Geographic and bathymetric trends in abundance, biomass and body size of four grenadier fishes along the Iberian coast in the western Mediterranean

Progress in Oceanography 72 (2007) 63–83

Progress inOceanography

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Geographic and bathymetric trends in abundance, biomassand body size of four grenadier fishes along the Iberian coast

in the western Mediterranean

Joan Moranta a,*, Enric Massutı a, Miquel Palmer b, John D.M. Gordon c

a IEO – Centre Oceanografic de les Balears, P.O. Box 291, 07015 Palma de Mallorca, Spainb UIB – CSIC Institut Mediterrani d’Estudis avancats, Miquel Marques 21, 07190 Esporles, Spain

c Scottish Association for Marine Science, Dunstaffnage Marine Laboratory, Oban, Scotland PA37 1QA, United Kingdom

Received 19 May 2006; received in revised form 26 August 2006; accepted 15 September 2006

Abstract

The present study is a mesoscale analysis of latitude and depth related trends in abundance, biomass and body size ofthe four grenadier species Caelorinchus caelorhincus, Hymenocephalus italicus, Nezumia aequalis and Trachyrinchus scabrus

inhabiting the deep western Mediterranean. We have analysed data from seven annual bottom trawl surveys, carried outdown to 800 m depth along the Iberian Mediterranean coast covering a distance of approximately 1200 km. The objectiveswere to establish general patterns in the mesoscale distribution of abundance, biomass and body size of deep-water gren-adier fishes and also analyse the consistency of the bathymetric distribution of these parameters along a large latitudinalgradient. Five complementary series of analyses have been completed. The first focussed on describing the general patternsof abundance and size by correspondence canonical analysis, CCA, in the area. The second and third series focussed on theexistence of temporal, geographical and bathymetric trends of abundance, weight and mean size by analysis of covariance,ANCOVA and multiple regression analysis. The fourth series compared the frequency distributions of body length.Finally, the last series focussed on the patterns of abundance versus size. The total number of individuals of all four gren-adier species captured in 260 bottom trawls amounted to 27,435 and their weight was 1404 kg. No general trends for thefour species have been observed between years. All four species showed a general pattern of increasing size with depth,which, except in the case of C. caelorhincus, was consistent along a large latitudinal gradient. Nezumia aequalis was uniquein showing the same noticeable trend of increasing abundance with depth along the entire latitudinal range, but with cleardifferences in the intercepts. The abundance of N. aequalis and C. caelorhincus decreased significantly northwards.Hymenocephalus italicus was the least abundant species and had a homogeneous distribution without any specific trendalong the entire latitudinal range analysed. The distribution of T. scabrus in the Mediterranean seemed to be more local-ised. Higher abundances were found to the north and south of the latitudinal gradient with lower values between. Thegrenadiers studied also showed a general trend of decreasing mean size northwards, except in the case of the smallest spe-cies, H. italicus. The relation between abundance and body size differed between sectors for the whole grenadier populationand species-specific variations were also observed. The relationship between individual body mass and population densityfit well to a second-order polynomial function rather than to a linear regression, showing a significant trend for density toincrease with increasing size until some mid-point, then to decline with increasing size thereafter. The observed latitudinal

0079-6611/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.

doi:10.1016/j.pocean.2006.09.003

* Corresponding author.E-mail address: [email protected] (J. Moranta).

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64 J. Moranta et al. / Progress in Oceanography 72 (2007) 63–83

gradient in the distribution patterns of grenadiers along the upper slope of the western Mediterranean can be discussed inrelation to direct and indirect factors of biogeographic, environmental and anthropogenic origin.� 2006 Elsevier Ltd. All rights reserved.

Keywords: Macrourid fishes; Vertical distribution; Latitudinal variations; Abundance-body mass relationship; Deep-sea fisheries; WesternMediterranean

1. Introduction

The grenadiers (Pisces: Macrouridae) are one of the dominant families of deep water demersal fishes. Of theapproximately 300 species making up this family, 90% inhabit the continental slope between 200 and 2000 mdepth (Cohen et al., 1990). They are present in all oceans, from Subarctic to Antarctic regions, where theycontribute considerably to the biomass of the ecosystem (Haedrich et al., 1980; Merrett and Marshall,1980; Stefanescu et al., 1992a). Many studies have analysed different aspects of the biology of grenadiers inthe Pacific and the Atlantic Oceans (Merrett and Haedrich, 1997; Randall and Farrell, 1997; Swan and Gor-don, 2001). Eight species of grenadier occur in the Mediterranean Sea, but only five are common on the upperslope of the western Mediterranean (Caelorinchus caelorhincus, Caelorinchus labiatus, Hymenocephalus italicus,Nezumia aequalis and Trachyrinchus scabrus; Massutı et al., 2004). In this area, there have been many studiesfocussed on their distribution, age composition, growth, reproduction and diet (Carrasson and Matallanas,1989; Carrasson and Matallanas, 2002; D’Onghia et al., 1999; D’Onghia et al., 2000; D’Onghia et al., 1996;Macpherson, 1979; Massutı et al., 1995; Morales-Nin, 1990).

The wide latitudinal and bathymetric distribution of the grenadiers makes this family especially interestingfor the study of macroecological factors that determine the distribution of deep-sea fish species. The knowl-edge of species distribution related to biogeographical and bathymetric trends in abundance and body size isone of the most important issues addressed in deep sea studies (Gage and Tyler, 1991; Haedrich, 1997; Merrettand Haedrich, 1997; Rex and Etter, 1998; Stuart et al., 2003). Depth is the major environmental gradient in thedeep sea, and consequently affects the vertical patterns of species distribution both in abundance (Fujita et al.,1995; Haedrich, 1997; Merrett and Haedrich, 1997; Moranta et al., 2004; Stefanescu et al., 1993) and size(Clain and Rex, 2000; Macpherson and Duarte, 1991; Moranta et al., 2004; Rex and Etter, 1998; Stefanescuet al., 1992b). Most of the evidence indicates that almost all deep-sea species occur only within circumscribeddepth limits, and that these may or may not change over the horizontal geographic range of the species (Mer-rett and Haedrich, 1997). Heincke’s law or the ‘bigger-deeper’ phenomenon, understood as the trend ofincreasing size of organisms with increasing depth, has been shown to hold true for some deep-sea speciesbut not for others (e.g., Merrett and Haedrich, 1997; Middleton and Musick, 1986; Moranta et al., 2004;Rex and Etter, 1998; Stefanescu et al., 1992b, and references cited therein). The hypotheses to explain changesof size with depth relate mainly to food availability, inter or intraspecific competition, predation, fishing or asampling artefact (e.g. Macpherson and Duarte, 1991; Merrett et al., 1991a,b; Merrett and Haedrich, 1997;Merrett and Marshall, 1980; Middleton and Musick, 1986; Moranta et al., 2004; Polloni et al., 1979; Stefane-scu et al., 1992b). Moreover, empirical evidence shows that latitudinal patterns also affect abundance andbody size of marine animals at the scale of the whole geographic range of the species (Macpherson andDuarte, 1994; Macpherson, 1989, 2003; O’Hara and Poore, 2000; Olabarria and Thurston, 2003; Roy andMartien, 2001).

The effects of fishing activity on the density and size structure of populations are widely described (Gislasonand Sinclair, 2000; Pauly et al., 1998; Roberts, 2002; Tegner and Dayton, 1999). At the species level, thedecline of the abundance, biomass and size both for target and non-target species due to fishing effort is a wellknown phenomenon (e.g Gislason et al., 2000; Goni, 1998; Haedrich and Barnes, 1997; Merrett and Haedrich,1997; Philippart, 1998). Thus, the effects of fishing must be taken into account as a causative factor affectingthe geographic and bathymetric distribution of the species.

In the deep sea, as in other environments, body size has been shown to be inversely related to abundance(Rex and Etter, 1998). As a whole, the form of the interspecific relationship between abundance and body sizeis still contentious. Different patterns have been suggested, which can broadly be characterized as negative and

Fig. 1. Picture of the four grenadier species analysed in this study. (a) Caelorhinchus caelorhincus (17.8 cm), (b) Hymenocephalus italicus

(18.3 cm), (c) Nezumia aequalis (20 cm) and (d) Trachyrinchus scabrus (17.5 cm) (size expressed as total length).

J. Moranta et al. / Progress in Oceanography 72 (2007) 63–83 65

linear, negative but non-linear, and parabolic (Blackburn and Gaston, 1997; Currie, 1993). Negative linearrelationships have been generally been found when considering many phyla, across wide geographical areas,including a large range of body size. By contrast, the parabolic or triangular distributions have often beenfound at the level of local assemblages of taxonomically related organisms, such as particular families of bee-tles, birds or fishes, and within a relatively narrow range of body masses.

In the western Mediterranean the geographical patterns of abundance and population structure have beenidentified for different fauna in relation to a variety of direct and indirect factors such as hydrographic con-ditions, topography characteristics, and surface production inputs (Abello et al., 2002; Abello et al., 2002; Car-bonell et al., 2003b; Massutı et al., 2001). The present study is a mesoscale analysis of latitude and depthrelated trends in abundance and body size of the four grenadier species C. caelorhincus, H. italicus, N. aequalis

and T. scabrus inhabiting the upper slope of the western Mediterranean (Fig. 1). These species constitute animportant fraction of the discards (up to 60%) from the deep-water bottom trawl fishery (Moranta et al.,2000), which is well established in the area and targets decapod crustaceans (Demestre and Martın, 1993; Gar-cıa-Rodriguez and Esteban, 1999a; Sarda, 1998). Caelorinchus labiatus, the fifth grenadier species on the upperslope, has not been considered because it only appeared very occasionally.

In this study, we analyse data from seven annual bottom trawl surveys, carried out on the continental shelfand upper slope off the Iberian Mediterranean coast, between latitudes 35� and 42� N, covering a distance ofapproximately 1200 km. This seven year data can be considered a long-time series for deep-sea fishes, speciallywhen using the same fishing gear as this study. The objectives were to establish general patterns in the meso-scale distribution of abundance, biomass and size of deep-water fishes and also to analyse the consistency ofthe bathymetric distribution of these parameters along a large latitudinal gradient and to identify trendsrelated to environmental and anthropogenic causes.

2. Materials and methods

2.1. Study area

The study area encompassed the whole Iberian Mediterranean coast, between Punta Europa and CaboCreus (Fig. 2). Three geographical sectors were established: sector A, between Punta Europa and Cabo de

Fig. 2. Map of the study area. Dots along the northwest shelf were trawling sites in this study.


Gata; sector B, between Cabo de Gata and Cabo San Antonio; and sector C, between Cabo San Antonio andCabo Creus. These sectors were established taking in to account two criteria: (i) the water circulation in thewestern Mediterranean Sea and (ii) fishing activity at a local scale. Moreover, these three sectors are coincidentwith the geographical sub-areas considered by the General Fisheries Commission for the Mediterranean(GFCM).

Sector A coincides with the well defined Alboran Basin, which is the first Mediterranean basin encounteredby the inflow of Atlantic water through the Gibraltar Strait. This basin is characterized by very complex bot-tom topography, with a maximum depth of 2000 m, and by the presence of Alboran Island. The Atlanticwater entering the Alboran Sea through the surface layer of the strait is gradually modified in its eastwardmigration and is usually identified as Modified Atlantic Water (MAW) (EUROMODEL Group, 1995; Millot,1999). Sector C is situated in the Balearic Basin, and it is open to depths greater than 2500 m (Sarda et al.,2004). This basin is characterized by the presence of submarine canyons and river discharges. The water cir-culation in this area is similar to a large cyclonic gyre linked to the Northern Current of cool and salty WesternMediterranean Intermediate Waters (WIW) and the Balearic Current towards North-east (Pinot et al., 2002).The transition zone, Sector B, off the south Levant coast of the Iberian Peninsula, is connected to the northernbasin by a series of sills in the arch of the Balearic Islands, which plays an essential role in the general circu-lation of the western Mediterranean, being important passages for the exchange between the cooler and moresaline waters of the Balearic Basin and the warmer and fresher waters of the Algerian, Basin (Pinot et al.,2002). This sector is mainly influenced by the dynamics of the Algerian Basin (Sarda et al., 2004), which actsas a reservoir for water of Atlantic origin (Millot, 1985).

A fishing pressure gradient exists from south to north along the Mediterranean Iberian coast. From officialdata, the bottom trawl fleet operating in this area can be estimated at around 800 boats, distributed 10% in


sector A, 25% in sector B and 65% in sector C. Some of these units (small vessels) operate almost exclusivelyon the continental shelf (targeting red mullet, octopus, hake and sea bream), others (larger vessels) operatealmost exclusively on the continental slope (targeting decapod crustaceans especially Norway lobster. Nephr-

ops norvegicus, and deep water red shrimp, Aristeus antennatus) and the rest can operate either on the conti-nental shelf or on the slope fishing grounds, depending on the season, the weather conditions and alsoeconomic factors (e.g. market price). The deep water red shrimp fishery was initiated in the 1950s, and nowthis species is exploited on the upper continental slope, between 500 and 800 m depth (off the Catalan coastthis can extend to �1000 m), along the whole Iberian coast, from Cape Gata to Cape Creus (Carbonell et al.,1999; Demestre and Lleonart, 1993; Garcıa-Rodriguez, 2003; Garcıa-Rodriguez and Esteban, 1999a; Garcıa-Rodriguez and Esteban, 1999b).

2.2. Sampling procedures

Samples were collected with a research bottom trawl GOC 73, during the Spanish MEDITS surveys, car-ried out during spring and for seven consecutive years (i.e., between 1994 and 2000). This bottom trawl hasbeen used throughout the western Mediterranean and its efficiency for catching demersal species has alreadybeen tested (Bertrand et al., 2002). The average towing speed was 2.8 knots. The average horizontal and ver-tical openings were estimated on 16.4 and 2.8 m, respectively using SCANMAR system. More detaileddescription of the MEDITS surveys are provided by Bertrand et al. (2002). A total of 710 hauls, at depthsbetween 27 and 795 m were analysed. For each trawl, the number and fresh weight of C. caelorhincus, H. ita-licus, N. aequalis and T. scabrus were recorded, and the pre-anal length (from snout to anus; PAL) of individ-uals was measured to the nearest mm. Catch values were standardised to number of individuals and biomassper hour of trawling for subsequent statistical analysis. The individual weight of each specimen was calculatedfrom the length–weight relationships provided by Morey et al. (2003).

2.3. Statistical analysis

Five complementary series of analyses were completed in order to describe general latitudinal and bathy-metric patterns of species abundance, weight and size. The first focused on the general patterns related toabundance and size. We specifically explore the existence of differential (or coincident) patterns when compar-ing the small, medium and large individuals of the four species. For this purpose the individuals of each specieswere classified into one of three size classes (small, medium and large), each size class representing 1/3 of themaximum size recorded for each species during the Spanish MEDITS surveys. Each of the four species wassplit into three ‘‘pseudospecies’’ (one per size class), thus resulting in 12 categories. We specifically focussedon the existence of multivariate responses in the resulting matrix of abundances (i.e., of pseudospecies) relatedwith temporal (year), geographical (PCA-Axis1; see below) and bathymetric (depth) patterns. These objectiveswere achieved using canonical correspondence analysis (CCA). This approach emulates that of Carbonellet al. (2003b).

Concerning geographical patterns, the original data (degrees and minutes) were first transformed to deci-mal coordinates and further rotated on axes derived from a principal component analysis (Carbonell et al.,2003b). In this way, the latitude–longitude coordinates were transformed into a single variable (PCA-Axis1;site scores on the first axis which explained more than 95% of total variance). For this new axis negative andpositive values correspond to samples collected at the southern and northern sampling area, respectively.

The second series of analyses focussed on the existence of temporal species-specific variations of abundance(A, number of individuals h�1), weight (W, kg h�1) and mean size (MS, pre-anal length). The interactionbetween year and depth was analysed by means of analysis of covariance (ANCOVA). Three parallel ANCO-VAs were completed for A, W and MS considered as dependent variables, while year and depth were categor-ical and continuous variables, respectively. Pairwise post hoc comparisons were evaluated using theBonferroni test.

The third series of analyses focused on species-specific responses of the same parameters analysed aboveagainst PCA-Axis1 and depth. These analyses were achieved by using a conventional multiple regression anal-ysis, with the A, W and MS as response variables and PCA-Axis1 and depth as explanatory variables. The


interaction between PCA-Axis1 and depth was analysed by means of ANCOVAs. These ANCOVAs are sim-ilar to the preceding ones but they focussed in sector-specific responses (sector as categorical variable).

The fourth series of analyses compared the frequency distributions of body length. Two comparisons wereconsidered. First, the three sectors were compared with each other for the four grenadier species. Second, thehistogram of N. aequalis and T. scabrus corresponding to the sector C (0–800 m depth; present study) wascompared with that obtained from the same sector but covering a deeper range. These data correspondedto the length–frequency distribution obtained from 25 hauls carried out in the Balearic basin (sector C)between 1000 and 1400 m depth, from BATHOS and RETROs deep sea surveys developed between 1987and 1992 in this area (see Massutı et al., 2004 and references cited therein for details). The objective of thislast analysis was to corroborate the size variation with depth for those species with a wider bathymetric dis-tribution. C. caelorhincus and H. italicus were not compared, because they are not distributed below 800 mdepth (Massutı et al., 1995).

Finally, the last series of analyses focussed on the patterns of abundance versus size. The mean abundanceof grenadiers in each haul (and by sector) was plotted against size (using body weight as a general surrogate ofbody size). A second order polynomial regression was fitted to these plots (separately for the four species)because the specific density–body length distributions tended to peak in the middle of the size distributions(Blackburn et al., 1990).

Table 1Annual data for each of the four species studied: depth range, size interval, total number of individuals and total weight (kg)

Year Species n Depth (m) Size (cm, PAL) Number Weight

1994 (N = 70) Cc 15 250–621 2–12 546 10.80Depth range (m): 27–786 Hi 9 405–686 2–4 94 0.42

Na 14 427–786 0.5–6 679 8.38Ts 11 417–786 1.5–23 449 17.12


Na 21 421–771 0.5–8 2403 49.05Ts 18 412–771 1–24 668 132.33

1996 (N = 106) Cc 25 248–638 1.5–13 1484 21.58Depth range (m): 27–795 Hi 15 364–795 1.5–4.5 57 0.35

Na 26 364–795 1.5–8.5 3057 88.03Ts 16 432–795 7–24 594 142.97

1997 (N = 100) Cc 20 235–636 1.5–12.5 1044 25.19Depth range (m): 27–761 Hi 15 413–761 1.5–4.5 88 0.38

Na 21 407–761 1–7 2569 76.42Ts 17 485–761 5.5–24.5 1080 300.13


Na 18 421–727 1–7 2120 55.92Ts 10 520–727 5.5–24 448 148.91


Na 19 381–790 1–7 1542 47.73Ts 13 504–790 5–24 343 80.61


Na 24 358–776 1–6 1953 42.56Ts 16 386–776 2–23 641 89.63

Total (N = 710) 260 168–790 0.5–24 27,435 1403.97

Cc: Caelorinchus caelorhincus, Hi: Hymenocephalus italicus, Na: Nezumia aequalis, Ts: Trachyrinchus scabrus, N: total number of samplesby year, n: number of samples with the presence of the target species, PAL: pre-anal length (length ranges are rounded to 0.5 cm). Numberand weight standardised to 1 h of trawling.


3. Results

The total number of individuals of all four grenadier species captured in 260 bottom trawls amounted to27,435 and their weight was 1403.97 kg. The total abundance (number of individuals) and the biomass per spe-cies, the depth range in which each species was present and the size interval of the individuals captured aresummarised for each of the 7 years surveyed in Table 1. In number, N. aequalis was the most abundant inall years, followed by C. caelorhincus. H. italicus was the least abundant species, both in number and biomass.In terms of total biomass, T. scabrus was the most important species, followed by N. aequalis, except in 1994,when C. caelorhincus was the second ranked species. T. scabrus had the greatest maximum length, followed byC. caelorhincus, N. aequalis and H. italicus in decreasing order.

The multivariate approach (the CCA analysis) revealed that a significant portion of the variability of theabundance of the 12 pseudospecies considered (three size intervals within each of the four species) is explainedby year (Trace = 0.069, F = 1.501, p = 0.018). However, this variable was responsible for a small proportion

Fig. 3. Results of the correspondence canonical analysis (CCA) on the effect of year (panel a) and depth and PCA-Axis1 (panel b) on thecombined variable of abundance and size. For this purpose the number of individuals was divided into three size classes small (1), medium(2) and large (3), considering each size class as 1/3 of the maximum size range recorded for each species during the MEDITS surveys.


(9.26%) of the total variance explained by the model (40.57%; the three explanatory variables included in thismodel were year, depth and PCA-Axis1). The year 1994 and, to some extent, 2000, were different from theother years, and 1996, 1997 and 1998 seem to be more similar to one another (Fig. 3a). Nevertheless, noattempt to interpret the temporal trend was made because no obvious pattern was observed. Therefore, thisvariable was included as a covariable for subsequent analyses with the sole purpose of allowing a proper inter-pretation of the variability explained by the other variables in the model. These other two variables accountedfor 46.64% and 44.09% of the explained variance (partial analyses: Depth, Trace = 0.347, F = 45.075,p < 0.001; PCA-Axis1, Trace = 0.328, F = 45.567, p < 0.001). The interaction between depth and PCA-Axis1was not considered in the model because this term showed a clear collinearity with PCA-Axis1. C. caelorhincus

and N. aequalis were more abundant in the southern area, and H. italicus was more abundant northward(Fig. 3b). For these three species, the gradient of size, represented by the classes of small, medium and largeindividuals, followed a common trend: larger individuals were found in the deepest hauls. Larger individualsof T. scabrus were also found at deeper depths, but in its case a clear latitudinal effect was detected, with thelargest individuals in the southern areas.

As with the multivariate analysis, no general trend for the four species was observed between years whencomparing the abundance, weight and mean size. The mean values of these three parameters varied betweenyears, but significant differences were only detected for mean size for N. aequalis and T. scabrus (Table 2). Inthe case of C. caelorhincus the maximum values in abundance were observed in 1995 and 2000 and in weight in1997 and 2000 (Fig. 4). For H. italicus and N. aequalis both the abundance and weight variables followed thesame trend with maximum values in 1994, 1995 and 1998 for H. italicus and in 1997 for N. aequalis. The abun-dance and weight of T. scabrus also peaked in 1997. For N. aequalis significant differences in mean size wereobtained only between 2000 (smallest mean size) and 1996–97 (largest mean size) (Table 2, Fig. 5). For T. sca-

brus significantly low mean sizes were found in 1994 and 2000.The size–frequency distributions for the four species showed only small differences between years, but these

differences were most evident in the case of T. scabrus (Fig. 5). For this species two modes at 8 and 19 cm wereobserved in the years 1995 and 1996, while in 1997 the modes were at 7 and 20 cm. The years 1994 and 2000

Table 2Results of the general linear model for the analysis of covariance for abundance (A), weight (W) and mean size (MS) (all three variableswere log10 transformed) among years (1994, 1995, 1996, 1997, 1998, 1999, 2000) considering depth as the covariate

Mean depth(m)

df C. caelorhincus H. italicus N. aequalis T. scabrus

421.92 557.05 595.64 617.51

MS F139,145 MS F77,83 MS F129,135 Between yearsdifferences

MS F87,93 Between years differences

Log(A)

Year (Y) 6 1.07 2.02 0.12 0.52 0.44 0.72 0.29 0.50Depth (D) 1 3.13 5.93* 0.01 0.04 3.09 5.05* 1.70 2.25Error 0.53 0.23 0.61 0.58

Log(W + 1)

Year (Y) 6 0.06 1.29 0.00 1.38 0.15 1.11 0.20 0.71Depth (D) 1 0.30 6.56* 0.00 2.29 2.04 15.07** 5.63 20.27**

Error 0.05 0.00 0.14 0.28

Log(MS)

Year (Y) 6 0.03 1.68 0.01 0.71 0.03 2.50* 00 > 96 = 97 0.26 8.17** 94 < 95 = 96 = 97 = 98 = 99Depth (D) 1 2.82 148.59** 0.20 19.99** 0.72 58.00** 0.81 25.46** 94 = 00 < 96 = 98 = 99Y * D 6 0.06 3.22*

Error 0.02 0.01 0.01 0.03

df: degrees of freedom, MS: mean of square, F: statistic (the subscript is the degrees of freedom for the error term in the model, with andwithout the interaction term). When the interaction was not significant, it was dropped from the model and the analysis was run againexcluding the interaction term. The underlined groups of years separated by the symbol < or > denote significant differences between pairsof years. The asterisk denotes significant differences.

* p < 0.05.** p < 0.001.

Fig. 4. Mean values and 95% confidence intervals (vertical lines) of the number of individuals and the weight (kg), both standardised to1 h of trawling, captured for Caelorhinchus caelorhincus, Hymenocephalus italicus, Nezumia aequalis and Trachyrinchus scabrus in eachyear.


were characterised by a high proportion of small individuals, contrasting with 1998 when these sizes were vir-tually absent. The size–frequency distributions obtained for the other species were unimodal except in 1994and 1997 for C. caelorhincus, for which a second mode was found at 6 cm (Fig. 5). For that species the mainmode was situated at either 3 or 4 cm in different years. Finally, the years 1994, 1995 and 2000 were charac-terized by a high proportion of individuals of N. aequalis less than 4 cm.

Significant linear relationships between abundance, weight and mean size against depth and PCA-Axis1were detected for C. caelorhincus and N. aequalis (Table 3). The relationships with the geographical positionwere stronger for abundance and weight and the values were higher southwards for both species (Fig. 6) withsignificant differences between sectors (Table 4). The relationship with depth for these two species showed alow partial regression coefficient (b) for both variables with different trends between sectors and within species(Fig. 7). The exceptions were the abundance of N. aequalis which increased with depth in all three sectors andthe weight of C. caelorhincus. In both cases the interaction term Sector *Depth was not significant (Table 4). Inthe case of H. italicus and T. scabrus although no significant latitudinal trend was detected for the abundance(Table 3), significant differences were detected for abundance between sectors with higher values in Sector Bfor H. italicus and lower values in the same sector for T. scabrus. T. scabrus had, higher values in sector A forweight and showed a significant latitudinal trend (Table 4, Fig. 6).

All four species showed a significant tendency of increasing size with depth, with the highest b value for C.

caelorhincus and the lowest b for T. scabrus (Table 3 and Fig. 7). Except in the case of C. caelorhincus, wherethere were significant differences in the interaction term Sector *Depth, this trend was consistent among thethree sectors (Table 4 and Fig. 7). A significant northward trend of decreasing size was found for C. caelor-hincus, N. aequalis and T. scabrus, the last of which showed the highest b value (Table 3). The mean size ofthese three species was larger in sector A than in the others, but no differences were found between sectors


B and C. H. italicus did not show any significant trend with respect to the variable PCA-Axis1 for size (Table3), but significant differences were detected for mean size between sectors A and B with higher values in sectorA.

The size frequency distributions showed marked differences between the three sectors for the four species(Fig. 8). In every case the proportion of larger individuals was higher in Sector A than the others, but thisdifference was more evident in the case of T. scabrus with individuals larger than 16 cm only found in sectorA. Similarly, individuals of C. caelorhincus and N. aequalis larger than 8 and 5.5 cm, respectively were onlyobserved in sector A. In sector C individuals of N. aequalis larger than 5.5 cm and of T. scabrus larger than16 cm were found at depths greater than 1000 m (Fig. 8).

Fig. 5. Length frequency distributions of Caelorhinchus caelorhincus, Hymenocephalus italicus, Nezumia aequalis and Trachyrinchus

scabrus obtained in each survey. Note that the y-axis has a different scale for Trachyrinchus scabrus.

Table 3Results for the multiple regression analysis among abundance (number of individuals h�1), weight (kg h�1) and mean size (pre-anal length,cm) against depth (m) and geographical position (transformed to a single variable from the first axis resulting from the principalcomponent analysis, see text for more details)

N b for abundance b for weight b for mean size

Depth Axis1 Depth Axis1 Depth Axis1

C. caelorhincus 153 �0.24** �0.54** 0.15* �0.49** 0.63** �0.27**

H. italicus 91 �0.04 0.21 0.11 0.08 0.46** �0.17N. aequalis 143 0.26** �0.73** 0.38** �0.63** 0.57** �0.30**

T. scabrus 101 0.14 �0.02 0.28* �0.40** 0.24* �0.52**

Abundance, weight and size are the dependent variables, and depth and PCA-Axis1 (Axis1) the independent variables. Zero-samples(those samples without any individual) have been excluded from the analyses. N: number of hauls, b: partial regression coefficient. Theasterisk denotes significant regressions.

* p < 0.05.** p < 0.001.


The relationship between abundance and body weight of the whole grenadier population fitted well to asecond order polynomial regression except in sector A, due to the higher abundance of large body weights(Fig. 9 and Table 5). At the species level the relationships between abundance and body weight also fit wellto a second order polynomial function except for H. italicus in sectors A and C and T. scabrus in sector B(Fig. 10 and Table 5). The linear term was also significant in the case of C. caelorhincus and T. scabrus in Sec-tor A (Table 5).

4. Discussion

The grenadiers C. caelorhincus, H. italicus, N. aequalis and T. scabrus show a general pattern of increasingsize with depth, which, except in the case of C. caelorhincus, is consistent along a large latitudinal gradient.Although some controversy exists about the existence of general trends with depth (Merrett and Haedrich,1997; Moranta et al., 2004; Rex and Etter, 1998; Stefanescu et al., 1992b), the bigger–deeper phenomenonhas been described for the macrourid species in the Mediterranean as a well defined rule (Massutı et al.,1995; Moranta et al., 2004). By contrast, the bathymetric distribution of the abundance was clearly relatedto geographical variations with no general patterns for the four species analysed. Nezumia aequalis was uniquein showing the same noticeable trend of increasing abundance with depth along the entire latitudinal range,but with clear differences in the intercepts. In general the abundance of deep-sea Mediterranean fishesdecreases with depth with a tendency to stabilise at depths greater than 500 m (Moranta et al., 1998; Stefane-scu et al., 1993). However, at the species level, the abundance of grenadiers, when their entire bathymetricrange of distribution is considered, fitted well to a unimodal function, with the maximum abundance in thecentre of their bathymetric distribution (Moranta et al., 2004). The entire depth range of H. italicus and C.

caelorhincus was sampled in the present study, while for N. aequalis and T. scabrus only the upper part of theirdepth range was sampled (Moranta et al., 1998; Stefanescu et al., 1992a). Thus, the linear relationship foundbetween abundance and depth for N. aequalis is in accordance with the previous results obtained for this spe-cies, with an increase in abundance to a maximum at 900 m and a decreasing abundance at greater depths(Moranta et al., 2004).

The observed gradient in the distribution patterns of grenadiers along the upper slope of the western Med-iterranean in relation to latitude can be explained by a variety of factors of biogeographic, environmental andanthropogenic origin.

The abundance of N. aequalis and C. caelorhincus, the two intermediate-sized and more abundant species,decreased significantly northwards. H. italicus was the least abundant but had a homogeneous distributionwithout any specific trend along the entire latitudinal range analysed. H. italicus differs from the other gren-adiers by having more pelagic feeding habits (Macpherson, 1979) and may be less susceptible to capture bybottom trawls when feeding in the water column.

Fig. 6. Geographical distribution of abundance (number of individuals per hour), weight (kg per hour) and mean size (pre-anal length) forthe four grenadier species analysed (logarithmically transformed data). The PCA-Axis1 represents the latitude–longitude coordinatestransformed to a single variable from the first axis resulting from the principal component analysis (see text for more details).


Nezumia aequalis can be considered as an Atlantic species with a centre of distribution to the west of theBritish Isles, where it has the highest density and the widest bathymetric range for this species (Coggan et al.,1999; Massutı et al., 2004). Biogeographic factors could explain the observed pattern of abundance in the wes-tern Mediterranean where there is a clear latitudinal gradient of decreasing abundance from south to north.On a broader scale there is a similar trend from west to east, and N. aequalis has not been reported in theeastern-central Mediterranean, where it is replaced by the other co-generic species Nezumia sclerorhynchus

(D’Onghia et al., 2000, 2004). Although data for C. caelorhincus in the Atlantic are scarce, its centre of dis-tribution is probably similar to N. aequalis, and in the Mediterranean it also decreases in abundance fromthe Strait of Gibraltar northwards. It is difficult to compare data on the abundance of this species in differentareas of the Mediterranean because different sampling gears were used. However, its frequency of occurrence

Table 4Results of the general linear model for the analysis of covariance for abundance (A) and mean size (MS) (both variables log10 transformed)among sectors (A,B,C) considering depth as the covariate

Mean depth(m)

df C. caelorhincus H. italicus N. aequalis T. scabrus

421.92 557.05 595.64 617.51

MS F147,149 Between Sdif.




Log10(A)

Sector (S) 2 4.46 12.39** A > B > C 0.94 4.53* A < B 25.59 104.30** A > B > C 4.03 10.19** A > B < C

Depth (D) 1 2.53 7.02* 0.03 0.14 6.99 28.48** 2.22 5.61*

S*D 2 2.01 5.59* 4.38 11.10**

Error 0.36 0.21 0.25 0.39

Log10(W + 1)

Sector (S) 0.94 27.08** A > B = C 0.00 0.97 0.04 0.58 1.59 11.25** A > B = C

Depth (D) 0.09 2.70 0.00 1.16 0.41 6.12* 3.03 21.50**

S*D 0.29 4.25* 2.25 15.95**

Error 0.03 0.00 0.07 0.14

Log10(MS)

Sector (S) 2 0.34 24.76** A > B = C 0.04 4.22* A > B 0.13 11.18** A > B = C 0.85 29.18** A > B = C

Depth (D) 1 0.81 59.85** 0.24 25.14** 0.87 75.87** 0.45 15.28**

S*D 2 0.53 38.89**

Error 0.01 0.01 0.01 0.03

df: degrees of freedom, MS: mean of square, F: statistic (the subscript is the degrees of freedom for the error term in the model with andwithout the interaction term). When the interaction was not significant, it was dropped from the model and the analysis was run againexcluding the interaction term. The underlined groups of years separated by the symbol < or > denote significant differences between pairsof years. The asterisk denotes significant differences.

* p < 0.05.** p < 0.001.


between 250 and 750 m depth decreased eastwards: in the western basin it occurred in 85% of the hauls (pres-ent study), while in the eastern-central basin it only occurred in 69% of the hauls (D’Onghia et al., 2000), or itwas not found (D’Onghia et al., 2004). The distribution of T. scabrus in the Mediterranean seems to be morelocalised. Higher abundances were found to the north and south of the latitudinal gradient with lower valuesbetween, as was previously reported by Moranta et al. (1998). In the Atlantic it was relatively abundant in thePorcupine Seabight but absent farther north in the Rockall Trough (Gordon and Bergstad, 1992; Massutıet al., 2004; Merrett et al., 1991a,b). The distribution of T. scabrus in the Atlantic is not so wide as that ofN. aequalis, and a congeneric species, Trachyrinchus murrayi, occurs in deeper water and also extends intohigher latitudes (Gordon et al., 1996; Merrett et al., 1991a,b).

The grenadiers studied also showed a decrease in mean size northward, except in the case of the smallestspecies, H. italicus, which exhibited no significant relationship between mean size and latitude. The markedlypelagic habit of this species clearly contributes to its lesser availability on the bottom and to lower vulnera-bility to capture by our bottom trawl (D’Onghia et al., 1999). The differences in the levels of fishing effortamong the three sectors could account for this trend. Many marine ecosystems have been impacted by fisheries(Myers and Worm, 2003; Pauly et al., 1998), and the results of any macroecological study will be influenced bythe ongoing removal of a substantial proportion of the biomass of larger animals (Jennings and Mackinson,2003). Fishing pressure affects demersal fish communities through selective removal of target species, throughthe by-catch and discarding of non-target species, and through habitat modifications. All of these result inchanges in overall biomass, in species composition and size structure (Bianchi et al., 2000; Daan et al.,2005; Jennings et al., 2001). The trawl fisheries exploiting red shrimp and Norway lobster will also have animpact on the other species of the upper slope. Discards from these fisheries have been estimated as up to40% of total catch, and are mainly composed of fishes, with Macrouridae being one of the most importantfamilies (Carbonell et al., 2003a; Moranta et al., 2000). It is probable that none of the discarded fish survive.

Trachyrinchus scabrus, the largest species, is the most plausible example of the impact of fishing on gren-adier populations. It has the highest regression coefficient with latitude for body size, but with an opposite


trend for abundance of smaller and larger individuals. Thus, small sizes are more abundant to the north andlarge sizes more abundant to the south. The red shrimp fishery is not well developed in the Alboran Basin, andthe western part of the open slope remains unexploited below 500 m depth. Large T. scabrus predominate onthese deeper grounds. Fishing pressure is high in the more northerly Algerian and Balearic Basins and takesplace over the whole bathymetric range of the present survey. Large fish were very scarce in these areas. Othersurveys in these two basins, where sampling was at depths greater than 800–1000 m where there is no fishingactivity, showed that large individuals predominate in the length–frequency distributions, similar to thoseobtained down to 800 m depth in the Alboran Sea. In fact, clear differences in fish biomass spectra have beenobserved between upper and middle slopes off the Iberian Mediterranean Coast, dominated by small and med-ium-large size classes, respectively, mainly attributed to the high fishing exploitation on the upper slope (Mas-

Fig. 7. Bathymetric distribution by sectors of abundance (number of individuals per hour), weight (kilograms per hour) and of mean size(pre-anal length) for the four grenadier species analysed (logarithmically transformed data).


sutı et al., 2004; Moranta et al., 2004). The middle sized N. aequalis, which has a bathymetric range similar tothat of T. scabrus (Moranta et al., 2000; Stefanescu et al., 1992a), also shows a comparable situation. Down toa depth of 800 m large specimens predominated in Alboran Basin, while in Balearic Basin they were dominantbelow this depth.

The relationship between abundance and body size varied between sectors for the whole grenadier popu-lation, and species-specific variations were also observed. In this study, the relationship between individualbody mass and population density fit well to a second order polynomial function rather than a linear regres-sion, showing a significant trend for density to increase with increasing size until some mid-point, then todecline with increasing size thereafter. Nevertheless, the polynomial relationship between abundance and bodyweight has not been found in the southern area for the whole grenadier assemblage due to the high density ofindividuals of T. scabrus larger than 300 g. Our results for the grenadiers are in marked contrast with the neg-

Fig. 8. Length frequency distributions by sector of the four grenadier species captured between 1994 and 2000 in this study. The lengthfrequency distribution of Nezumia aequalis and Trachyrinchus scabrus captured from 25 hauls carried out in the Balearic basin (sector C)between 1000 and 1400 m depth, from BATHOS and RETROs deep sea surveys between 1987 and 1992 in this area (see Massutı et al.,2004 and references cited therein for details) are also provided. Note that the y-axis has a different scale in some graphics.


ative linear relationship previously described for demersal fish communities, both among and within species(Ackerman and Bellwood, 2003; Gordoa and Duarte, 1992). The parabolic distribution found in our casemay be an artefact because of size selectivity against the smaller body sizes by the bottom trawl. By contrast,large individuals demand more from environmental resource pools than small ones, but also tend to occur atlower population densities (Brown and Maurer, 1986).

Nevertheless, body size has been described as a weak predictor of the abundance of benthic fishes and otherfactors such as habitat complexity or competition have been suggested to be regulating the patterns of speciesabundance (Macpherson, 1989). In this sense, the dietary overlaps between C. caelorhincus and N. aequalis

and between C. caelorhincus and T. scabrus reported by (Macpherson, 1979) could explain the occurrence

Fig. 9. Plots of body weight and population density (logarithmically transformed data) for the whole grenadier assemblage found in eachsector.

Table 5Results of fitting a second order polynomial regression between abundance and body weight (both variables log10 transformed) for thefour grenadier species studied

Sector A Sector B Sector C

F1(x) d.f. F2(x2) d.f. F1(x) d.f. F2(x2) d.f. F1(x) d.f. F(x2) d.f.

Whole assemblage

Sector A 0.03 86 1.25 85Sector B 1.51 61 18.04** 60Sector C 1.92 65 11.93** 64

Single species

H. italicus 0.40 6 3.93 5 0.20 8 5.73* 7 3.78 4 2.04 3C. caelorhincus 7.34* 23 68.30** 22 1.27 16 27.41** 15 2.68 10 5.41* 9N. aequalis 0.50 15 15.16** 14 5.08 11 7.96** 10 0.05 10 8.94** 9T. scabrus 24.49** 36 11.94** 35 0.11 20 0.80 19 0.85 35 17.49** 34

F(x2) is for the quadratic term in the model controlling for the linear term F(x). d.f. = Degrees of freedom associated with the F statistic.The asterisk denotes significant regressions.

* p < 0.05.** p < 0.001.

Fig. 10. Pattern of body weight and population density (logarithmically transformed data) for the four grenadier species studied.


of their maximum abundances at the shallowest (C. caelorhincus) and the deepest (N. aequalis, T. scabrus)depths surveyed. By contrast, H. italicus, which has a bathymetric distribution overlapping with the other spe-cies, probably leaves the bottom to feed in midwater.

If the environmental conditions are considered as another determining factor affecting the abundance ofgrenadiers, the primary production in pelagic waters, and thus the food availability in the continental slopeecosystems, could be decisive in determining the patterns of grenadier distribution on the western Mediterra-


nean slope. Due to the particular oceanographic conditions of the Alboran Sea and the presence of submarinecanyons and river discharges in the Balearic Basin, these areas have an unusually high primary production incomparison to neighbouring areas. These two basins are characterized by the presence of permanent fronts,the Almerıa-Oran hydrographic front in the Alboran Sea and the two fronts linked to the Northern Mediter-ranean Current and the Balearic Current in the Balearic Basin (Millot, 1999). These boundary regions standour against the general oligotrophic context of the Mediterranean Sea, since they increase the biomass (Lho-renz et al., 1988) and are locations of enhanced biological activity in the western Mediterranean. Moreover,the presence of submarine canyons, which play an important role in the concentration of sediment and in itstransport to greater depths, have been proved to be areas of high productivity (Monaco et al., 1990). Canyonscan also act as recruitment grounds (Stefanescu et al., 1994).

These characteristics of the northern basin could increase abundance of C. caelorhincus and T. scabrus inthis area. These two species with a long rostrum and a subterminal mouth have similar feeding habits, mainlyfeeding on prey that live buried in the sediment (Macpherson, 1979). However, the abundance of C. caelor-

hincus decreases northwards and T. scabrus does not show any trend. For this reason it can concluded thatin areas intensively exploited for high value decapod crustaceans, such as the upper slope of the western Med-iterranean, the effect of any abiotic factor on the mesoscale patterns of distribution of abundance and bodyweight of grenadier species could be masked by the impact of fishing exploitation.

Acknowledgement

This paper is a result of the Spanish MEDITS project (DGXIV/IEO/054). We are most grateful to L. Gil deSola, head of MEDITS_ES surveys, and all the participants in the surveys as well as the captains and crew ofRV ‘Cornide de Saavedra’.

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Documents

Geographic and bathymetric trends in abundance, biomass and body size of four grenadier fishes along the Iberian coast in the western Mediterranean