Trawling is known to disturb benthic communities and habitats, which may in turn indirectly affect populations of commercial species that live in close association with the seabed. The degree of impact on both benthic communities and demersal species depends on the fishing effort level. This may vary over the year because of the fleet dynamics, which are in turn normally driven by the main target species’ life cycle. In this study we describe changes in benthic functional components of a northwestern Mediterranean fishing ground that represents a recruitment area for an important target species (red mullet,
Se sabe que la pesca de arrastre provoca una perturbación en los hábitats y ecosistemas bentónicos, lo cual a su vez puede afectar indirectamente a las poblaciones de especies comerciales que viven en estrecha relación con el fondo marino. El nivel de impacto en las comunidades bentónicas y en las especies comerciales depende en ambos casos del nivel de esfuerzo pesquero. Este esfuerzo puede variar a lo largo del año, ya que la dinámica de la flota está normalmente determinada por el ciclo vital de las especies objetivo. En este estudio se describen cambios en los componentes funcionales del bentos de un caladero del Mediterráneo noroccidental que constituye un área de reclutamiento para una importante especie objetivo como es el salmonete de fango (
Trawling is widely held to be the human activity with the greatest impact on continental shelves all over the world (
The degree of seabed alteration and potential consequences on commercial species will depend on the intensity of the fishing effort. Therefore, it is important to understand the responses of benthic ecosystems to variations in trawling intensity. Communities vary over time and space in response to natural variability (
The effects of different levels of fishing pressure on habitats and benthic communities have been explored over spatial gradients of trawling disturbance (
The European Marine Strategy Framework Directive (EMSFD) established by the European Commission 2008 (EC2008/56) encourages Member States to move towards an ecosystem-based fisheries management (EBFM) in order to protect ecosystems goods and services that marine ecosystems provide. Consequently, it is important to take into account the link between habitat and commercial species in management in order to move towards an EBFM if the goals of the EMSFD are to be met. There are a number of interactions through which fishing activity may influence commercial species (the principal ones are depicted in
i) Production: ecosystem production is represented as a food source for demersal commercial species. Production by small infauna does not seem to be affected by high fishing intensity (
Jennings et al. 2002 ), although it can increase at moderate levels of disturbance (Jennings et al. 2001 ), which may benefit species feeding on small opportunistic fauna (Rijnsdorp and Vingerhoed 2001 ). On the other hand, production by larger infauna and epifauna would decrease in heavily trawled areas (Jennings et al. 2001 ,Hiddink et al. 2006b ,Queirós et al. 2006 ), which may result in a food impoverishment for fish. Benthic carnivorous fish consume larger prey as they grow (Lukoschek and McCormick 2001 ), so a decrease in larger infauna might principally affect adult populations and the most economically important components of the stock (Fanelli et al. 2010 ). Another important food source for several demersal species, especially during the juvenile phase, is suprabenthos, whose abundance and biomass could also be affected by trawling (de Juan et al. 2007a ,Fanelli et al. 2011 ).ii) Habitat structure: important negative consequences of trawl fishing activity have also been described at the benthic habitat level. Habitat structure that provides shelter and favours the establishment of spawning and nursery habitats may also be altered as trawling activity is known to homogenize habitat structure (
Jennings and Kaiser 1998 ,Thrush et al. 2001 ).iii) Species interactions: changes observed in trawled areas, such as changes in epifaunal composition, might also affect commercial species as some epifaunal species compete with commercial fish for food. The epifaunal size decrease caused by trawling (
de Juan et al. 2007b ) might actually benefit commercial species by releasing them from large potential competitors, but the increase in predator and scavenging species (Rumohr and Kujawski 2000 ) could increase the food competition.
Current management strategies of the Mediterranean trawl fisheries imply effort limitation (temporal and spatial closed areas, engine power limitation, licence controls, etc.) and technical measures (minimum landing sizes, mesh size, etc.) (
Mediterranean trawl fisheries are characterized by seasonal dynamics which are mainly driven by the life cycle of the main target species (
One of the main demersal commercial species in the study area, a trawl fishing ground in the northwestern Mediterranean, is red mullet (
In the study area, fishing effects on benthic communities were assessed by characterizing it as a chronically impacted seabed (
With the aim of advancing on EBFM approaches, taking into account all the effects depicted in
i) changes in benthic production will affect red mullet’s food provision;
ii) homogenization of habitat structure affects both nursery and spawning habitat for red mullet’s, and
iii) changes in epifaunal assemblage composition affect interspecific competition between epifaunal species and red mullet.
The study was conducted on a muddy fishing ground located in the northwestern Mediterranean. This fishing ground spreads over 400 km2 in a depth range between 30 and 80 m, and the study area covers a depth range of 40-60 m (
Cruise | 27 to 30 June 2003 | 14 to 17 July 2003 | 28 to 31 July 2003 | 19 to 22 August 2003 | 26 to 29 September 2003 | 17 to 17 November 2003 | 18 to 21 June 2004 | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Site | C | F | C | F | C | F | C | F | C | F | C | F | C | F |
Turbidity (mg/l) | 1.48 | 2.38 | 1.65 | 1.37 | 1.25 | 2.66 | 1.13 | 1.72 | 4.57 | 5.76 | 3.27 | 8.11 | 1.89 | 2.88 |
% OM | 0.55 | 0.59 | 0.48 | 0.59 | 0.54 | 0.64 | 0.63 | 0.70 | 0.61 | 0.68 | 0.51 | 0.63 | 0.52 | 0.61 |
%Mud | 99.5 | 99.59 | 99.48 | 99.46 | 99.23 | 99.52 | 99.29 | 99.47 | 99.38 | 99.43 | 99.33 | 99.5 | 99.33 | 99.51 |
D50 (mm) | 2.65 | 4.53 | 2.73 | 4.58 | 2.68 | 4.41 | 2.67 | 4.55 | 2.82 | 4.78 | 2.75 | 4.82 | 2.75 | 4.67 |
Effort level | - | Low | - | Closed | - | Closed | - | Closed | - | High | - | High | - | Low |
Samples of epifauna and infauna were collected during seven experimental cruises. Epifauna was collected with a surface dredge, similar to a 2 m beam-trawl with a 1-cm cod-end, and infauna with a 0.1-m2 Van Veen grab. On each cruise, a total of three epifaunal and five infaunal replicates were randomly collected at both fished and control sites. To collect the minimum sample size, estimated from species accumulation curves, the surface dredge was towed for approximately 15 minutes for each replicate and five grabs were collected per replicate. Epifaunal and infaunal organisms were identified to the lowest possible taxonomical level, generally species for epifauna and genera for infauna, and counted (see
Data on landings and income from 2000 to 2011 were obtained from records from the local fish auction that takes place upon the arrival of vessels at port (data source: fishing statistics elaborated by the Fisheries Department of the Catalan government). Data were available on daily landings by species (weight and income) for each fishing vessel.
Trait classification to characterize benthic communities
Eleven biological traits covering aspects of the benthic organisms’ morphology, feeding patterns and life histories were selected to represent benthic community. The biological trait approach (BTA) allows community structure and functionality to be better represented in order to link them to the ecosystem services that the community can provide. In our case, a benthic ecosystem from a fishing ground, one of the main ecosystem services that this community provides is food production.
These 11 traits were broken down into categories. For example, feeding type was separated into the categories deposit feeder, filter/suspension feeder, opportunist/scavenger and predator (
Trait | Categories |
---|---|
Feeding behaviour | Deposit feeders |
Filter/suspension feeders | |
Opportunistic/scavengers | |
Predators | |
Food type | Invertebrates |
Carrion | |
Detritus | |
Plankton | |
Microorganisms | |
Nekton | |
Fragility | Fragile |
Intermediate | |
Robust | |
Living habit | Tube dweller |
Permanent burrow dweller | |
Free-living | |
Size | Very small <1 cm |
Small 1-2 cm | |
Small-medium 3-10 cm | |
Medium 11-20 cm | |
Medium-large 21-50 cm | |
Flexibility | None <10 degrees |
Low 10-15 degrees | |
High >45 degrees | |
Life span | <1 y |
1-2 y | |
3-5 y | |
>5 y | |
Age at sexual maturity | < 1 y (i)/ ≤1 y (e) |
≥ 1 y (i)/> 1 y (e) | |
Adult movement | Sessile |
Crawl | |
Swim | |
Burrow | |
Reproduction frequency | Continuous |
1 reproductive event per year | |
2 or more reproductive events per year | |
Less than annual | |
Type of larvae | Direct development |
Short planktonic (<1 week) | |
Long planktonic (>1 week) |
Each taxon in the database was scored for its affinity to each trait category using a scale of 0–3 (0 = no affinity to 3 = high affinity). The score was given using the ‘fuzzy scoring’ method, which allowed the taxa to exhibit more than one category of a given trait as long as the total score per trait was 3 (
The frequency of each trait category in the dataset was calculated by weighting the category scores by the abundance (number of individuals per m2) of each taxon exhibiting that category (
Similarity between each pair of samples was calculated using the Bray-Curtis index after a square root transformation of the data to reduce the influence of dominant traits/species. A PERMANOVA analysis was used to test for significant differences between sites (control and fished as fixed factors) and time (fishing effort periods, i.e. before, during and after closure, as fixed factor). The trait data were further analysed with the SIMPER routine to determine which traits accounted for the significant dissimilarities identified by PERMANOVA. Then, the most important traits highlighted by SIMPER (traits showing ratio of dissimilarity to standard deviation [diss/sd] >1.5 and being among the ones summing 50% of cumulative contribution to dissimilarity) were selected for univariate analyses. When traits had a normal distribution and homogeneity of variances, a two-way ANOVA was performed to test for the factors treatment and effort period. If traits were not normally distributed (even after log transformation), a Kruskall-Wallis test was performed instead. All the multivariate analyses were carried out using the PRIMER6 & PERMANOVA statistical package (
Despite an overall decrease since 2007, red mullet landings consistently followed the same trend, with a peak of catches in September/October (the recruitment months for this species), which accounted for almost 20% of the total landings (
PERMANOVA analyses highlighted significant differences for both infauna and epifauna between sites (control vs. fished) and time (different effort regimes), and site:time interaction for infauna (
INFAUNA | df | MS | Pseudo F | p-value |
---|---|---|---|---|
Time | 2 | 158.56 | 3.87 | 0.008 |
Site | 1 | 1199.40 | 29.33 | 0.001 |
Time:site | 2 | 246.35 | 6.02 | 0.003 |
EPIFAUNA | df | MS | Pseudo F | p-value |
Time | 2 | 460.56 | 5.70 | 0.002 |
Site | 1 | 474.93 | 5.88 | 0.006 |
Time:site | 2 | 83.05 | 1.03 | 0.354 |
SIMPER analysis for infaunal samples highlighted the traits "sexual maturity at less than 1 year" and "life span of less than 1 year" as the principal traits driving the differences between fished and control sites, both being more abundant in the control site. "Medium-large size" (more prevalent at the fished site) was also an important trait discriminating sites (
FISHED vs CONTROL (Average dissimilarity=12.64) | |||||
---|---|---|---|---|---|
Traits | Ab. Fished | Ab. Control | Diss/sd | Contrib % | Cum. Contrib % |
<1 y (sex. mat) | 24.29 | 36.98 | 1.61 | 5.44 | 5.44 |
<1 y (life span) | 24.05 | 34.90 | 1.50 | 4.77 | 10.21 |
High flexibility | 41.92 | 47.32 | 1.38 | 4.31 | 14.52 |
Direct development | 32.34 | 39.36 | 1.45 | 4.15 | 18.67 |
Medium-large | 21.47 | 12.13 | 2.90 | 4.09 | 22.76 |
Continuous reproduction | 25.73 | 31.67 | 1.46 | 3.96 | 26.69 |
Tube dweller | 18.15 | 26.10 | 1.50 | 3.62 | 30.31 |
Permanent burrow dweller | 24.25 | 31.70 | 1.54 | 3.49 | 33.82 |
Detritus | 41.44 | 46.80 | 1.38 | 3.51 | 37.30 |
Filter feeder | 20.47 | 27.95 | 1.51 | 3.45 | 40.75 |
Small size | 21.33 | 28.89 | 1.51 | 3.28 | 44.03 |
Burrow | 44.44 | 48.03 | 1.33 | 3.25 | 47.28 |
Small-medium size | 31.28 | 35.20 | 1.40 | 3.24 | 50.51 |
BEFORE vs CLOSED (Average dissimilarity=10.03) | |||||
Traits | Ab. Before | Ab. Closed | Diss/sd | Contrib % | Cum. Contrib % |
High flexibility | 40.13 | 45.89 | 1.54 | 4.29 | 4.29 |
Intermediate fragility | 40.88 | 46.93 | 1.56 | 4.18 | 8.47 |
<1 y (sex. mat.) | 21.93 | 28.21 | 1.57 | 3.86 | 12.33 |
Burrow | 42.51 | 46.73 | 1.43 | 3.85 | 16.18 |
1 repr. event/year | 35.39 | 41.18 | 1.46 | 3.72 | 19.90 |
Direct development | 30.35 | 35.67 | 1.42 | 3.69 | 23.59 |
Detritus | 39.49 | 43.93 | 1.40 | 3.61 | 27.20 |
<1 y (life span) | 22.42 | 27.92 | 1.41 | 3.52 | 30.72 |
Deposit feeder | 37.95 | 42.12 | 1.40 | 3.33 | 34.04 |
2+repr. events/y | 3.37 | 8.94 | 1.76 | 3.26 | 37.30 |
Filter feeder | 17.72 | 23.27 | 1.70 | 3.15 | 40.45 |
Free-living | 33.90 | 37.92 | 1.47 | 3.14 | 43.60 |
Small-medium size | 30.61 | 33.56 | 1.43 | 3.07 | 46.66 |
very small size | 18.38 | 22.17 | 1.08 | 3.03 | 49.69 |
BEFORE vs AFTER (Average dissimilarity=8.65) | |||||
Traits | Ab. Before | Ab. After | Diss/sd | Contrib % | Cum. Contrib % |
High flexibility | 40.13 | 45.97 | 1.46 | 4.62 | 4.62 |
Intermediate fragility | 40.88 | 46.56 | 1.43 | 4.12 | 8.73 |
Burrow | 42.51 | 46.61 | 1.44 | 3.86 | 12.59 |
Direct development | 30.35 | 35.28 | 1.44 | 3.84 | 16.43 |
Detritus | 39.49 | 43.83 | 1.42 | 3.81 | 20.23 |
small-medium size | 30.61 | 34.40 | 1.47 | 3.70 | 23.93 |
Crawl | 9.56 | 15.01 | 1.78 | 3.66 | 27.59 |
Deposit feeder | 37.95 | 42.40 | 1.40 | 3.61 | 31.20 |
1 repr. event/y | 35.39 | 40.27 | 1.48 | 3.48 | 34.68 |
<1 y (sex. mat.) | 21.93 | 25.81 | 1.37 | 3.34 | 38.02 |
Filter feeder | 17.72 | 22.52 | 1.56 | 3.27 | 41.29 |
Continuous reproduction | 25.00 | 28.18 | 1.39 | 2.97 | 44.26 |
Long planktonic | 16.69 | 20.28 | 1.44 | 2.88 | 47.15 |
Free-living | 33.90 | 37.53 | 1.38 | 2.86 | 50.01 |
SIMPER analysis performed only for infaunal fished samples revealed "high flexibility", "intermediate fragility" and "<1 y sexual maturity" as the main traits driving the differences between before closure and closed season periods, although they showed relatively low diss/sd (
The SIMPER routine for epifaunal samples highlighted the traits "medium", ">5 y life span", "low flexibility" and "medium-large" as the most important traits driving the differences between control and fished sites, all of them being more abundant at the control site (
FISHED vs CONTROL (Average dissimilarity=12.98) | |||||
---|---|---|---|---|---|
Traits | Ab. Fished | Ab. Control | Diss/sd | Contrib % | Cum. Contrib % |
High flexibility | 15.10 | 13.11 | 1.26 | 4.43 | 4.43 |
Medium size | 1.09 | 5.00 | 2.37 | 4.42 | 8.85 |
3-5 y (life span) | 15.13 | 13.81 | 1.24 | 4.29 | 13.14 |
>1 y (sex.mat) | 15.40 | 15.37 | 1.25 | 4.18 | 17.32 |
Crawl | 17.48 | 15.86 | 1.25 | 3.93 | 21.25 |
Intermediate fragility | 19.10 | 19.49 | 1.36 | 3.81 | 25.07 |
>5 y (life span) | 5.59 | 8.83 | 1.68 | 3.8 | 28.86 |
1 repr. event/year | 20.05 | 20.37 | 1.35 | 3.73 | 32.60 |
Long planktonic | 19.42 | 19.61 | 1.37 | 3.71 | 36.31 |
Small-medium size | 19.77 | 18.55 | 1.29 | 3.69 | 40.00 |
Free-living | 18.06 | 18.47 | 1.43 | 3.67 | 43.67 |
Low flexibility | 5.41 | 8.22 | 1.66 | 3.42 | 47.09 |
Medium-large size | 3.80 | 6.57 | 1.72 | 3.23 | 50.32 |
BEFORE vs AFTER (Average dissimilarity = 16.33) | |||||
Traits | Ab. Before | Ab. After | Diss/sd | Contrib % | Cum. Contrib % |
No flexibility | 15.46 | 9.15 | 2.16 | 6.16 | 6.16 |
3-5 y (life span) | 13.01 | 15.00 | 1.36 | 4.71 | 10.87 |
>1 y (sex. mat) | 14.10 | 15.53 | 1.37 | 4.68 | 15.54 |
High >45 | 12.91 | 14.61 | 1.40 | 4.45 | 19.99 |
Intermediate fragility | 19.96 | 17.43 | 1.45 | 3.97 | 23.97 |
Deposit feeder | 9.99 | 6.03 | 2.11 | 3.95 | 27.92 |
Permanent burrow dweller | 11.30 | 7.35 | 1.68 | 3.94 | 31.86 |
1 repr. event/y | 20.98 | 17.93 | 1.44 | 3.94 | 35.80 |
Long planktonic | 20.27 | 17.40 | 1.43 | 3.92 | 39.72 |
Burrow | 9.93 | 5.90 | 2.06 | 3.9 | 43.62 |
Detritus | 10.30 | 6.36 | 2.03 | 3.89 | 47.51 |
Small-medium size | 20.01 | 16.99 | 1.35 | 3.72 | 51.23 |
CLOSED vs AFTER (Average dissimilarity = 13.83) | |||||
Traits | Ab. Close | Ab. After | Diss/sd | Contrib % | Cum. Contrib % |
No flexibility | 14.48 | 9.15 | 2.10 | 6.00 | 6.00 |
1 repr. event /y | 21.21 | 17.93 | 1.44 | 4.40 | 10.40 |
Long planktonic | 20.43 | 17.40 | 1.42 | 4.25 | 14.65 |
Small-medium size | 20.04 | 16.99 | 1.44 | 4.16 | 18.80 |
Permanent burrow dweller | 10.92 | 7.35 | 1.82 | 4.11 | 22.91 |
Intermediate fragility | 20.10 | 17.43 | 1.40 | 4.08 | 27.00 |
Deposit feeder | 9.54 | 6.03 | 2.07 | 4.01 | 31.00 |
Detritus | 9.81 | 6.36 | 2.08 | 3.99 | 34.99 |
Burrow | 9.33 | 5.90 | 2.08 | 3.86 | 38.85 |
Fragile | 7.12 | 3.94 | 1.80 | 3.84 | 42.69 |
Free-living | 19.07 | 16.85 | 1.39 | 3.61 | 46.29 |
Crawl | 17.27 | 15.84 | 1.42 | 3.29 | 49.58 |
Though these traits were highlighted by SIMPER analysis, it should be noted that average dissimilarities among fishing effort periods were low (10.03 and 8.65 for infauna and 16.33 and 13.83 for epifauna) (
Infauna | Site | Time | Site: time |
---|---|---|---|
<1 y (life span) | *** | ns | * |
<1 y (sex.mat) | *** | ns | * |
Medium-large size | *** | ns | ns |
Tube dweller | *** | ns | * |
Permanent burrow dweller | *** | ns | ** |
Intermediate fragility | ns | * (c≠a, b) | * |
High flexibility | * | ns | * |
Filter/suspension feeder | *** | ns | * |
Crawl | * | * (b≠a, c) | ns |
2+ repr. events/y | *** | *1 | * |
Epifauna | Site | Time | Site: time |
Deposit feeder | ns | * (a≠b, c) | ns |
Detritus | ns | * (a≠b, c) | ns |
Burrow | ns | * (a≠b, c) | ns |
No flexibility | ns | * (a≠b, c) | ns |
Permanent burrow dweller | ns | *** (a≠b, c) | ns |
Fragile | ns | ***all times | ns |
Medium size | *** | ns | * |
Medium- large size | *** | ns | * |
Low flexibility | *** | ns | * |
>5 y (life span) | ** | ns | ns |
Different fish species have different habitats requirements, which could be more or less resilient to trawling impacts (
As red mullet lives in a close relationship with the benthic environment for feeding, reproduction and refuge, this species might be particularly affected by the chronic alteration of benthic ecosystems (
Regarding the food availability, small, short-lived infaunal organisms were more abundant at the control site, which might contribute to higher food production for red mullet in this site, especially for young recruits that feed on smaller prey (
Some of the observed trends in infaunal traits over the study period matched the fishing effort pattern, but the variability in infaunal abundance would more likely be related to seasonal patterns as the closed season in the fishing ground is too short to allow ecosystem recovery (
In the epifaunal community, as expected and in agreement with
Regarding the habitat structure, as the control site is slightly deeper than the fished site, it might be a spawning area for red mullet. However, no traits related to habitat structure (e.g. sessile emerging epifauna) were highlighted in the analysis. In general, the whole fishing ground holds a homogenized community with a reduced habitat structure due to historical trawling disturbance in the area (
Associating demersal fish with their habitats is very critical to the definition of EFH and to correctly managing those EFH impacted by trawling activities (
Red mullet are an important commercial species in the Mediterranean, being one of the main target species for trawling fleets (
This work shows that changes in the effort regime within a year only had limited consequences for benthic community structure, whereas changes between a non-fished control site and a fished site were clearly evident. The observed changes at the fished site might benefit adult red mullet, as their food provision will be higher due to an increase in medium-large infauna and to lower interspecific trophic competition. However, red mullet recruits will be negatively affected by functional changes caused by fishing as their food provision might overall decrease, although they could benefit from a short-term increase in food production during summer. Moreover, both adults and recruits will suffer from lack of protection of habitat structures. Thus, the overall effect of trawling on the red mullet stock, considering the high fishing pressure on recruits and the indirect negative effects caused by ecosystem disturbance, could be a decrease in the spawning stock that will worsen the recruit's stock situation.
This study highlights the idea that permanent closure areas, which would allow recovery of the benthic ecosystem, restructuring habitats and communities, might be more beneficial for commercial species and their habitats than temporary closures.
This study was funded by the EU project RESPONSE (Q5RS-2002-00787) and the COMSOM project (CTM2008-04617). We thank the participants in the "Veda" cruises and the crew of the RV