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Spatial and temporal variation in pelagic community of the western and southern Iberian Atlantic waters
Estuarine, Coastal and Shelf Science 221 (2019) 147–155
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Spatial and temporal variation in pelagic community of the western and southern Iberian Atlantic waters
T
Eva García-Seoanea,∗,1, Vítor Marquesa, Alexandra Silvaa, Maria Manuel Angélicoa a
Instituto Português do Mar e Atmosfera (IPMA)- Rua Alfredo Magalhães Ramalho, 61495-006, Lisbon, Portugal
A R T I C LE I N FO
A B S T R A C T
Keywords: Community structure Environmental influences Iberian peninsula Pelagic fish Spatio-temporal variation
This study analyzed the spatial and temporal variation in the community composition of the pelagic species inhabiting the Atlantic Iberian waters using a multivariate approach. Trawl data (pelagic and bottom fishing) were collected during the spring acoustic surveys of pelagic fish from 1996 to 2015. There were significant effects of geographical area, periods, and type of trawls in terms of both, abundance and biomass. Sardine was typical throughout the study area whereas other species were typical of few areas, such as anchovy. The main difference between periods was the variation in typical pelagic species, diminishing the importance of sardine and increasing others, such as chub mackerel, bogue or anchovy. Depth also influenced the community structure with horse mackerel being the principally responsible for sample similarity in bottom trawls. Surface temperature and salinity showed significant relationship with the taxa-derived multivariate data cloud but only explained between 5 and 7% of the total variability.
1. Introduction There is a need for information and knowledge at the decadaltemporal scale to support decision making for management (Newton et al., 2014). Long term biological data is extremely valuable for differentiating natural changes from those caused by humans (Wolfe et al., 1987), since natural disturbances tend to be pulse disturbances while human activities tend to transform pulse disturbances into persistent changes (Elmqvist et al., 2003). Permanent changes in community structure tend to be associated with environmental degradation, whereby communities exhibit characteristic shifts in the dominance of species with different life-histories (Berumen and Pratchett, 2006). Ecosystem-based fishery management reverses the order of management priorities, so that management starts with the ecosystem rather than a target species (Pikitch et al., 2004). In that sense, an understanding of the ecological context within which fishery takes place, is required to minimize the adverse impact of fishing and evaluate the long-term capacity of the ecosystem to sustain the catches (Sousa et al., 2005). Hence, it is expressly important to monitor the community composition and spatial distribution over time to evaluate resistance to perturbation (Gomes et al., 2001). In the Iberian waters, pelagic stocks are traditionally assessed and managed using single-species approaches. Despite knowledge on
biological interactions among species (e.g. (Garrido et al., 2015), basic information on their relative abundance and spatial distribution is still scarce. Santos et al. (2013) demonstrated the utility of using trawl data collected during acoustic surveys in order to characterize the pelagic community. These authors, investigated the pelagic community in the north-western and northern Spanish shelf, but knowledge of this community for the west and south Iberian waters is scarce, and mainly come from demersal surveys (Gomes et al., 2001; Sousa et al., 2005), which are focused on fishes associated to the bottom. In Portuguese waters, the pelagic community is composed by small and median pelagics, such as the European sardine Sardina pilchardus, the Chub mackerel Scomber colias, Atlantic horse mackerel Trachurus trachurus, the Atlantic mackerel Scomber scombrus, Blue jack mackerel Trachurus picturatus, the European anchovy Engraulis encrasicolus and the Bogue Boops boops (Feijó et al., 2018). In the last decade, in particular since 2006, the abundance of sardine has decreased abruptly (ICES, 2017). The goal of this paper is to analyze how this reduction in sardine population might have an impact in the other species of the pelagic ecosystem. For that, this paper studies the changes in the community composition of the pelagic species inhabiting the Atlantic Iberian waters (Portuguese shelf and Gulf of Cadiz). This characterization is based on a large data set collected over the past two decades by the acoustic surveys of the Portuguese Institute for the Ocean and
∗
Corresponding author. E-mail address: [email protected] (E. García-Seoane). 1 Present address: Institute of Marine Research (IMR)- P. O. Box 1870 Nordnes, 5817-Bergen, Norway. https://doi.org/10.1016/j.ecss.2019.03.018 Received 12 August 2018; Received in revised form 3 March 2019; Accepted 24 March 2019 Available online 28 March 2019 0272-7714/ © 2019 Elsevier Ltd. All rights reserved.
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beam echo sounder. The hull-mounted transducer has a beam width of 7° x 8° and the transmitted pulse length employed is 1 ms. Several type of trawls (pelagic and bottom) are conducted according to the echogram information, in order to assist in the identification of the species that are reflecting the acoustic energy. The pelagic trawl net has a horizontal opening of 18 m, a vertical opening of 8 m, and a mesh size of 20 mm in the codend. This net captures small pelagic species, from the surface to the bottom. In shallow waters, the net is placed close to the bottom to catch because pelagic fish usually goes to the bottom as a reaction of the ship noise during trawling. Two different bottom trawls were used: the first years a Norwegian Campbell Trawl with rollers in the ground rope and after other otter trawl. Both bottom trawls have a codend mesh size of 20 mm. and they capture small pelagic species near the bottom and also demersal fish. From 1996 to 2015, a total of 18 spring surveys and 628 hauls (496 pelagic and 132 bottom fishing) were conducted during light hours. The haul duration is variable, depending on the number of individuals that enters in the net and the conditions where the fishing takes place. Due to this variability, to the fact thatnets with different sweep areas were routinely used during the surveys, and mainly because the abundance estimations using acoustic energy are not available for most pelagic species, the relative importance of the different species was estimated by each haul. The relative importance was estimated as follow:
the Atmosphere (IPMA). The linkages of these spatial and temporal changes with the environmental variables are also analyzed. A good description of the pelagic community and its correlation with environmental factors is particularly relevant for implementing multispecific approaches to the management of fisheries in the future. 2. Material and methods 2.1. Data collection The IPMA began its spring acoustic surveys in 1986 with the original aim of acquiring the necessary fishery-independent data to conduct the assessment of the sardine stock using acoustic techniques. The acoustic survey PELAGO takes place annually (with some interruptions) during spring (between February and May). This annual survey series had several methodological changes over the years, and nowadays produces not only biomass estimates for sardine and for anchovy but also collects information on other ecosystem components, such as environmental variables and bird census. The sampling area covered each year, extends over the Iberian shelf (including Portuguese waters, western and southern shores and the Spanish coast of the Gulf of Cadiz) between 10-15 m and close to the shelf break (200 m isobath). These surveys are conducted along predefined parallel transects mostly perpendicular to the coast and separated by 8 nautical miles (nmi) on average (Fig. 1). Sampling is conducted during a period of around 30 days and the vessel speed is approximately 8–10 knots. Due to the increased difficulty in attributing echotraces to individual species in the absence of clear school formations at night, and the logistic limitations in crew size surveying was limited to daylight (Zwolinski et al., 2007). The main objective of the survey is monitoring the abundance distribution of small pelagic fish, mainly sardine (S. pilchardus) and anchovy (E. encrasicolus), with acoustics methods. During the survey, acoustic energy backscattered by marine organisms is continuously recorded by a calibrated (Foote et al., 1987) 38 kHz Simrad EK500 split
• Abundance values were converted to percent composition, reducing •
the variability resulting from methodological differences while still retaining the relative abundance of individual taxa within each haul (Mathieson et al., 2000). Biomass values were converted to the percent of biomass, i.e. standardized as the sum of the weight (kg) of each species divided by the total weight of all species in the haul (kg). This process avoids that trawls with higher catches contribute more to the estimated overall composition of the pelagic community (Santos et al., 2013).
From 2000, environmental variables (temperature -°C-, salinity and fluorescence –volts-) have been routinely measured continuously along the track of the acoustics transects from water pumped from 3 m depth by a Continuous, Underway Fish Egg Sampler (CUFES). Surface temperature, salinity and fluorescence were averaged for units of 3 nmi (the standard procedure associated to the CUFES zooplankton samples). Extreme values were removed from the analysis following expert judgment. ESRI ArcMap 10.1.3 was used to calculate the environmental values at the fishing stations. First, temperature, salinity and fluorescence grids of data were interpolated using kriging. The search radius was fixed to 9 nmi in all years, except in 2006 for fluorescence, when the program was unable to estimate the semivariogram with radius less than 21 nmi. Finally, for each year, the environmental measures were estimated at hauls locations extracting the environmental values from the maps previously interpolated. 2.2. Multivariate analysis The multivariate analysis was performed with PRIMER 6 with PERMANOVA + statistical package (Anderson et al., 2008). Individuals of 226 taxa were identified in the hauls (Table S1) but many of them were considered rare since they were very infrequent. In addition, only hauls with at least 100 individuals in total were considered in the analyses. In order to better describe the core of the community and avoid undue relevance to rare species, those with an average percentage of occurrence (i.e., average of the percentage of hauls in which each taxon occurred in relation to the total number of hauls conducted for each survey) < 10% were not considered in the analyses. As a result, a total of 16 taxa were employed in the construction of the data matrix used for multivariate analyses. In spite of being a demersal species, the European hake Merluccius merluccius was retained in our analyses because it was frequently caught in the acoustic surveys.
Fig. 1. Map of the Iberian Peninsula showing the acoustic transects and the boundaries of the areas. 148
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(Fig. 3a). The lowest temperatures coincided with the only survey that started in February (year 2003). Considering inter-annual variability in salinity, the 2001 is highlighted for the low values of surface salinity (median = 34.4, IQR = 2.4) (Fig. 2). These values are probably related with the high levels of precipitation registered during this winter (IPMA, 2018). For fluorescence, the highest medians were found in 2009, 2013 and 2014 perhaps associated to the onset of spring blooms. On the other hand, seasonal differences were not found for surface salinity and fluorescence medians (Fig. 3b and c). However, the dispersion in the fluorescence is higher in April and May, when the spring blooms are already well underway.
Table 1 Number of pelagic and bottom trawls per area (OCN- from Caminha to Nazaré Canyon-, OCS -from Nazaré to Cape S. Vicente-, Algarve -from Cape S. Vicente to V. R. Santo António- and Cadiz -from V. R. Santo António to Cape Trafalgar) and period (1996–2005 and 2006–2015). P - pelagic trawls and B- bottom trawls. 1996–2005 OCN
2006–2015
OCS
ALG
CAD
OCN
OCS
ALG
CAD
P
B
P
B
P
B
P
B
P
B
P
B
P
B
P
B
57
21
67
14
49
5
41
16
59
18
63
16
47
17
34
18
3.2. General description of the pelagic community The Bray-Curtis coefficient was used to calculate similarities of taxa at each sampling haul. Permutational multivariate analysis of variance (PERMANOVA, main test) (Anderson et al., 2008) was performed to test for spatial and temporal differences in the composition of the pelagic community. The PERMANOVA design had the following fixed factors: period (1996–2005, 2006–2015), area (OCNe from Caminha to Nazaré Canyon-, OCS -from Nazaré to Cape S. Vicente-, Algarve -from Cape S. Vicente to V. R. Santo António- and Cadiz -from V. R. Santo António to Cape Trafalgar-, Fig. 1) and fishing trawl type (pelagic trawl and bottom trawl). The selection of these two periods analyzed was based on the marked sardine abundance decrease in Iberian waters since 2006 (ICES, 2017) and selection of the areas on the geomorphology of the shelf and historical records of sardine distribution. The distribution of the hauls between these three factors considered in the analyses is detailed in Table 1. The pair-wise PERMANOVA tests were also made when significant differences were found for the factors. All PERMANOVA procedures were run with 9999 permutations. In addition, a test for homogeneity of multivariate dispersion (PERMDISP with 9999 permutations) was applied. SIMPER analyses were used to identify species that most contributed for similarities among the significant groups tested in the PERMANOVA, considering the significant interactions. Taxa contributing to the average similarity of each sampling site in at least 2% were considered as typical of that site, following criteria defined by Drake et al. (2002). Draftsman plot, which is an ensemble of plots showing each variable plotted against each other variable, was constructed to identify skewness and multi-collinearity for surface temperature, salinity and fluorescence. The relationship between the pelagic community and the environmental variables was explored with distance-based linear model (DISTLM with Adjusted-R2 criterion and forward model selection) and distance-based redundancy analysis (dbRDA) (Legendre and Anderson, 1999; McArdle and Anderson, 2001).
In general, most hauls caught few species, with an average of 5 taxa (ranging from 1 to 13). Fish (13 taxa) dominated the hauls, followed by crustaceans (Henslow's swimming crab Polybius henslowii), which was present in more than one third of the hauls) (Table 2). Cephalopods (Allotheutis spp. and European squid Loligo vulgaris) were present in more than one quarter of the hauls. The most important species in terms of frequency was sardine, which was present in 88% of the hauls (Table 2). Other common species were chub mackerel and bogue, appearing over half of the hauls. 3.3. Pelagic community structure The three PERMANOVA factors analyzed were significant for both pelagic community abundance (Table 3) and biomass (Table 4), as well as the interactions between Period x Area and Area x Trawl. Considering biomass, Period x Trawl is in the boundary of significance (PERMANOVA, P-value = 0.0138). The areas have differences in pelagic community structure (PERMANOVA pair-wise test, P-value < 0.01), except for OCS and ALG, in terms of abundance (PERMANOVA pair-wise test, t = 1.3608, P-value = 0.0884) and biomass (PERMANOVA pair-wise test, t = 1.2717, P-value = 0.1372). In terms of abundance, sardine was typical throughout the study area, contributing at least 21% to the average similarity. In Cadiz, the contribution to similarity of sardine is lower than in the other areas. Other typical species in Cadiz are anchovy (contributing between 16 and 62% to the similarity) and chub mackerel (contributing between 2 and 12% to the similarity) (Table S2). Similar results were found for biomass data (Table S3). These differences between areas were reflected also in both types of trawl (PERMANOVA pair-wise test), being all areas significantly different in both pelagic and bottom samples, except OCS and ALG. However, lower p-values were found for pelagic trawls. For example, when comparing OCS and Algarve in terms of abundance, both trawls showed no significant differences (i.e., P-values > 0.01) between these two areas. For pelagic trawl P-value = 0.0416 (PERMANOVA pair-wise test) whereas for bottom trawl P-value = 0.2184). Bottom trawls were more diverse than pelagics. For abundance data, bottom fishing presented a total of 12 typical species (Alloteuthis spp., bogue, the common two-banded seabream Diplodus vulgaris, anchovy, hake, Axillary seabream Pagellus acarne, P. henslowii, sardine, chub mackerel, atlantic mackerel, jack mackerel and horse mackerel) versus the 4 typical species of pelagic trawls (sardine, chub mackerel, anchovy and bogue) (Table S4). In terms of biomass, the same 4 species were typical of pelagic trawl and 12 for bottom trawl (Table S5). The main differences in comparison with abundance data were that in bottom trawls Black seabream Spondyliosoma cantharus appeared as typical while Alloteuthis spp. was not a typical species. An important difference between periods is the decrease of sardine contribution to the average similarity (in both terms of abundance and biomass) compensated by an increase of other species, such as horse mackerel, anchovy, chub mackerel or bogue. The differences between areas were also stable between the two periods studied, except for OCN and Algarve, which were not significantly different in the first period
3. Results 3.1. Environmental parameters There was an increase in the surface temperatures from north to south, having OCN lower values (median = 14.7 °C, interquartile range -IQR- = 1.6) than Algarve (median = 16.3 °C, IQR = 1.5) (Fig. 2a). The highest temperatures were found in Cadiz (median = 17.1 °C, IQR = 1.9), the easternmost area adjacent to the Mediterranean Sea. Salinity values were also higher in Cadiz and then decreasing towards the west and north. The minimum were observed in OCN (median = 35.5, IQR = 0.9) and maximum in Cadiz and Algarve (medians of 36.1 -IQR = 0.2 - and 36.0 -IQR = 0.2 - respectively) (Fig. 2c). For fluorescence, the median values (and also the dispersion) were higher in OCN in comparison with the other areas (Fig. 2e). There was substantial inter-annual variability in surface temperature (Fig. 2b). However, it is important to note that this variability is also influenced by the period during which the survey was conducted 149
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Fig. 2. Boxplots of temperature, salinity and fluorescence along the areas (left plots) and the surveys (right plots). The middle line indicates the median and extremities of the box are the 25th and 75th percentiles. The maximum length of each whisker represents the 1.5 times the interquartile range, but when no points exceed this distance, the whiskers represent the minimum or maximum values.
4. Discussion
(1996–2005) in both in terms of abundance and of biomass. However, it is important to note that it is in the boundary of the significance (Pvalue = 0.0153 for abundance and P-value = 0.0119 for biomass). The pair-wise analyses of the interaction terms showed that the differences in the structure of the pelagic community between the two periods are present in all areas. In the first period (1996–2005), sardine contributed from 96 to 78% in terms of abundance, and from 96 to 79% in terms of biomass, whereas in the second (2006–2015) only contributed from 85 to 21% in abundance and from 86 to 26% in biomass (Tables S2 and S3). In fact, during the second period, anchovy is the species that contributed the most to the similarity in Cadiz (in both abundance and biomass data). The order of importance of the other pelagic species differed for abundance and biomass in the different areas. PERMDISP tests were significant for the three factors analyzed: period, area and type of trawl (PERMDISP, P-values < 0.01), except for area in abundance, but it is in the boundary (P-values = 0.015). These results indicate heterogeneity of multivariate dispersion among groups in most of cases.
Identifying the habitats that fish species use is vital to apply the ecosystem-based approach to fisheries management (Levin and Stunz, 2005). The usage of long-term data sets, like in this study, is very relevant for establishing reference conditions and assess fluctuations and trends in the communities composition (Boero, 2009). In the most productive regions of the world oceans, particularly in the upwelling regions, small pelagic fish, such as sardines and anchovies, occupy an intermediate trophic level in the coastal marine food webs, having a key role as food source for a wide range of predators (Bakun, 2006). A characteristic of the upwelling ecosystems is the occurrence of decadal fluctuations in species abundance and sometimes species replacement (Alheit et al., 2009). These modifications appear to be caused by environmental variability and are often amplified by fishing pressure (Alheit et al., 2009; Essington et al., 2015). Our results indicate that a relatively small number of species in the pelagic community predominates in the western and southern waters of the Iberian Peninsula, as has been reported for the pelagic community of the north and northwestern Iberian waters (Santos et al., 2013). However, in the northern Iberian waters the most frequent species was the Atlantic mackerel, being sardine as important in terms of biomass as horse mackerel and bogue (Santos et al., 2013). Further south, in our study, despite spatial and temporal variations, sardine was clearly predominant in the western and southern waters. The dominance of one or a few pelagic species appears to be a common characteristic of upwelling systems (Bakun, 2006). The variability in community composition was in part geographical, as shown by the significant effect of the variable area in the PERMANOVA. The present work showed three distinct geographical areas with mostly persistent typical pelagic species along the western and southern Iberian waters: the northern area (OCN), the central and south western area (OCS and Algarve) and the Gulf of Cadiz. The differences between areas are not only associated to the latitude gradient (with increasing
3.4. Relationship between pelagic community and environmental parameters Draftsman plot did not detect skewness nor outliers. Additionally, the three environment variables were tested and none was collinear. In the marginal test of DISTLM, surface temperature, salinity and fluorescence showed significant relationship with the taxa-derived multivariate data cloud (P < 0.001). However, together these variables explained only 5.8% of the total variability in the data cloud for abundance (Table S6) and 6.8% for biomass (Table S7). There was some discrimination of the areas along the RDA axis 1, with OCN samples more associated to low surface temperatures and a wide range of salinity variations while Cadiz and Algarve samples more associated to high temperatures (Fig. 4). Similar results were found for biomass data (Fig. 5). 150
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Table 2 Percentage of hauls containing each taxa in a total of 542 hauls analyzed. Taxa
Percentage of hauls (%)
Fish Boops boops Diplodus vulgaris Engraulis encrasicolus Merluccius merluccius Pagellus acarne Pagellus erythrinus Sardina pilchardus Scomber colias Scomber scombrus Spondyliosoma cantharus Trachurus mediterraneus Trachurus picturatus Trachurus trachurus
53 15 39 30 13 16 88 58 40 21 10 16 47
Cephalopods Alloteuthis spp. Loligo vulgaris
24 13
Crustaceans Polybius henslowii
36
Table 3 Results of PERMANOVA main test in terms of abundance used to test the effects of period, area and type of trawl as fixed factors, and their interactions. Source
df
SS
MS
Pseudo-F
P(perm)
Unique perms
Pe Ar Tr PexAr PexTr ArxTr PexArxTr Res Total
1 3 1 3 1 3 3 526 541
40573 92044 1.42E+05 13817 4474.3 22265 8998.7 1.13E+06 1.54E+06
40573 30681 1.42E+05 4605.6 4474.3 7421.7 2999.6 2149.7
18.874 14.273 65.93 2.1424 2.0814 3.4525 1.3954
0.0001 0.0001 0.0001 0.0053 0.052 0.0001 0.1175
9934 9903 9934 9907 9934 9898 9915
Significant differences are shown in bold. Table 4 Results of PERMANOVA main test in terms of biomass used to test the effects of period, area and type of trawl as fixed factors, and their interactions. Fig. 3. Boxplots of temperature (a), salinity (b) and fluorescence (c) along months sampled.
temperatures from northern to southern regions), but also to the topographical and hydrographical features. The Portuguese western coast environment is driven by wind and solar radiation, but the way in which each area (OCN and OCS) responds depends on shelf bathymetry, coastal morphology, river run-off and ocean currents (Cunha, 2001). The northern area is characterized by a wide continental shelf, with a regular coast without important capes and with an intense freshwater runoff, mainly from the rivers Miño, Douro and Mondego. Sardine was clearly one of the characteristic species in the northern region (more than 90% average similarity), which has been reported as an area of recurrent recruitment for this species (Rodríguez-Climent et al., 2017) and also for other typical species from the area, such as horse mackerel (Murta et al., 2008). In productive areas, such as Iberian waters, continental shelf areas influenced by important rivers assure a minimum successful recruitment and act as nursery areas (Uriarte et al., 1996). The freshwater outflows in the northern area explain the lowest values of salinity that we found in that region, and it leads to an earlier stratification of the water column in comparison to the south, giving an early boost to primary production, which is maintained in high levels, with pulses, throughout the summer by the coastal upwelling system
Source
df
SS
MS
Pseudo-F
P(perm)
Unique perms
Pe Ar Tr PexAr PexTr ArxTr PexArxTr Res Total
1 3 1 3 1 3 3 526 541
42460 85262 1.51E+05 14249 6031.1 25646 8110.5 1.10E+06 1.52E+06
42460 28421 1.51E+05 4749.8 6031.1 8548.5 2703.5 2088.8
20.328 13.607 72.194 2.274 2.8874 4.0926 1.2943
0.0001 0.0001 0.0001 0.0036 0.0138 0.0001 0.1781
9932 9912 9935 9909 9938 9919 9919
Significant differences are shown in bold.
(Cunha, 2001). Due to upwelling, zooplankton grazing is very important in northern waters, allowing high encounter rates between fish and their food, and leading to higher aggregation of pelagics (Cunha, 2001). In Iberian waters, pelagic fish species present a high degree of trophic overlap, being calanoid copepods an important prey (Bachiller and Irigoien, 2015; Garrido et al., 2015). Thus, the availability of food for pelagic species depends not only on plankton productivity, but also on the competition with other planktivorous co-occurring in the area of distribution (Garrido et al., 2015). The central area presents an irregular coastline with the presence of several capes, which increases the spatial heterogeneity in plankton distribution, and a shelf area relatively narrow (Cunha, 2001). Narrow
151
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Fig. 4. Distance-based redundancy analysis (dbRDA) to visualize the distance-based linear model (DISTLM) in terms of abundance of the areas studied to the environmental variables (surface temperature, salinity and fluorescence).cad-Cadiz and alg-Algarve.
with the northern area, mainly in the recent period. In Iberian waters, these two species have been reported as trophic competitors, in particular chub mackerel juveniles with sardine (both adults and juveniles individuals) (Garrido et al., 2015). The southern shores of the Atlantic Iberia Peninsula (Algarve and Gulf of Cadiz) are substantially different in its hydrography and dominant environmental forcing. Its zonal orientation, the influence of the warmer waters of the Canary current and the proximity to the
shelf region has a lower biomass of phytoplankton and zooplankton due to its more unstable water mass in which the utilization of nutrients and primary and secondary production are therefore less efficient (Cunha, 2001), and hence, also the food available for pelagic fish species. Landings and estimates from acoustic surveys point generally to lower abundance of sardine south of Lisbon (Zwolinski et al., 2010). In the central region, as well as in southern areas, chub mackerel appeared as a typical species and the importance of sardine decreases in comparison
Fig. 5. Distance-based redundancy analysis (dbRDA) to visualize the distance-based linear model (DISTLM) in terms of biomass of the areas studied to the environmental variables (surface temperature, salinity and fluorescence).cad-Cadiz and alg-Algarve. 152
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landings from the region duplicated partly compensating for sardine scarcity. Also the southern horse mackerel stock, distributed in the western and southern Iberian Peninsula, had several good recruitments in recent years leading to a biomass increase (ICES, 2017). The alternation on multi-annual time scale between two different pelagic species is a widely observed pattern of many regional marine systems (Bakun, 2006). In other worldwide upwelling systems (e.g., California, Benguela and Humboldt current), sardine and anchovy fluctuated out of phase over several decades (Alheit et al., 2009). The alternation between anchovy and sardine periods is probably trophically mediated (van der Lingen et al., 2006, 2009). For the anchovy/ sardine species pair, anchovy frequently prey on larger zooplankton than sardine, and phytoplankton is mostly more important for sardine than for anchovy (van der Lingen et al., 2009). The climatic variations associated to the El Niño events that affect the abundance of pelagic fish (Yáñez et al., 2001) are also related with prey availability. The warmer temperatures in the upper layers during these events, not only enhance sardine recruitment but also lead to a shift in the size spectrum of the crustaceans zooplankton towards smaller size copepods, such as cyclopoids, which are more favorable for sardine (Alheit et al., 2009; van der Lingen et al., 2009). On the other hand, cold conditions (La Niña) were associated to larger copepods, favoring the presence and abundance of anchovy (van der Lingen et al., 2009). In pelagic ecosystems, fish abundance and distribution are related to physical and biological variables (Santos et al., 2013). In this work, there was a significant relationship between pelagic community structure and the physical variables studied (surface temperature, salinity and fluorescence), considering these variables alone. However, in the conditional tests, fluorescence was not significant, showing that a great portion of the variation in the multivariate cloud explained by fluorescence, overlaps with the variability explained by temperature and salinity (Anderson et al., 2008). Several studies reported sea surface temperature outside some optimum range as a factor that negatively affects the recruitment of sardine (Santos et al., 2012; Malta et al., 2016; Garrido et al., 2017; Rodríguez-Climent et al., 2017). Variability in recruitment is related to environmental processes and furthermore, environmental conditions that enhance recruitment for one species could be unfavorable for the recruitment of others (Carrera and Porteiro, 2003; Martins et al., 2013). For example, chub mackerel spawns at higher temperatures than sardine, suggesting that early life stages of chub mackerel are more tolerant to higher temperatures than those stages for sardine (Martins et al., 2013). The environmental variables studied here, only explained 5.8% of the total variability for abundance and 6.8% for biomass. The temperature, salinity and fluorescence measured during specific surveys do not reflect entirely the environment. Habitats characteristics result from a combination of factors of which, geomorphology, river influence, local wind, coastal current patterns and productivity are probably the major forces. Anthropogenic pressure should also be considered to explain the total variability, e.g., fishery exploitation can modify the ability of pelagic species to respond to environmental variability, as a result of the alteration of the structure of populations and ecosystems (Planque et al., 2010). The purse-seine fishery, which target pelagic fish species (sardine, chub mackerel, horse mackerel, blue jack mackerel, atlantic mackerel and anchovy), is one of the most important Portuguese fisheries in terms of landings (50% by weight) (Feijó et al., 2018). For this fishery, the seafloor impact is considered insignificant, but discards (including slipping) could be important (Almeida et al., 2014).
Mediterranean Sea originate a different habitat (Relvas et al., 2007). The Algarve has been characterized as a transition region between the dominance of sardine in the west coast and multispecies pelagic assemblage of the Gulf of Cadiz (Zwolinski et al., 2007). However, our results pointed to a similar pelagic community structure in the central western, region (OCS) and Algarve. The Gulf of Cadiz is a wide basin that connect the Atlantic Ocean and the Mediterranean Sea through the Strait of Gibraltar. Sardine and anchovy are two important typical species in the pelagic community in Cadiz. In fact, in the most recent period anchovy is the species that most contribute to the similarity in this region in terms of number and biomass. The greatest concentrations for anchovy have been reported around the mouth of large rivers: the Guadalquivir, Guadiana, Tinto and Odivel (Uriarte et al., 1996). This gulf, in particular the eastern most wide and shallow area, is a highly suitable habitat for the reproduction of many marine species (Catalán et al., 2006). In particular, the anchovy recruitment in the Gulf of Cadiz is influenced by temperature, wind regimes and discharges from the Guadalquivir river (Ruiz et al., 2006). The river outflow has different effects: low levels of freshwater input constrain primary productivity on the shelf limiting the food for juveniles while very high discharges decrease salinity below the threshold, forcing juveniles to leave the estuary (Ruiz et al., 2009). Depth also influences the community composition, as has been previously reported for pelagic (Santos et al., 2013) and demersal communities that inhabit the continental shelf and upper slope (Fariña et al., 1997). In this study the type of trawl is a proxy for depth. Pelagic trawl was generally used in shallow waters (< 55 m) to caught pelagic fish. In deeper waters the fish usually avoid the pelagic trawl due to the opening of the net. Consequently, we took advantage of the fish avoidance reaction to the vessel noise, i.e., the fish usually goes down, and can be caught with the bottom trawl. The importance of horse mackerel over sardine in the bottom trawls is supported by the distribution area of both species. Young horse mackerel individuals are generally distributed in shallow areas (less than 108 m) and large individuals have a more offshore distribution (Murta et al., 2008). On the other hand, sardine generally occupies shallow coastal waters, being rarely found in depths of more than 100 m (Zwolinski et al., 2010). The bottom trawl is not an efficient sampler for some pelagic species, although these data are useful for studying pelagic distributions when the conservative metric of rate of occurrence in trawls is employed (Montero-Serra et al., 2015). In the studied surveys, where the objective is the abundance estimation of small pelagic species, the bottom trawl was mainly used when schools were detected in deep waters by the echo sounder, being the sampling representative of the species present in that area. Thus, in this work, this bias is smaller than in the demersal surveys. Our results demonstrated a substantial change in the pelagic community structure from the first period (1996 to 2005) to the recent period (2006–2016). The main change was the variation in typical pelagic species, diminishing the importance of sardine and increasing others, such as chub mackerel, horse mackerel, bogue and anchovy. It is widely known that sardine has decreased markedly since 2006 in Iberian waters due to weak recruitments (ICES, 2017). The relative increase in the similarity contribution of chub mackerel observed in the present study is consistent with the results of Martins et al. (2013). Moreover, landings referred in that study showed an inverse correlation of chub mackerel and sardine recruitment indices, which supports the hypothesis of fluctuation in the dominance between these two species (Martins et al., 2013). Such fluctuation may be taking place in the southwest and south Iberian waters, where the two species co-exist. In the Gulf of Cadiz, the fluctuation could be also with the anchovy, which is the species that most contribute to the similarity in the recent period. On the northern Iberian waters, the anchovy shifted from a residual population to a typical species in recent years, following several peaks of recruitment and biomass (ICES, 2017). In a short period anchovy
5. Conclusion Overall, this work has described the pelagic community of several geographical areas in the Iberian waters, which is related to environmental variables (such as surface temperature and salinity). Although these two variables, which are routinely measured in the studied surveys, are significant, most of the variability observed remains 153
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unexplained. Habitat mapping, feeding analyses and effects of pollution and fisheries in the pelagic populations need to be addressed to better understand the influence of other factors in the Iberian pelagic community. In the last decades, the main change in the pelagic community structure was the decrease in importance of sardine and the increasing in others species (e.g. chub mackerel, horse mackerel, bogue and anchovy). Most small short-living pelagic fish species show population highly changing and fluctuating, due to their short life span, fast growth and the strong dependency of the population on recruitment (Uriarte et al., 1996). Long-term monitoring of the communities variability are crucial to follow eventual changes in the system and get support for adequate management advice. Only regular surveying can prevent atypical results due to possible random noise associated to sampling from being misled by real anomalies (Sousa et al., 2005). Analyzing the structure of the pelagic community, such as in this work, is a fundamental step towards a more detailed knowledge of pelagic species distribution, their temporal variation and inter-actions. Thus, contributing to the comprehension of the pelagic community dynamics is fundamental for the ecosystem approach to fisheries management.
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Acknowledgments We are grateful to the crew and colleagues who have carried out the surveys along the years. E. García-Seoane was supported by National Programme for Biological Sampling (PNAB), within the scope of the EU Data Collection Framework (DCF). The IPMA (Instituto Português do Mar e da Atmosfera) acoustic surveys were also undertaken within the framework of PNAB. A. Silva was supported by project Sardinha2020 (MAR2020, Fundo Europeu dos Assuntos Marítimos e das Pescas) and Marine and Environmental Sciences Centre (MARE) funded with project UID/MAR/04292/2013 of the Portuguese Foundation for Science and Technology. We are grateful to the anonymous referees for their constructive comments. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ecss.2019.03.018. References Alheit, J., Roy, C., Kifani, S., 2009. Decadal-scale variability in populations. In: Checkley, D., Alheit, J., Oozeki, Y., Roy, C. (Eds.), Climate Change and Small Pelagic Fish. Cambridge University Press, Cambridge, pp. 64–87. Almeida, C., Vaz, S., Cabral, H., Ziegler, F., 2014. Environmental assessment of sardine (Sardina pilchardus) purse seine fishery in Portugal with LCA methodology including biological impact categories. Int. J. Life Cycle Assess. 19, 297–306. Anderson, M.J., Gorley, R.N., Clarke, R.K., 2008. Permanova+ for Primer: Guide to Software and Statistical Methods. Primer-E Ltd, Plymouth, UK, pp. 214. Bachiller, E., Irigoien, X., 2015. Trophodynamics and diet overlap of small pelagic fish species in the Bay of Biscay. Mar. Ecol. Prog. Ser. 534, 179–198. Bakun, A., 2006. Wasp-waist populations and marine ecosystem dynamics: navigating the “predator pit” topographies. Prog. Oceanogr. 68, 271–288. Berumen, M.L., Pratchett, M.S., 2006. Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef. Moorea. Coral Reefs 25, 647–653. Boero, F., 2009. Recent innovations in marine biology. Mar. Ecol. 30, 1–12. Carrera, P., Porteiro, C., 2003. Stock dynamic of the Iberian sardine (Sardina pilchardus, W.) and its implication on the fishery off Galicia (NW Spain). Sci. Mar. 67, 245–258. Catalán, I.A., Jiménez, M.T., Alconchel, J.I., Prieto, L., Muñoz, J.L., 2006. Spatial and temporal changes of coastal demersal assemblages in the Gulf of Cadiz (SW Spain) in relation to environmental conditions. Deep Sea Res. Part II Top. Stud. Oceanogr. 53, 1402–1419. Cunha, M.E., 2001. Physical Control of Biological Processes in a Coastal Upwelling System: Comparison of the Effects of Coastal Topography, River Run-Off and Physical Oceanography in the Northern and Southern Parts of Western Portuguese Coastal Waters. Faculdade de Ciências. University of Lisbo, Lisbon (Portugal), pp. 305. Drake, P., Arias, A.M., Baldó, F., Cuesta, J.A., Rodríguez, A., Silva-Garcia, A., Sobrino, I., García-González, D., Fernández-Delgado, C., 2002. Spatial and temporal variation of the nekton and hyperbenthos from a temperate European estuary with regulated freshwater inflow. Estuaries 25, 451–468. Elmqvist, T., Folke, C., Nyström, M., Peterson, G., Bengtsson, J., Walker, B., Norberg, J., 2003. Response diversity, ecosystem change, and resilience. Front. Ecol. Environ. 1,
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marine systems. Estuaries 10, 181–193. Yáñez, E., Barbieri, M.A., Silva, C., Nieto, K., Espı́ndola, F., 2001. Climate variability and pelagic fisheries in northern Chile. Prog. Oceanogr. 49, 581–596. Zwolinski, J., Morais, A., Marques, V., Stratoudakis, Y., Fernandes, P.G., 2007. Diel variation in the vertical distribution and schooling behaviour of sardine (Sardina pilchardus) off Portugal. ICES (Int. Counc. Explor. Sea) J. Mar. Sci. 64, 963–972. Zwolinski, J.P., Oliveira, P.B., Quintino, V., Stratoudakis, Y., 2010. Sardine potential habitat and environmental forcing off western Portugal. ICES (Int. Counc. Explor. Sea) J. Mar. Sci. 67, 1553–1564.
Checkley, D.M., Roy, C., Alheit, J., Oozeki, Y. (Eds.), Synthesis Book of the Program “Small Pelagic Fish and Climate Change Program (SPACC)” of Globec International. Cambridge University Press, pp. 392. van der Lingen, C.D., Hutchings, L., Field, J.G., 2006. Comparative trophodynamics of anchovy Engraulis encrasicolus and sardine Sardinops sagax in the southern Benguela: are species alternations between small pelagic fish trophodynamically mediated? Afr. J. Mar. Sci. 28, 465–477. Wolfe, D.A., Champ, M.A., Flemer, D.A., Mearns, A.J., 1987. Long-term biological data sets: their role in research, monitoring, and management of estuarine and coastal
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Spatial and temporal variation in pelagic community of the western and southern Iberian Atlantic waters
T
Eva García-Seoanea,∗,1, Vítor Marquesa, Alexandra Silvaa, Maria Manuel Angélicoa a
Instituto Português do Mar e Atmosfera (IPMA)- Rua Alfredo Magalhães Ramalho, 61495-006, Lisbon, Portugal
A R T I C LE I N FO
A B S T R A C T
Keywords: Community structure Environmental influences Iberian peninsula Pelagic fish Spatio-temporal variation
This study analyzed the spatial and temporal variation in the community composition of the pelagic species inhabiting the Atlantic Iberian waters using a multivariate approach. Trawl data (pelagic and bottom fishing) were collected during the spring acoustic surveys of pelagic fish from 1996 to 2015. There were significant effects of geographical area, periods, and type of trawls in terms of both, abundance and biomass. Sardine was typical throughout the study area whereas other species were typical of few areas, such as anchovy. The main difference between periods was the variation in typical pelagic species, diminishing the importance of sardine and increasing others, such as chub mackerel, bogue or anchovy. Depth also influenced the community structure with horse mackerel being the principally responsible for sample similarity in bottom trawls. Surface temperature and salinity showed significant relationship with the taxa-derived multivariate data cloud but only explained between 5 and 7% of the total variability.
1. Introduction There is a need for information and knowledge at the decadaltemporal scale to support decision making for management (Newton et al., 2014). Long term biological data is extremely valuable for differentiating natural changes from those caused by humans (Wolfe et al., 1987), since natural disturbances tend to be pulse disturbances while human activities tend to transform pulse disturbances into persistent changes (Elmqvist et al., 2003). Permanent changes in community structure tend to be associated with environmental degradation, whereby communities exhibit characteristic shifts in the dominance of species with different life-histories (Berumen and Pratchett, 2006). Ecosystem-based fishery management reverses the order of management priorities, so that management starts with the ecosystem rather than a target species (Pikitch et al., 2004). In that sense, an understanding of the ecological context within which fishery takes place, is required to minimize the adverse impact of fishing and evaluate the long-term capacity of the ecosystem to sustain the catches (Sousa et al., 2005). Hence, it is expressly important to monitor the community composition and spatial distribution over time to evaluate resistance to perturbation (Gomes et al., 2001). In the Iberian waters, pelagic stocks are traditionally assessed and managed using single-species approaches. Despite knowledge on
biological interactions among species (e.g. (Garrido et al., 2015), basic information on their relative abundance and spatial distribution is still scarce. Santos et al. (2013) demonstrated the utility of using trawl data collected during acoustic surveys in order to characterize the pelagic community. These authors, investigated the pelagic community in the north-western and northern Spanish shelf, but knowledge of this community for the west and south Iberian waters is scarce, and mainly come from demersal surveys (Gomes et al., 2001; Sousa et al., 2005), which are focused on fishes associated to the bottom. In Portuguese waters, the pelagic community is composed by small and median pelagics, such as the European sardine Sardina pilchardus, the Chub mackerel Scomber colias, Atlantic horse mackerel Trachurus trachurus, the Atlantic mackerel Scomber scombrus, Blue jack mackerel Trachurus picturatus, the European anchovy Engraulis encrasicolus and the Bogue Boops boops (Feijó et al., 2018). In the last decade, in particular since 2006, the abundance of sardine has decreased abruptly (ICES, 2017). The goal of this paper is to analyze how this reduction in sardine population might have an impact in the other species of the pelagic ecosystem. For that, this paper studies the changes in the community composition of the pelagic species inhabiting the Atlantic Iberian waters (Portuguese shelf and Gulf of Cadiz). This characterization is based on a large data set collected over the past two decades by the acoustic surveys of the Portuguese Institute for the Ocean and
∗
Corresponding author. E-mail address: [email protected] (E. García-Seoane). 1 Present address: Institute of Marine Research (IMR)- P. O. Box 1870 Nordnes, 5817-Bergen, Norway. https://doi.org/10.1016/j.ecss.2019.03.018 Received 12 August 2018; Received in revised form 3 March 2019; Accepted 24 March 2019 Available online 28 March 2019 0272-7714/ © 2019 Elsevier Ltd. All rights reserved.
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beam echo sounder. The hull-mounted transducer has a beam width of 7° x 8° and the transmitted pulse length employed is 1 ms. Several type of trawls (pelagic and bottom) are conducted according to the echogram information, in order to assist in the identification of the species that are reflecting the acoustic energy. The pelagic trawl net has a horizontal opening of 18 m, a vertical opening of 8 m, and a mesh size of 20 mm in the codend. This net captures small pelagic species, from the surface to the bottom. In shallow waters, the net is placed close to the bottom to catch because pelagic fish usually goes to the bottom as a reaction of the ship noise during trawling. Two different bottom trawls were used: the first years a Norwegian Campbell Trawl with rollers in the ground rope and after other otter trawl. Both bottom trawls have a codend mesh size of 20 mm. and they capture small pelagic species near the bottom and also demersal fish. From 1996 to 2015, a total of 18 spring surveys and 628 hauls (496 pelagic and 132 bottom fishing) were conducted during light hours. The haul duration is variable, depending on the number of individuals that enters in the net and the conditions where the fishing takes place. Due to this variability, to the fact thatnets with different sweep areas were routinely used during the surveys, and mainly because the abundance estimations using acoustic energy are not available for most pelagic species, the relative importance of the different species was estimated by each haul. The relative importance was estimated as follow:
the Atmosphere (IPMA). The linkages of these spatial and temporal changes with the environmental variables are also analyzed. A good description of the pelagic community and its correlation with environmental factors is particularly relevant for implementing multispecific approaches to the management of fisheries in the future. 2. Material and methods 2.1. Data collection The IPMA began its spring acoustic surveys in 1986 with the original aim of acquiring the necessary fishery-independent data to conduct the assessment of the sardine stock using acoustic techniques. The acoustic survey PELAGO takes place annually (with some interruptions) during spring (between February and May). This annual survey series had several methodological changes over the years, and nowadays produces not only biomass estimates for sardine and for anchovy but also collects information on other ecosystem components, such as environmental variables and bird census. The sampling area covered each year, extends over the Iberian shelf (including Portuguese waters, western and southern shores and the Spanish coast of the Gulf of Cadiz) between 10-15 m and close to the shelf break (200 m isobath). These surveys are conducted along predefined parallel transects mostly perpendicular to the coast and separated by 8 nautical miles (nmi) on average (Fig. 1). Sampling is conducted during a period of around 30 days and the vessel speed is approximately 8–10 knots. Due to the increased difficulty in attributing echotraces to individual species in the absence of clear school formations at night, and the logistic limitations in crew size surveying was limited to daylight (Zwolinski et al., 2007). The main objective of the survey is monitoring the abundance distribution of small pelagic fish, mainly sardine (S. pilchardus) and anchovy (E. encrasicolus), with acoustics methods. During the survey, acoustic energy backscattered by marine organisms is continuously recorded by a calibrated (Foote et al., 1987) 38 kHz Simrad EK500 split
• Abundance values were converted to percent composition, reducing •
the variability resulting from methodological differences while still retaining the relative abundance of individual taxa within each haul (Mathieson et al., 2000). Biomass values were converted to the percent of biomass, i.e. standardized as the sum of the weight (kg) of each species divided by the total weight of all species in the haul (kg). This process avoids that trawls with higher catches contribute more to the estimated overall composition of the pelagic community (Santos et al., 2013).
From 2000, environmental variables (temperature -°C-, salinity and fluorescence –volts-) have been routinely measured continuously along the track of the acoustics transects from water pumped from 3 m depth by a Continuous, Underway Fish Egg Sampler (CUFES). Surface temperature, salinity and fluorescence were averaged for units of 3 nmi (the standard procedure associated to the CUFES zooplankton samples). Extreme values were removed from the analysis following expert judgment. ESRI ArcMap 10.1.3 was used to calculate the environmental values at the fishing stations. First, temperature, salinity and fluorescence grids of data were interpolated using kriging. The search radius was fixed to 9 nmi in all years, except in 2006 for fluorescence, when the program was unable to estimate the semivariogram with radius less than 21 nmi. Finally, for each year, the environmental measures were estimated at hauls locations extracting the environmental values from the maps previously interpolated. 2.2. Multivariate analysis The multivariate analysis was performed with PRIMER 6 with PERMANOVA + statistical package (Anderson et al., 2008). Individuals of 226 taxa were identified in the hauls (Table S1) but many of them were considered rare since they were very infrequent. In addition, only hauls with at least 100 individuals in total were considered in the analyses. In order to better describe the core of the community and avoid undue relevance to rare species, those with an average percentage of occurrence (i.e., average of the percentage of hauls in which each taxon occurred in relation to the total number of hauls conducted for each survey) < 10% were not considered in the analyses. As a result, a total of 16 taxa were employed in the construction of the data matrix used for multivariate analyses. In spite of being a demersal species, the European hake Merluccius merluccius was retained in our analyses because it was frequently caught in the acoustic surveys.
Fig. 1. Map of the Iberian Peninsula showing the acoustic transects and the boundaries of the areas. 148
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(Fig. 3a). The lowest temperatures coincided with the only survey that started in February (year 2003). Considering inter-annual variability in salinity, the 2001 is highlighted for the low values of surface salinity (median = 34.4, IQR = 2.4) (Fig. 2). These values are probably related with the high levels of precipitation registered during this winter (IPMA, 2018). For fluorescence, the highest medians were found in 2009, 2013 and 2014 perhaps associated to the onset of spring blooms. On the other hand, seasonal differences were not found for surface salinity and fluorescence medians (Fig. 3b and c). However, the dispersion in the fluorescence is higher in April and May, when the spring blooms are already well underway.
Table 1 Number of pelagic and bottom trawls per area (OCN- from Caminha to Nazaré Canyon-, OCS -from Nazaré to Cape S. Vicente-, Algarve -from Cape S. Vicente to V. R. Santo António- and Cadiz -from V. R. Santo António to Cape Trafalgar) and period (1996–2005 and 2006–2015). P - pelagic trawls and B- bottom trawls. 1996–2005 OCN
2006–2015
OCS
ALG
CAD
OCN
OCS
ALG
CAD
P
B
P
B
P
B
P
B
P
B
P
B
P
B
P
B
57
21
67
14
49
5
41
16
59
18
63
16
47
17
34
18
3.2. General description of the pelagic community The Bray-Curtis coefficient was used to calculate similarities of taxa at each sampling haul. Permutational multivariate analysis of variance (PERMANOVA, main test) (Anderson et al., 2008) was performed to test for spatial and temporal differences in the composition of the pelagic community. The PERMANOVA design had the following fixed factors: period (1996–2005, 2006–2015), area (OCNe from Caminha to Nazaré Canyon-, OCS -from Nazaré to Cape S. Vicente-, Algarve -from Cape S. Vicente to V. R. Santo António- and Cadiz -from V. R. Santo António to Cape Trafalgar-, Fig. 1) and fishing trawl type (pelagic trawl and bottom trawl). The selection of these two periods analyzed was based on the marked sardine abundance decrease in Iberian waters since 2006 (ICES, 2017) and selection of the areas on the geomorphology of the shelf and historical records of sardine distribution. The distribution of the hauls between these three factors considered in the analyses is detailed in Table 1. The pair-wise PERMANOVA tests were also made when significant differences were found for the factors. All PERMANOVA procedures were run with 9999 permutations. In addition, a test for homogeneity of multivariate dispersion (PERMDISP with 9999 permutations) was applied. SIMPER analyses were used to identify species that most contributed for similarities among the significant groups tested in the PERMANOVA, considering the significant interactions. Taxa contributing to the average similarity of each sampling site in at least 2% were considered as typical of that site, following criteria defined by Drake et al. (2002). Draftsman plot, which is an ensemble of plots showing each variable plotted against each other variable, was constructed to identify skewness and multi-collinearity for surface temperature, salinity and fluorescence. The relationship between the pelagic community and the environmental variables was explored with distance-based linear model (DISTLM with Adjusted-R2 criterion and forward model selection) and distance-based redundancy analysis (dbRDA) (Legendre and Anderson, 1999; McArdle and Anderson, 2001).
In general, most hauls caught few species, with an average of 5 taxa (ranging from 1 to 13). Fish (13 taxa) dominated the hauls, followed by crustaceans (Henslow's swimming crab Polybius henslowii), which was present in more than one third of the hauls) (Table 2). Cephalopods (Allotheutis spp. and European squid Loligo vulgaris) were present in more than one quarter of the hauls. The most important species in terms of frequency was sardine, which was present in 88% of the hauls (Table 2). Other common species were chub mackerel and bogue, appearing over half of the hauls. 3.3. Pelagic community structure The three PERMANOVA factors analyzed were significant for both pelagic community abundance (Table 3) and biomass (Table 4), as well as the interactions between Period x Area and Area x Trawl. Considering biomass, Period x Trawl is in the boundary of significance (PERMANOVA, P-value = 0.0138). The areas have differences in pelagic community structure (PERMANOVA pair-wise test, P-value < 0.01), except for OCS and ALG, in terms of abundance (PERMANOVA pair-wise test, t = 1.3608, P-value = 0.0884) and biomass (PERMANOVA pair-wise test, t = 1.2717, P-value = 0.1372). In terms of abundance, sardine was typical throughout the study area, contributing at least 21% to the average similarity. In Cadiz, the contribution to similarity of sardine is lower than in the other areas. Other typical species in Cadiz are anchovy (contributing between 16 and 62% to the similarity) and chub mackerel (contributing between 2 and 12% to the similarity) (Table S2). Similar results were found for biomass data (Table S3). These differences between areas were reflected also in both types of trawl (PERMANOVA pair-wise test), being all areas significantly different in both pelagic and bottom samples, except OCS and ALG. However, lower p-values were found for pelagic trawls. For example, when comparing OCS and Algarve in terms of abundance, both trawls showed no significant differences (i.e., P-values > 0.01) between these two areas. For pelagic trawl P-value = 0.0416 (PERMANOVA pair-wise test) whereas for bottom trawl P-value = 0.2184). Bottom trawls were more diverse than pelagics. For abundance data, bottom fishing presented a total of 12 typical species (Alloteuthis spp., bogue, the common two-banded seabream Diplodus vulgaris, anchovy, hake, Axillary seabream Pagellus acarne, P. henslowii, sardine, chub mackerel, atlantic mackerel, jack mackerel and horse mackerel) versus the 4 typical species of pelagic trawls (sardine, chub mackerel, anchovy and bogue) (Table S4). In terms of biomass, the same 4 species were typical of pelagic trawl and 12 for bottom trawl (Table S5). The main differences in comparison with abundance data were that in bottom trawls Black seabream Spondyliosoma cantharus appeared as typical while Alloteuthis spp. was not a typical species. An important difference between periods is the decrease of sardine contribution to the average similarity (in both terms of abundance and biomass) compensated by an increase of other species, such as horse mackerel, anchovy, chub mackerel or bogue. The differences between areas were also stable between the two periods studied, except for OCN and Algarve, which were not significantly different in the first period
3. Results 3.1. Environmental parameters There was an increase in the surface temperatures from north to south, having OCN lower values (median = 14.7 °C, interquartile range -IQR- = 1.6) than Algarve (median = 16.3 °C, IQR = 1.5) (Fig. 2a). The highest temperatures were found in Cadiz (median = 17.1 °C, IQR = 1.9), the easternmost area adjacent to the Mediterranean Sea. Salinity values were also higher in Cadiz and then decreasing towards the west and north. The minimum were observed in OCN (median = 35.5, IQR = 0.9) and maximum in Cadiz and Algarve (medians of 36.1 -IQR = 0.2 - and 36.0 -IQR = 0.2 - respectively) (Fig. 2c). For fluorescence, the median values (and also the dispersion) were higher in OCN in comparison with the other areas (Fig. 2e). There was substantial inter-annual variability in surface temperature (Fig. 2b). However, it is important to note that this variability is also influenced by the period during which the survey was conducted 149
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Fig. 2. Boxplots of temperature, salinity and fluorescence along the areas (left plots) and the surveys (right plots). The middle line indicates the median and extremities of the box are the 25th and 75th percentiles. The maximum length of each whisker represents the 1.5 times the interquartile range, but when no points exceed this distance, the whiskers represent the minimum or maximum values.
4. Discussion
(1996–2005) in both in terms of abundance and of biomass. However, it is important to note that it is in the boundary of the significance (Pvalue = 0.0153 for abundance and P-value = 0.0119 for biomass). The pair-wise analyses of the interaction terms showed that the differences in the structure of the pelagic community between the two periods are present in all areas. In the first period (1996–2005), sardine contributed from 96 to 78% in terms of abundance, and from 96 to 79% in terms of biomass, whereas in the second (2006–2015) only contributed from 85 to 21% in abundance and from 86 to 26% in biomass (Tables S2 and S3). In fact, during the second period, anchovy is the species that contributed the most to the similarity in Cadiz (in both abundance and biomass data). The order of importance of the other pelagic species differed for abundance and biomass in the different areas. PERMDISP tests were significant for the three factors analyzed: period, area and type of trawl (PERMDISP, P-values < 0.01), except for area in abundance, but it is in the boundary (P-values = 0.015). These results indicate heterogeneity of multivariate dispersion among groups in most of cases.
Identifying the habitats that fish species use is vital to apply the ecosystem-based approach to fisheries management (Levin and Stunz, 2005). The usage of long-term data sets, like in this study, is very relevant for establishing reference conditions and assess fluctuations and trends in the communities composition (Boero, 2009). In the most productive regions of the world oceans, particularly in the upwelling regions, small pelagic fish, such as sardines and anchovies, occupy an intermediate trophic level in the coastal marine food webs, having a key role as food source for a wide range of predators (Bakun, 2006). A characteristic of the upwelling ecosystems is the occurrence of decadal fluctuations in species abundance and sometimes species replacement (Alheit et al., 2009). These modifications appear to be caused by environmental variability and are often amplified by fishing pressure (Alheit et al., 2009; Essington et al., 2015). Our results indicate that a relatively small number of species in the pelagic community predominates in the western and southern waters of the Iberian Peninsula, as has been reported for the pelagic community of the north and northwestern Iberian waters (Santos et al., 2013). However, in the northern Iberian waters the most frequent species was the Atlantic mackerel, being sardine as important in terms of biomass as horse mackerel and bogue (Santos et al., 2013). Further south, in our study, despite spatial and temporal variations, sardine was clearly predominant in the western and southern waters. The dominance of one or a few pelagic species appears to be a common characteristic of upwelling systems (Bakun, 2006). The variability in community composition was in part geographical, as shown by the significant effect of the variable area in the PERMANOVA. The present work showed three distinct geographical areas with mostly persistent typical pelagic species along the western and southern Iberian waters: the northern area (OCN), the central and south western area (OCS and Algarve) and the Gulf of Cadiz. The differences between areas are not only associated to the latitude gradient (with increasing
3.4. Relationship between pelagic community and environmental parameters Draftsman plot did not detect skewness nor outliers. Additionally, the three environment variables were tested and none was collinear. In the marginal test of DISTLM, surface temperature, salinity and fluorescence showed significant relationship with the taxa-derived multivariate data cloud (P < 0.001). However, together these variables explained only 5.8% of the total variability in the data cloud for abundance (Table S6) and 6.8% for biomass (Table S7). There was some discrimination of the areas along the RDA axis 1, with OCN samples more associated to low surface temperatures and a wide range of salinity variations while Cadiz and Algarve samples more associated to high temperatures (Fig. 4). Similar results were found for biomass data (Fig. 5). 150
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Table 2 Percentage of hauls containing each taxa in a total of 542 hauls analyzed. Taxa
Percentage of hauls (%)
Fish Boops boops Diplodus vulgaris Engraulis encrasicolus Merluccius merluccius Pagellus acarne Pagellus erythrinus Sardina pilchardus Scomber colias Scomber scombrus Spondyliosoma cantharus Trachurus mediterraneus Trachurus picturatus Trachurus trachurus
53 15 39 30 13 16 88 58 40 21 10 16 47
Cephalopods Alloteuthis spp. Loligo vulgaris
24 13
Crustaceans Polybius henslowii
36
Table 3 Results of PERMANOVA main test in terms of abundance used to test the effects of period, area and type of trawl as fixed factors, and their interactions. Source
df
SS
MS
Pseudo-F
P(perm)
Unique perms
Pe Ar Tr PexAr PexTr ArxTr PexArxTr Res Total
1 3 1 3 1 3 3 526 541
40573 92044 1.42E+05 13817 4474.3 22265 8998.7 1.13E+06 1.54E+06
40573 30681 1.42E+05 4605.6 4474.3 7421.7 2999.6 2149.7
18.874 14.273 65.93 2.1424 2.0814 3.4525 1.3954
0.0001 0.0001 0.0001 0.0053 0.052 0.0001 0.1175
9934 9903 9934 9907 9934 9898 9915
Significant differences are shown in bold. Table 4 Results of PERMANOVA main test in terms of biomass used to test the effects of period, area and type of trawl as fixed factors, and their interactions. Fig. 3. Boxplots of temperature (a), salinity (b) and fluorescence (c) along months sampled.
temperatures from northern to southern regions), but also to the topographical and hydrographical features. The Portuguese western coast environment is driven by wind and solar radiation, but the way in which each area (OCN and OCS) responds depends on shelf bathymetry, coastal morphology, river run-off and ocean currents (Cunha, 2001). The northern area is characterized by a wide continental shelf, with a regular coast without important capes and with an intense freshwater runoff, mainly from the rivers Miño, Douro and Mondego. Sardine was clearly one of the characteristic species in the northern region (more than 90% average similarity), which has been reported as an area of recurrent recruitment for this species (Rodríguez-Climent et al., 2017) and also for other typical species from the area, such as horse mackerel (Murta et al., 2008). In productive areas, such as Iberian waters, continental shelf areas influenced by important rivers assure a minimum successful recruitment and act as nursery areas (Uriarte et al., 1996). The freshwater outflows in the northern area explain the lowest values of salinity that we found in that region, and it leads to an earlier stratification of the water column in comparison to the south, giving an early boost to primary production, which is maintained in high levels, with pulses, throughout the summer by the coastal upwelling system
Source
df
SS
MS
Pseudo-F
P(perm)
Unique perms
Pe Ar Tr PexAr PexTr ArxTr PexArxTr Res Total
1 3 1 3 1 3 3 526 541
42460 85262 1.51E+05 14249 6031.1 25646 8110.5 1.10E+06 1.52E+06
42460 28421 1.51E+05 4749.8 6031.1 8548.5 2703.5 2088.8
20.328 13.607 72.194 2.274 2.8874 4.0926 1.2943
0.0001 0.0001 0.0001 0.0036 0.0138 0.0001 0.1781
9932 9912 9935 9909 9938 9919 9919
Significant differences are shown in bold.
(Cunha, 2001). Due to upwelling, zooplankton grazing is very important in northern waters, allowing high encounter rates between fish and their food, and leading to higher aggregation of pelagics (Cunha, 2001). In Iberian waters, pelagic fish species present a high degree of trophic overlap, being calanoid copepods an important prey (Bachiller and Irigoien, 2015; Garrido et al., 2015). Thus, the availability of food for pelagic species depends not only on plankton productivity, but also on the competition with other planktivorous co-occurring in the area of distribution (Garrido et al., 2015). The central area presents an irregular coastline with the presence of several capes, which increases the spatial heterogeneity in plankton distribution, and a shelf area relatively narrow (Cunha, 2001). Narrow
151
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Fig. 4. Distance-based redundancy analysis (dbRDA) to visualize the distance-based linear model (DISTLM) in terms of abundance of the areas studied to the environmental variables (surface temperature, salinity and fluorescence).cad-Cadiz and alg-Algarve.
with the northern area, mainly in the recent period. In Iberian waters, these two species have been reported as trophic competitors, in particular chub mackerel juveniles with sardine (both adults and juveniles individuals) (Garrido et al., 2015). The southern shores of the Atlantic Iberia Peninsula (Algarve and Gulf of Cadiz) are substantially different in its hydrography and dominant environmental forcing. Its zonal orientation, the influence of the warmer waters of the Canary current and the proximity to the
shelf region has a lower biomass of phytoplankton and zooplankton due to its more unstable water mass in which the utilization of nutrients and primary and secondary production are therefore less efficient (Cunha, 2001), and hence, also the food available for pelagic fish species. Landings and estimates from acoustic surveys point generally to lower abundance of sardine south of Lisbon (Zwolinski et al., 2010). In the central region, as well as in southern areas, chub mackerel appeared as a typical species and the importance of sardine decreases in comparison
Fig. 5. Distance-based redundancy analysis (dbRDA) to visualize the distance-based linear model (DISTLM) in terms of biomass of the areas studied to the environmental variables (surface temperature, salinity and fluorescence).cad-Cadiz and alg-Algarve. 152
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landings from the region duplicated partly compensating for sardine scarcity. Also the southern horse mackerel stock, distributed in the western and southern Iberian Peninsula, had several good recruitments in recent years leading to a biomass increase (ICES, 2017). The alternation on multi-annual time scale between two different pelagic species is a widely observed pattern of many regional marine systems (Bakun, 2006). In other worldwide upwelling systems (e.g., California, Benguela and Humboldt current), sardine and anchovy fluctuated out of phase over several decades (Alheit et al., 2009). The alternation between anchovy and sardine periods is probably trophically mediated (van der Lingen et al., 2006, 2009). For the anchovy/ sardine species pair, anchovy frequently prey on larger zooplankton than sardine, and phytoplankton is mostly more important for sardine than for anchovy (van der Lingen et al., 2009). The climatic variations associated to the El Niño events that affect the abundance of pelagic fish (Yáñez et al., 2001) are also related with prey availability. The warmer temperatures in the upper layers during these events, not only enhance sardine recruitment but also lead to a shift in the size spectrum of the crustaceans zooplankton towards smaller size copepods, such as cyclopoids, which are more favorable for sardine (Alheit et al., 2009; van der Lingen et al., 2009). On the other hand, cold conditions (La Niña) were associated to larger copepods, favoring the presence and abundance of anchovy (van der Lingen et al., 2009). In pelagic ecosystems, fish abundance and distribution are related to physical and biological variables (Santos et al., 2013). In this work, there was a significant relationship between pelagic community structure and the physical variables studied (surface temperature, salinity and fluorescence), considering these variables alone. However, in the conditional tests, fluorescence was not significant, showing that a great portion of the variation in the multivariate cloud explained by fluorescence, overlaps with the variability explained by temperature and salinity (Anderson et al., 2008). Several studies reported sea surface temperature outside some optimum range as a factor that negatively affects the recruitment of sardine (Santos et al., 2012; Malta et al., 2016; Garrido et al., 2017; Rodríguez-Climent et al., 2017). Variability in recruitment is related to environmental processes and furthermore, environmental conditions that enhance recruitment for one species could be unfavorable for the recruitment of others (Carrera and Porteiro, 2003; Martins et al., 2013). For example, chub mackerel spawns at higher temperatures than sardine, suggesting that early life stages of chub mackerel are more tolerant to higher temperatures than those stages for sardine (Martins et al., 2013). The environmental variables studied here, only explained 5.8% of the total variability for abundance and 6.8% for biomass. The temperature, salinity and fluorescence measured during specific surveys do not reflect entirely the environment. Habitats characteristics result from a combination of factors of which, geomorphology, river influence, local wind, coastal current patterns and productivity are probably the major forces. Anthropogenic pressure should also be considered to explain the total variability, e.g., fishery exploitation can modify the ability of pelagic species to respond to environmental variability, as a result of the alteration of the structure of populations and ecosystems (Planque et al., 2010). The purse-seine fishery, which target pelagic fish species (sardine, chub mackerel, horse mackerel, blue jack mackerel, atlantic mackerel and anchovy), is one of the most important Portuguese fisheries in terms of landings (50% by weight) (Feijó et al., 2018). For this fishery, the seafloor impact is considered insignificant, but discards (including slipping) could be important (Almeida et al., 2014).
Mediterranean Sea originate a different habitat (Relvas et al., 2007). The Algarve has been characterized as a transition region between the dominance of sardine in the west coast and multispecies pelagic assemblage of the Gulf of Cadiz (Zwolinski et al., 2007). However, our results pointed to a similar pelagic community structure in the central western, region (OCS) and Algarve. The Gulf of Cadiz is a wide basin that connect the Atlantic Ocean and the Mediterranean Sea through the Strait of Gibraltar. Sardine and anchovy are two important typical species in the pelagic community in Cadiz. In fact, in the most recent period anchovy is the species that most contribute to the similarity in this region in terms of number and biomass. The greatest concentrations for anchovy have been reported around the mouth of large rivers: the Guadalquivir, Guadiana, Tinto and Odivel (Uriarte et al., 1996). This gulf, in particular the eastern most wide and shallow area, is a highly suitable habitat for the reproduction of many marine species (Catalán et al., 2006). In particular, the anchovy recruitment in the Gulf of Cadiz is influenced by temperature, wind regimes and discharges from the Guadalquivir river (Ruiz et al., 2006). The river outflow has different effects: low levels of freshwater input constrain primary productivity on the shelf limiting the food for juveniles while very high discharges decrease salinity below the threshold, forcing juveniles to leave the estuary (Ruiz et al., 2009). Depth also influences the community composition, as has been previously reported for pelagic (Santos et al., 2013) and demersal communities that inhabit the continental shelf and upper slope (Fariña et al., 1997). In this study the type of trawl is a proxy for depth. Pelagic trawl was generally used in shallow waters (< 55 m) to caught pelagic fish. In deeper waters the fish usually avoid the pelagic trawl due to the opening of the net. Consequently, we took advantage of the fish avoidance reaction to the vessel noise, i.e., the fish usually goes down, and can be caught with the bottom trawl. The importance of horse mackerel over sardine in the bottom trawls is supported by the distribution area of both species. Young horse mackerel individuals are generally distributed in shallow areas (less than 108 m) and large individuals have a more offshore distribution (Murta et al., 2008). On the other hand, sardine generally occupies shallow coastal waters, being rarely found in depths of more than 100 m (Zwolinski et al., 2010). The bottom trawl is not an efficient sampler for some pelagic species, although these data are useful for studying pelagic distributions when the conservative metric of rate of occurrence in trawls is employed (Montero-Serra et al., 2015). In the studied surveys, where the objective is the abundance estimation of small pelagic species, the bottom trawl was mainly used when schools were detected in deep waters by the echo sounder, being the sampling representative of the species present in that area. Thus, in this work, this bias is smaller than in the demersal surveys. Our results demonstrated a substantial change in the pelagic community structure from the first period (1996 to 2005) to the recent period (2006–2016). The main change was the variation in typical pelagic species, diminishing the importance of sardine and increasing others, such as chub mackerel, horse mackerel, bogue and anchovy. It is widely known that sardine has decreased markedly since 2006 in Iberian waters due to weak recruitments (ICES, 2017). The relative increase in the similarity contribution of chub mackerel observed in the present study is consistent with the results of Martins et al. (2013). Moreover, landings referred in that study showed an inverse correlation of chub mackerel and sardine recruitment indices, which supports the hypothesis of fluctuation in the dominance between these two species (Martins et al., 2013). Such fluctuation may be taking place in the southwest and south Iberian waters, where the two species co-exist. In the Gulf of Cadiz, the fluctuation could be also with the anchovy, which is the species that most contribute to the similarity in the recent period. On the northern Iberian waters, the anchovy shifted from a residual population to a typical species in recent years, following several peaks of recruitment and biomass (ICES, 2017). In a short period anchovy
5. Conclusion Overall, this work has described the pelagic community of several geographical areas in the Iberian waters, which is related to environmental variables (such as surface temperature and salinity). Although these two variables, which are routinely measured in the studied surveys, are significant, most of the variability observed remains 153
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unexplained. Habitat mapping, feeding analyses and effects of pollution and fisheries in the pelagic populations need to be addressed to better understand the influence of other factors in the Iberian pelagic community. In the last decades, the main change in the pelagic community structure was the decrease in importance of sardine and the increasing in others species (e.g. chub mackerel, horse mackerel, bogue and anchovy). Most small short-living pelagic fish species show population highly changing and fluctuating, due to their short life span, fast growth and the strong dependency of the population on recruitment (Uriarte et al., 1996). Long-term monitoring of the communities variability are crucial to follow eventual changes in the system and get support for adequate management advice. Only regular surveying can prevent atypical results due to possible random noise associated to sampling from being misled by real anomalies (Sousa et al., 2005). Analyzing the structure of the pelagic community, such as in this work, is a fundamental step towards a more detailed knowledge of pelagic species distribution, their temporal variation and inter-actions. Thus, contributing to the comprehension of the pelagic community dynamics is fundamental for the ecosystem approach to fisheries management.
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