean number of gadoids of the larger size classes (>32 cm) caught over maerl, rock, and gravel using fykenets by day and by night, September–November. Error bars = s.d.

Similar numbers of juvenile cod, saithe, and pollack were caught over each substratum during each diel period (H 2 all <6.46, p all >0.0085; the Dunn–Šidák adjusted p value) apart from significantly more juvenile pollack than cod or saithe over maerl by day (H 2 =15.92, p<0.0001; Figure 6 ).

Figure 6

Mean number of juvenile cod, saithe, and pollack (<12 cm) caught over maerl, rock, and gravel using fykenets by day and by night, September–November. Error bars = s.d. Horizontal lines indicate fish densities that did not differ significantly within each substratum/diel period group.

Figure 6

Mean number of juvenile cod, saithe, and pollack (<12 cm) caught over maerl, rock, and gravel using fykenets by day and by night, September–November. Error bars = s.d. Horizontal lines indicate fish densities that did not differ significantly within each substratum/diel period group.

3.3 Community structure

Significant differences in assemblage composition associated with substrata (global R=0.24, p=0.001) and month (global R=0.234, p=0.001) were detected with a two-way crossed ANOSIM. Pairwise comparisons indicated “gravel and maerl” and “rock and maerl” assemblages to be slightly separable (R>0.25), whereas “gravel and rock” assemblages were indistinguishable (R<0.25; Table 1 ). No 2 months had well-separated (R>0.75) assemblage compositions, though “May and January” and “July and January” had overlapping but clearly different assemblage composition (R>0.5). “May and July”, “May and September”, “May and November”, “July and November”, “July and September”, and “September and January” were all slightly separable (R>0.25), whereas “September and November”, and “November and January” were not separable (R<0.25) in terms of assemblage composition ( Table 1 ).

Table 1

Pairwise comparisons of untransformed month and substratum pairs using a two-way crossed ANOSIM (analysis of similarity). Where R significance ∼ 0, the null hypothesis is accepted and the compared assemblages are indistinguishable; where R=1, similarities within substrata (all replicates) are greater than any similarities between substrata.

Pairwise comparison R significance statistic R significance level (%) 
Gravel and maerl 0.312 0.1 
Gravel and rock 0.015 34.6 
Maerl and rock 0.272 0.1 
May and July 0.283 1.3 
May and September 0.375 0.2 
May and November 0.240 0.5 
May and January 0.500 0.2 
July and September 0.215 0.6 
July and November 0.325 0.1 
July and January 0.566 0.1 
September and November 0.011 37.5 
September and January 0.258 0.6 
November and January 0.139 3.3 
Pairwise comparison R significance statistic R significance level (%) 
Gravel and maerl 0.312 0.1 
Gravel and rock 0.015 34.6 
Maerl and rock 0.272 0.1 
May and July 0.283 1.3 
May and September 0.375 0.2 
May and November 0.240 0.5 
May and January 0.500 0.2 
July and September 0.215 0.6 
July and November 0.325 0.1 
July and January 0.566 0.1 
September and November 0.011 37.5 
September and January 0.258 0.6 
November and January 0.139 3.3 

As indicated by the low global R statistic (ANOSIM), no substrata were typified by any particular species or age group. However, maerl and gravel were discriminated from each other (1.13 (dissimilarity/s.d.)) by higher abundances of juvenile pollack on maerl (0.18 (average abundance)) than on gravel (0.02), and similarly maerl and rock were discriminated (1.09) by higher abundances of juvenile pollack on maerl (0.18) than on rock (0.05).

Only May could be typified by great abundance (0.09) of juvenile cod (1.94 (similarity/s.d.)). All other months were not typified by any particular species or size class. Abundances of juvenile cod in May (0.09 (average abundance)) contributed to its dissimilarity with September (0.06, 1.17 (average abundance, dissimilarity/s.d.)), and January (0.04, 1.77). High densities of juvenile pollack in January (0.08) contributed to its dissimilarity with May (0.00, 1.45) and July (0.00, 1.26), and high densities in September (0.18) contributed to its dissimilarity with January (0.08, 1.43). Enhanced abundance of saithe in July (0.13) contributed to its dissimilarity with November (0.11, 1.05) and January (0.03, 1.07).

4 Discussion

Gadoid densities were highest in Caol Scotnish during late summer and autumn. Recruitment of post-settlement juvenile gadoids to shallow inshore waters is well documented ( Carr, 1991 ; Gibson et al ., 1996 ; Pihl and Wennhage, 2002 ), and to a lesser extent seasonal migrations of larger fish into the shallows ( Pihl and Wennhage, 2002 ), probably in search of food, does take place. Although our fykenet catches were quite low during the period of high density of juveniles (owing to the static nature of the gear and the use of otter guards, that reduce catch rates; Jeffries et al ., 1984, 1988), direct observations confirmed abundant juvenile fish (up to 201 juvenile gadoids 100 m −3 ). High variability associated with these observations was most likely attributable to the non-territoriality, high mobility, shoaling, and diver-avoidance behaviour of the species being monitored.

Juvenile gadoids were in greater densities over maerl than over heavily vegetated rock and gravel substrata. As juveniles were caught on all substrata it is possible that, considering the static nature of the sampling gear, they were less active while in vegetated areas, possibly seeking refuge, and actively foraging while over the less heterogeneous substrata ( Eklov and Persson, 1996 ), such as the macroalgae-devoid maerl, so increasing their catchability. Unlike the current findings, a comparison of coralline algal sites, so-called “barrens”, with dense macroalgal stands in Newfoundland by Keats et al . (1987) , revealed significantly more 1- and 2-group cod in fleshy macroalgal beds ( Desmarestia sp.) than on barrens (all 8–10 m CD) surveyed using scuba. Those authors concluded that the juvenile cod were using the macroalgal stands for protection.

During the period September–November, significantly more juvenile gadoids were present by day than by night over maerl, whereas numbers remained lower over rock and gravel by both day and night. Perhaps the juveniles were more active, probably foraging, during daylight (i.e. increasing their catchability) than at night in the shallow waters of Loch Sween. However, Methven and Schneider (1998) observed more juvenile cod in shallow water by night than by day, which they considered as being either to feed or to avoid predation. It is unlikely that fish caught by day were migrating to or from deeper water, because juvenile gadoids make such migrations at dusk and dawn ( Methven and Schneider, 1998 ; Pihl and Wennhage, 2002 ), both of which periods are here defined as night/darkness.

The numbers of juveniles on each substratum and diel period were not affected by the presence of larger, predatory gadoids, nor did the numbers of gadoids of larger size class differ between diel periods. This was unexpected, because juvenile cod avoid predators and larger conspecifics ( Methven and Schneider, 1998 ). It is possible, therefore, that the densities of larger size classes were so low that impacts on juvenile distributions remained very localized and were not picked up by our sampling regime, that juveniles and larger size classes were temporally segregated within each sampling session, so we could not determine the presence of any relationships, and that the otter guards we used only allowed capture of the smallest of the large size classes of gadoids. Although we found no effect of predator presence on juvenile densities (possibly an artefact of the sampling technique), higher densities of larger size class individuals (i.e. potential predators) occurred at night on maerl during late summer and early autumn, supporting our suggestion that juvenile gadoids do prefer to forage in daylight over maerl.

Olsen and Soldal (1989) observed that the so-called holding capacity of coastal locations suitable for 0-group cod is most likely restricted primarily by food capacity. Therefore, considering the high organic biomass (e.g. polychaetes) associated with maerl grounds than the other substrata ( BIOMAERL team, 1999 , 2003 ), and that juvenile gadoids do forage over maerl grounds (through unpublished stomach content analysis), such grounds may provide higher holding capacities of juvenile gadoids per unit area than the sand and gravel areas traditionally associated with foraging juvenile gadoids such as pollack ( Rangeley and Kramer, 1998 ). Gadoids that forage on gravel exhibit better survival, partly because of greater food availability ( Lough et al ., 1989 ), because survival of overwintering young-of-year fish is generally higher in larger fish, and the rapid growth of newly settled individuals is physiologically and ecologically selectively advantageous in terms of lowering predation risk ( Walsh, 1987 ). Maerl grounds may therefore increase such survival further.

Nursery areas are defined by their high population densities of juveniles, fast somatic growth rates, and characteristically good survival, as well as by their ability to supply recruits to adult populations ( Beck et al ., 2001 ). Considering our findings and the difficulty of testing recruitment success, we conclude that juvenile gadoids are using Caol Scotnish as a nursery area during late summer and autumn, partly sustained by the abundant food biomass of the live maerl matrix.

No months had well-separated gadoid assemblages, though May was typified by abundance of juvenile cod, probably the previous year's late-spawned cohort. Of note, though, was the sequential appearance of other gadoid juveniles around and during the months of greater juvenile density, with abundance of saithe in July followed by similar abundance of pollack from September to January. This separation was likely coincidental, because juvenile cod were present from July to January. However, it may demonstrate temporal niche separation of nursery area usage by the different species within the gadoid guild, to reduce interspecific competition for food and/or refugia. Although site-specific, juvenile (5–15 cm) saithe and pollack utilize similar benthopelagic food sources, which differ from those utilized by the more benthic-tending cod ( Bromley et al ., 1997 ; Høines and Bergstad, 1999 ), allowing cod, and either saithe or pollack, to co-exist. Older saithe and pollack have less dietary overlap ( Sarno et al ., 1994 ). Unlike the current result, Pihl and Wennhage (2002) demonstrated clear separation of fish assemblages during summer, when considering 25 adult and juvenile fish species, including gadoids.

Densities of juvenile pollack were greatest over maerl than were those of other gadoids. Of course, this may indicate increased catchability of pollack by fykenets when foraging over maerl during daylight, and/or lesser catchability at night when in vegetated areas. It is therefore possible that pollack are less active nocturnally than other juvenile gadoids, or that they are more active foragers than other species during daylight, so increasing their catchability by static fykenets. However, adult pollack are less active foragers than adult saithe ( Sarno et al ., 1994 ).

We conclude that maerl grounds may increase the holding capacity of localized inshore shallow-water nursery areas, with gadoids consistently preferring to forage over maerl than over gravel, despite the extra vegetative cover provided by the latter (at least in Caol Scotnish). Considering that anthropogenic damage can kill maerl and reduce its heterogeneity to areas resembling a gravel substratum ( Hall-Spencer and Moore, 2000a ; Kamenos et al ., 2003 ), it is clear that if maerl areas are helping to increase the localized juvenile gadoid holding capacities of inshore waters, destruction of such habitats may lead to significant reduction of the holding capacity of inshore areas.

Scottish Natural Heritage contributed to funding this research, NAK received a Sheina Marshall studentship from the University Marine Biological Station Millport, and JMH-S was funded by the Royal Society. Thanks are due also to Kenny Cameron, Stephen Muir, Martin Sayer, and Roger Coggan for sampling help and advice, and two anonymous reviewers for constructive suggestions.

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Author notes

1
Present address for J. M. Hall-Spencer: Marine Biology and Ecology Research Group, Department of Biological Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, England, UK.