Relationships between Octopus vulgaris landings and environmental factors in the northern Alboran Sea (Southwestern Mediterranean)

Fisheries Research 99 (2009) 159–167

Contents lists available at ScienceDirect

Fisheries Research journal homepage: www.elsevier.com/locate/fishres

Relationships between Octopus vulgaris landings and environmental factors in the northern Alboran Sea (Southwestern Mediterranean) ˜ ∗ , F. Moya, M. García-Martínez, J. Rey, M. González, P. Zunino M. Vargas-Yánez Instituto Espa˜ nol de Oceanografía, C.O. Málaga (Fuengirola), Puerto pesquero de Fuengirola s/n, 29640 Fuengirola, Málaga, Spain

a r t i c l e

i n f o

Article history: Received 13 February 2009 Received in revised form 14 May 2009 Accepted 24 May 2009 Keywords: Octopus vulgaris Alboran Sea Environmental factors Predictive model

a b s t r a c t The relationships between environmental factors and fluctuations in Octopus vulgaris landings in the northern Alboran Sea are studied from 1987 to 2007. Landings during this period show both a long term decrease and a strong inter-annual variability. An exploratory phase revealed that local coastal temperatures and those averaged for the whole Alboran Sea during the previous year were the main factors controlling such variability. Warm anomalies have a detrimental effect on the octopus landings on the following year and this suggests that the decreasing trend in octopus landings could be partially linked to the long term warming observed in the Western Mediterranean. It is not yet clear which are the specific mechanisms linking warm anomalies to landing decrease. Nevertheless some hypotheses are proposed and a statistical model is developed for attempting to predict octopus landings one year ahead. © 2009 Elsevier B.V. All rights reserved.

1. Introduction Abundance of fish stocks can experience large fluctuations caused by both natural and man-made factors (Rosenzweig et al., 2007). In the case of short life-cycle species the stock abundance is very sensitive to the strength of annual recruitment (Caddy, 1983; Fogarty, 1989) and the latter seems to be modulated or highly influenced by a large set of environmental factors. Temperature seems to be a main factor controlling the distribution and abundance of fish populations and temperature anomalies can be responsible for stock fluctuations at both the inter-annual and long term time scale. The influence of temperature depends on the species considered. MacKenzie and Koster (2004) showed that the warming of the Baltic Sea increased the abundance of Sprattus sprattus and similar results were found by Sabatés et al. (2006) for Sardinella aurita in the Western Mediterranean. Contrary to this positive influence, those species occupying the southern limit of their geographical range can be negatively affected by the northward progression of warm anomalies as could be the case for cod in the North Sea (Stenevik and Sundby, 2007). Other environmental variables influencing recruitment strength and stock abundances are salinity, light, rainfall rates or dispersion/retention processes and food availability linked to the time variability of the main wind and current systems (Pierce, 1995; Sobrino et al., 2002; Roberts and van den

∗ Corresponding author. Tel.: +34 952 197124; fax: +34 952 463808. ˜ E-mail address: [email protected] (M. Vargas-Yánez). 0165-7836/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2009.05.013

Berg, 2002; Suda et al., 2005; Stenevik and Sundby, 2007; Bellido et al., 2008). In the case of cephalopod species, annual recruitment seems to be responsible for the entire stock biomass and therefore these animals could be especially susceptible to environmental variability (Caddy, 1983; Pierce, 1995; Boyle and Rodhouse, 2005; Pierce et al., 2008). Numerous works have evidenced this sort of environmental–abundance relationships. Wang et al. (2003) found a positive correlation between Sea Surface Temperature (SST) and the abundance of Sepia officinalis in the English Channel. These authors suggested that the link between SST and cuttlefish abundances could be through the beneficial effect of high temperatures on the embryonic and larval development. Pierce (1995) and Pierce et al. (1998) also found a positive relationship between temperature and salinity in the Scottish waters and the abundance of squid Loligo forbesi. These authors considered that temperature could influence the larval growth but also pointed out that the positive correlation with temperature could simply be an indication of a more complex process involving warm and salty water advection from the North Atlantic current. Bazzino et al. (2005) reported higher abundances of the squid Illex argentinus in the Patagonian shelf associated with low temperatures. Once again, temperature anomalies were considered as an indicator of complex oceanographic processes such as upwelling and other processes associated with frontal systems. According to these authors, the nutrient enriched frontal waters would favor the primary production and it would be transferred to higher trophic levels. In the case of Octopus vulgaris, Balguerias et al. (2002) showed that the abundance of this species in the Saharan bank was influenced by temperature, but a small scale analysis

160

M. Vargas-Yᘠnez et al. / Fisheries Research 99 (2009) 159–167

revealed that positive and negative correlations were found for different sub-regions. Sobrino et al. (2002) found that low temperatures in spring favored higher O. vulgaris catches during the next fishing season. These authors also reported a negative and significant correlation with rainfall during the preceding rainy season. Faure et al. (2000) showed that octopus recruitment in Mauritania could be dependent on upwelling/retention processes. González et al. (2005) studied the distribution of octopus paralarvae in Galician waters. In the same geographical area, Otero et al. (2007) carried out morphometric analysis of octopus catches and Otero et al. (2008) studied the relationship between octopus landings and environmental variables. These works suggested that the reproductive cycle and the strength of O. vulgaris recruitment was modulated by the seasonal pattern of upwelling in the Galician waters. The Alboran Sea is the westernmost basin of the Mediterranean Sea (Fig. 1) and is an area where many different oceanographic processes and complex physical–biological interactions take place. Because of the thermohaline circulation of the Mediterranean, a swift current of Atlantic Water (AW) flows into the Mediterranean Sea through the Strait of Gibraltar, while an undercurrent of Mediterranean origin flows westwards and overflows into the Atlantic Ocean. The Atlantic current describes two anticyclonic gyres where surface waters accumulate (Fig. 1), creating very oligotrophic conditions to the south of the Alboarn Sea. Ageostrophic circulation induces upward vertical velocities in the northern part of the basin increasing primary production (Morán and Estrada, 2001). This general circulation pattern creates a strong frontal sys˜ et al., 2008 tem known as the Alboran Sea front (see Vargas Yánez and references therein for a review) which roughly coincides with the northern boundary of the Atlantic current (Fig. 1) and which is evidenced by strong thermal, haline and trophic north–south gradients. Beside these processes, several areas to the north of this frontal zone are occupied by cyclonic circulation areas (Fig. 1) enhancing primary production. Prevailing winds blow from the west (Parrilla and Kinder, 1987), favoring upwelling by Ekman transport. Sarhan et al. (2000) have reported an Alboran-specific upwelling process which would be linked to the southward displacements of the Atlantic current. The influence of the Alboran Sea upper layer circulation and the upwelling/downwelling processes on the icthyo and zooplanktonic distributions have been extensively studied (Vargas˜ and Sabatés, 2007; Rubín, 1997) but very little is known about Yánez the influence of these oceanographic conditions and environmental factors on the abundance of fish stocks. In the particular case of common octopus, Belcari et al. (2002) have studied its spatial distribution in the Mediterranean Sea, showing that it is a neritic species being more abundant in the 10–100 m depth range and Sánchez and Obarti (1993) studied some aspects of the biology and

clay pots fishery in the Spanish Mediterranean. Nevertheless, to our knowledge, no attempts have been made to relate the fluctuations in abundance and landings of O. vulgaris in the Alboran Sea to the variability of environmental conditions in this highly productive area of the Mediterranean Sea. The present work is aimed at detecting those environmental variables which have a larger influence on the inter-annual and long term variability of common octopus landings within the northern Alboran Sea. After an exploratory analysis we test the hypothesis that temperature is the main variable influencing such variability and explore the possibility of using it as a proxy for predicting octopus landings. 2. Material and methods 2.1. Fishery data Monthly octopus landings from 1987 to 2007 were obtained at eight ports covering almost the whole northern coast of the Alboran Sea (Fig. 1). Data were compiled from three different sources: The Spanish Fishery and Agriculture Ministry, the Agriculture and Fishery council from the Andalusia regional government and from ˜ de Oceanografía (IEO) sampling networks. the Instituto Espanol Octopus fishery is a multi-gear one (Fernández and Esteban, 2003). Landings from different gears are pooled in the statistics from 1987 to 2001 and fishing effort statistics are not available for this period. From 2002 to 2007 fishing days and landings from the bottom trawl and artisanal fleets were available. Data for this second period have been used for calculating correlations between landings and landings per unit effort. Total monthly landings from 1987 to 2007 (bottom trawl and artisanal fleets pooled) in the three best sampled ports (Marbella, Estepona and Fuengirola) have been used to analyze abundance–environmental relationships. 2.2. Environmental data Monthly SST data were collected from 1986 to 2007 from ICOADS (International comprehensive Oceanographic and Atmospheric Data base from the National Oceanographic and Atmospheric Agency, NOAA, http://icoads.noaa.gov/). This data set has a 1◦ × 1◦ resolution. Time series for those grid points within a square 5.5◦ W/2◦ W and 35.5◦ N/37◦ N were averaged to produce a monthly time series representing those temperature conditions in the Alboran Sea. ICOADS data set has a low spatial resolution and the northern Alboran Sea presents strong north–south temperature gradients. In order to get information about temperature variability within the coastal zone we collected monthly temperature time series in the Fuengirola beach (TF ; hereafter) from the web site of the ˜ de Mediterranean Group on Climate Change from Instituto Espanol Oceanografía (GCC, http://www.ma.ieo.es/gcc). We also obtained three-monthly time series of temperature vertical profiles in the Fuengirola continental shelf from the project RADMED (“Series Temporales de Datos Oceanográficos”, time series of oceanographic data) funded by IEO. Monthly rainfall rates (R) were obtained from the NCEP (Nacional Center for Environmental Prediction/Reanalysis Project, provided by NOAA-CIRES Climate Diagnostics Center, Boulder, Colorado, USA, http://www.cdc.noaa.gov/). Ekman transport (Qy ) along the northern Alboran Sea coast was calculated from east–west wind stress time series ( x ) also from NCEP. Data from NCEP have a 1.8◦ × 1.8◦ resolution and were averaged over the same square used for SST data. 2.3. Data analysis

Fig. 1. Alboran Sea and the ports where octopus landings were compiled. Grey lines describe the main circulation patterns in the upper layer. A stands for anticyclonic and C for cyclonic circulation areas. The square is the area where ICOADS and NCEP data were averaged. The arrow and circle indicate the position of the station were vertical temperature profiles were collected.

In order to detect the existence of a seasonal or annual cycle in octopus landings, mean values were calculated for each month of the year over the whole period. 95% confidence intervals were

M. Vargas-Yᘠnez et al. / Fisheries Research 99 (2009) 159–167

calculated by means of t-tests (Zar, 1984; for instance). Nevertheless, the main objective of the present work is to carry out an exploratory analysis of octopus landings inter-annual variability and their relationships with environmental factors. For this purpose, monthly time series were averaged to obtain annual landings time series. Several works have revealed that rainfall rates, temperature (Sobrino et al., 2002) or wind intensity (Faure et al., 2000; Otero et al., 2008) have a different influence on the strength of recruitment and octopus abundances depending on the season of the year when the environmental variable was considered, and in all of these studies this influence was delayed in time. Therefore, in a preliminary analysis we considered as response variable the annual landings (L(t)) and as predictor variables SST, TF , R and Qy for the four seasons (winter, spring, summer and autumn) on the preceding year (t − 1). Response and predictor time series were de-trended subtracting a strait line by means of least squared fit: L(t) = a + bt + ε(t)

(1)

where L(t) is landings in metric tons for year t. a is the intercept and b the slope or rate of change in tons per year. ε(t) represents a zero mean anomaly or deviation which contains the information about inter-annual variability, which we hypothesize to be determined by environmental inter-annual variability. The same de-trending was applied to all the predictor variables and time series were tested for normality by means of Kolmogórov–Smirnov tests. On one hand, this procedure allows us to detect the possible existence of long term trends in octopus abundances and their relation with long term changes in environmental factors. On the other hand, long term variability, even in the case of not being statistically significant or not having a known cause, introduces a serial autocorrelation in time series that can produce spurious correlations and should be removed previously to the analysis (Pierce, 1995). Although those variables initially considered (temperature, rainfall rates and Ekman transport) are very likely candidates to have some influence on octopus abundance, they constitute a very large number of variables. In order to keep a predictive model as simple as possible, a preliminary analysis consisted in the calculation of Pearson correlation coefficients between landing anomalies and environmental variables following the strategy used by Sobrino et al. (2002). The aim of this analysis was to detect which variables should be considered in the linear multivariate analysis, keeping a low number of predictor variables and parameters. Those variables not correlated with octopus landings were discarded. Then, in order to select a set of candidate models to explain the inter-annual fluctuations of octopus abundance, we performed an exploratory study using a forward stepwise linear regression: ε(t) =



ˇk Vk (t − 1) + z(t)

(2)

k

where ε(t) is landing anomalies, Vk the predictor variables and z(t) the errors or part of the landings which remains unexplained by the model. Errors were tested for normality and statistical independence. Predictor variables were checked for co-linearity regressing each predictor on the rest of them. If the unexplained variance was lower than 10% of the initial predictor variance it was eliminated from the analysis. Stepwise linear regression was repeated 21 times, each time leaving out the predictor and response data corresponding to one of the 21 years. At each step the forward stepwise analysis was allowed to select a different set of predictor variables. The purpose of this preliminary analysis was to check which variables had a larger influence on octopus abundance and to provide an initial set of candidate models. The final “best” model was selected in a secondary analysis using an Akaike Information Criterion. AICc was

161

used instead of AIC because of the low number of data points (see Burnham and Anderson, 2002 and references therein). The reliability of the best model selected was also tested by means of a cross-validation method (Francis, 2006; Lavín et al., 2007). First we used a one-leave-out procedure similar to the one used in the exploratory phase. That is, we proceeded with 21 steps. In each step we leaved out the data corresponding to one of the years and fit the “best” selected model to the remaining 20 years of data. The fitted linear model was used to estimate landing anomalies for the left-out year and differences with the observed ones were used to calculate a mean square error (MSE). The MSE was compared with a default one based on the mean value of landings. Notice the difference with the exploratory phase when at each step different predictor variables could enter the model. Now, the linear regression considers always those predictors selected by means of the AICc criterion. According to Francis (2006) the reliability of the model can be tested by means of the statistic PVE (percent variance explained): PVE =

100(MSEdefault − MSE) MSEdefault

(3)

Positive values of this statistic indicate that the model MSE is lower and therefore improves the default one. A second crossvalidation test was carried out predicting the octopus landings on the following year. That is, we considered predictors and response variables on years 1 to t. By applying the best model selected we predicted landing anomalies on year t + 1. The differences between predicted and observed landings were used to compute a MSE which once again was compared with a default prediction based on the mean value of landings from year 1 to t. 3. Results 3.1. Landings and landings per unit effort Fig. 2A shows total landings and trawl landings versus fishing effort for the years 2002 to 2007. Fig. 2B shows the scatter plot for landings versus LPUE and Fig. 2C and D provide the same information for landings from the artisanal fleet. We have to admit that the time series with complete information about fishing gears and effort are too short to obtain statistically significant results and this is one of the main shortcomings of the available data set. Nevertheless, Fig. 2 shows no correlation between landings and effort and a positive correlation between landings and LPUE suggesting that octopus landings can be considered as an index of abundance in the Alboran Sea. 3.2. Seasonal cycle and long term trends Fig. 3 shows the mean values of landings for each month of the year. Fig. 3A corresponds to the total landings adding those of the three analyzed ports (Marbella, Estepona and Fuengirola) and Fig. 3B shows the annual cycle for each of the ports considered. The 95% confidence intervals for the estimated means were calculated in all the cases although it has only been included in Fig. 3A for the clarity of the plot. Landings seem to have two relative minima, one in spring and a secondary minimum in August–September with the only exception of Marbella landings where one single minimum is observed in spring. Fig. 4 shows the seasonal cycle of temperature at the sea surface (Fig. 4A, triangles-solid line) and at 25 m depth (Fig. 4B) in the Fuengirola continental shelf. Notice that the maximum of temperature occurs in August at the surface and 25 m. Octopus landings in the Alboran Sea showed a decreasing linear trend of −8.58 ± 8.66 t/year which is only marginally significant (p < 0.1). Fig. 5A shows the octopus landings and the de-trended or zero mean anomaly time series. Fig. 5B–D show the temperature

162

M. Vargas-Yᘠnez et al. / Fisheries Research 99 (2009) 159–167

Fig. 2. (A) Landings (all gears) in tons versus fishing days for total landings (black filled triangles) and bottom trawl (open triangles). (B) shows landings (t) versus landings per unit effort calculated as landings divided by the number of fishing days. Symbols follow the same criterion as in (A). (C) and (D) are the same as in (A) and (B), but for artisanal fleet landings.

Fig. 3. (A) Mean octopus landings for each month of the year. Means have been calculated using the complete series from 1987 to 2007. Vertical error bars are the 95% confidence interval for the means calculated using a t-test. (B) Is the same as (A) for each of the three ports studied: Marbella, Estepona and Fuengirola. May month has not been included because of the temporary ban for trawl fishery established since 2000.

Fig. 4. Thick solid black line is the length (in days) of the embryonic development as a function of the spawning day (bottom axis). Dashed black line is the length of the larval phase, that is, from hatching to settlement, and grey solid line is the addition of both. The duration of these periods are calculated according to formulae in Katsanevakis and Verriopoulos (2006) and using two different temperature cycles: Temperature in the Fuengirola beach (A) and temperature at 25 m depth close to Fuengirola (B).

M. Vargas-Yᘠnez et al. / Fisheries Research 99 (2009) 159–167

Fig. 5. (A) Solid line is the evolution of total landings in tons in the three ports studied. A linear fit is included and the value of the slope and its 95% confidence interval using a t-test is shown in the insert. Triangles are the residuals, anomalies or deviations from the linear fit. (B)–(D) are the same for winter and spring temperature in Fuengirola beach and SST averaged for the Alboran Sea, which are the predictors used to model octopus landings variability.

and anomaly time series for Fuengirola beach in winter and spring, and the Alboran Sea SST in autumn. In all the cases these time series increase with time, although only in the case of spring temperatures the estimated trends were significant at the 0.05 significance level (see inserts in Fig. 5). 3.3. Linear multivariate model Annual landings were not correlated with rainfall rates nor with Ekman transport (see Section 4). Negative and significant correlations were obtained between landings and SST and TF with correlation coefficients ranging between −0.5 and −0.6 for the different seasons of the year considered. The negative correlation between sea temperature and landings on the following year is partially in agreement with Balguerias et al. (2002) and Sobrino et al. (2002) and the inclusion of both SST (averaged for the Alboran Sea) and the local temperature in Fuengirola beach is justified because they can be representative of different oceanographic processes or simply basin versus local conditions. Therefore, time series of SST in the Alboran Sea for winter, spring, summer and autumn (SSTwint. , SSTspr. , SSTsum. and SSTaut. ) and sea temperature in Fuengirola beach (TF,wint. , TF,spr. , TF,sum. and TF,aut. ) were considered in an exploratory phase. A

163

forward stepwise linear regression selected the linear model ε(t) = −133.9TF,wint. (t − 1) − 142.5SSTaut. (t − 1). The use of this kind of multivariate linear analysis can yield different results when applied to different data sets, and some other criterion such as AIC should be used in order to select the best model. The lack of previous information in this particular area of the Mediterranean Sea does not allow us to consider the temperature in a particular season of the year to be more influential on the octopus abundance than any other one. Neither can be established, a priori, whether coastal temperatures or basin averaged ones will provide more information about the processes controlling octopus abundance fluctuations. We repeated the stepwise analysis 21 times, each time leaving out the data from a different year. Each time, the forward stepwise analysis selected a different model. Column 2 in Table 1 shows how many times each model was selected. Those models that were chosen at least once, plus the simplest models consisting of one single predictor variable were considered as candidate models. The best model between these candidates was selected using an AICc criterion (Burnham and Anderson, 2002). Columns 3 and 4 show the AICc values and the AICc differences between each model and the minimum AICc . Models have been ranked according to the AICc values and Akaike weights have been calculated (column 5). According to this criterion, the best model was a linear combination of Fuengirola beach temperature in winter and spring, and SST in autumn the preceding year. The reliability of this model was tested by means of two crossvalidation tests. As already explained in Section 2, in the first case we proceeded at 21 steps leaving out one year data at each step and fitting the TF,wint. /TF,spr. /SSTaut. model. The PVE was 63%, which supports the model selection (Fig. 6A). A second cross-validation test was conducted using the selected model to predict the landings anomalies on the following year (see Section 2). The first year predicted was year 11 (1997) and in this case the PVE was 29% (Fig. 6B), once again supporting the selection of our best model. Considering both the linear or long term trend observed in octopus landings and the relationships found between inter-annual oscillations and water temperature for the model selected, we can construct the general model: Lˆ (t) = 484.2 − 8.58(t − 1987) − 135.1TF,wint. (t − 1) − 71.5TF,spr. (t − 1) − 120.5SSTaut. (t − 1)

(4)

Fig. 7 shows the observed total landings and those estimated using expression (4). One of the objectives of the present work is to develop a predictive model which could be helpful for management purposes. According to the calculated Akaike differences and weights (Table 1), both the first and second models in Table 1 have some support. We followed a multi-model inference approach. Landings for the 2008 year (when fishery statistics are not yet available) were estimated using the models ranked in first and second place in Table 1. These estimations were averaged using Akaike weights (open circle in Fig. 7). The uncertainty for the estimation

Table 1 Predictors used in the different models tested. Column 2 presents the times each model was selected in a 21 step one-leave-out regression. AICc values for each model are presented in column 3, column 4 is AICc –AICc,min and column 5 is Akaike coefficients calculated according to Burnham and Anderson (2002). Model

Times selected

AICc

i

Wi

TF,wint. /TF,spr. /SSTaut. TF,wint. /SSTaut. SSTwint. /SSTaut. SSTaut. TF,wint. TF,spr.

1 18 1

187.0 188.5 192.9 197.4 200.2 202.0

0 1.5 5.9 10.4 13.2 15

0.65 0.31 0.03 0.004 0.001 0.000

164

M. Vargas-Yᘠnez et al. / Fisheries Research 99 (2009) 159–167

Fig. 6. (A) shows the results of the first cross-validation test. Triangles black line are observed landing anomalies and grey-triangle line are those obtained from a oneleave-out procedure using the TF,wint. /TF,spr. /SSTaut. model selected on the basis of an AICc criterion. (B) Is the same but landing anomalies are predicted on year t + 1 from the regression of landing anomalies on TF,wint. TF,spr. SSTaut. using years 1 to t (see text for details).

Fig. 7. Octopus landings (black line) and those obtained using the complete model in expression (4) which takes into account both the long term trend of landings and the multivariate linear model. Landings in 2008 and the corresponding uncertainty have been predicted using a multi-model inference using the two models supported by AICc criterion and the corresponding AIC coefficients in Table 1.

has been included taking into account both the uncertainty corresponding to each model and the uncertainty between models (see Burnham and Anderson, 2002). 4. Discussion and conclusions Sobrino et al. (2002) found that catches in the Gulf of Cadiz reached a maximum in winter and then decreased until a minimum value in September. A similar behavior has been described in other areas of the Mediterranean Sea, although the minimum can be displaced to August–September (Sánchez and Martin,

1993; Quetglas et al., 1998) or even to spring in the Northeastern Atlantic (Balguerias et al., 2002). Similarly, our results show that octopus catches reach a minimum in late summer (August–September) and then start increasing until a maximum in late autumn (November–January, Fig. 3). O. vulgaris has a protracted spawning period. Mangold (1983) reported a 9 month spawning season from March to October while Sánchez and Obarti (1993) found that the spawning season in the Mediterranean Sea extended from January to July. Otero et al. (2007) also found one single spawning peak in spring in the Galician waters while Silva et al. (2002) reported two spawning periods in the nearby Gulf of Cadiz, one in April–May and a second one in August. The same behavior was found by Katsanevakis and Verriopoulos (2005) in the Eastern Mediterranean. The increase of landings in autumn–winter in the Alboran Sea would indicate the incorporation of juveniles to fisheries during these months. The length of the embryonic development (Caverivière et al., 1999) and that of the octopus planktonic stage is highly dependent on temperature. Depending on the day of the year corresponding to spawning, eggs and paralarvae would face different temperature conditions. Katsanevakis and Verriopoulos (2006) provided expressions for calculating the length of the embryonic development and planktonic stage for any given spawning day and using daily temperature values at the sea surface and 25 m depth. These depths were considered because spawning of common octopus mainly occurs in shallow coastal waters. Fig. 4 shows the seasonal cycle of water temperature at the sea surface and at 25 m depth in Fuengirola continental shelf. Triangles show temperature measurements which have been interpolated into daily values (solid lines) for applying expressions in Katsanevakis and Verriopoulos (2006). Fig. 4A and B show that the upper 25 m of the water column is well mixed throughout the year and no significant differences can be appreciated. The black thick line is the length of embryonic development and the dashed black line is that of the paralarvae phase. The grey line is the addition of both, representing the length of the period between spawning and settlement. The three curves are expressed as functions of the spawning day. That is, considering a hypothetical spawning on day 1 (1st January), and taking into account the daily temperatures at the sea surface from this day on, the length of embryonic plus paralarvae phases would be higher than 160 days (Fig. 4A, grey line). If we consider a possible spawning peak from 1st April to 31st May (Silva et al., 2002, days 91–151) the length of embryonic plus paralarvae stages ranges between 110 and 130 days for the temperature at sea surface and 25 m depth, respectively (grey lines in Fig. 4A and B). This means that settlement would occur between days 220 and 260, that is 8th August and 17th September. The recruitment of these juveniles to the fishery would be several weeks after settlement and therefore would be responsible for the increase of landings from October. In the case that spawning extends during July (Sánchez and Obarti, 1993), settlement would extend to mid October being in a better agreement with the maximum ladings in November. A secondary peak in landings is observed in June (Fig. 3), nevertheless this seems to be a consequence of the temporary ban on trawl fishery in Andalusian waters in May. Octopus landings in the three ports analyzed within the northern Alboran Sea showed a strong inter-annual variability for the period 1987–2007 with values ranging between 205 and 717 t (Fig. 5A). This is a frequent characteristic for this species as well as other cephalopod ones and these large fluctuations seem to be related to environmental inter-annual variability. It is widely accepted that temperature is one of the main factors affecting cephalopod abundances and therefore it has been considered in the present work. Balguerias et al. (2002) found a negative correlation between annually averaged temperature anomalies in the Saharan bank and annual octopus catches and Sobrino et al. (2002) reported

M. Vargas-Yᘠnez et al. / Fisheries Research 99 (2009) 159–167

that low temperature anomalies in spring induced high abundances on the following fishing season starting in autumn–winter. Our results also show an increase of landings for negative temperature anomalies during the preceding spring, in agreement with Sobrino et al.’s work and also a beneficial influence of low temperatures in winter on the following year catches. These relationships can be summarized stating that a −1 ◦ C low anomaly in winter and spring would produce increases of 135 and 71.5 t, respectively, on the following year’s landings. It is difficult to interpret these results as temperature can affect embryonic and paralarvae growth or can simply be a proxy for more complex process such as upwelling intensity, and consequently food availability, retention/dispersion processes, or advection of water masses from distant places. Sobrino et al. (2002) already suggested that cold waters in the Gulf of Cadiz could simply indicate higher upwelling intensities and an enhanced primary production that could be transferred to higher trophic levels. If low temperatures were simply an index for wind-induced upwelling intensity, Ekman transport should show some sort of significant correlation with octopus abundances. Contrary to this, Ekman transport (Qy ) was not correlated with octopus landings. Although we are aware of the speculative character of our arguments we propose two hypotheses for explaining the temperature–abundance correlation and the lack of it for Qy . The first possibility is that in the case of an April–May spawning peak and considering surface temperatures and results in Fig. 4, hatching would occur from mid June to the end of July. If the spawning extends to 1st July, then hatchlings would appear until mid August. In the case that we consider temperature at 25 m depth, these dates are slightly modified and paralarvae would appear from the beginning of June to mid August. Prevailing or mean winds in the Alboran Sea are from the west (Parrilla and Kinder, 1987) favoring wind-induced upwelling and offshore transport and dispersion of ˜ and Sabatés, 2007). icthyo and zooplanktonic species (Vargas-Yánez Nevertheless the prevalence of westerly winds is interrupted during summer months when easterly winds increase their frequency ˜ (Vargas Yánez et al., 2008). The latter winds accumulate planktonic organisms in coastal areas and we speculate that the survival of paralarvae appeared during summer months could be favored by this retention process. A fraction of these individuals would increase landings during next winter months increasing landings corresponding to the following year. Anomalously warm waters in winter and spring could accelerate embryonic and paralarval growth or even spawning, placing hatching in spring months when ˜ intense westerly winds are frequent (Vargas Yánez et al., 2008) and paralarvae dispersion could be a detrimental factor for their survival. The second hypothesis is that cold waters in the Alboran Sea could be an index for upward vertical velocities and enhanced primary production, but not necessarily linked to offshore Ekman transport. Sarhan et al. (2000) described southward displacements of the Atlantic current. The room left by the Atlantic current in the northern sector of the Alboran Sea would be replaced by subsurface nutrient rich waters. It is not clear which is the mechanism responsible for the Atlantic current instabilities but they seem to be independent from wind direction or intensity. We have also found a negative correlation between autumn temperatures and abundances during the following year. In this case, it is not the coastal temperature which is considered as a predictor by the model, but SST averaged for the Alboran Sea. This fact could indicate that low temperatures favor octopus abundances through some sort of mechanism linked to the Alboran Sea general circulation, but for the moment we have no information to conclude and further research is needed. Finally, rainfall rates were considered in the preliminary correlation analysis following Sobrino et al. (2002). We found no correlation between rainfall and octopus abundances, while they affected the catches negatively in the Gulf of Cadiz. These authors

165

hypothesized that high rainfall rates would produce large river discharges increasing water turbidity and pollutants from agriculture. It is important to notice that the Gulf of Cadiz receives the water of the two main rivers in Andalusia: Guadalquivir and Guadiana, while there are no main rivers draining into the Alb˜ oran Sea. Vargas-Yánez et al. (2005) analyzed temperature and salinity time series from 1992 to 2001 in the northern Alboran Sea and never found any decrease of salinity linked to river discharges nor other kind of influence of continental origin which could suggest any correlation between octopus abundances and rainfall rates in the Alboran Sea through the effect of river runoff. Long term changes in temperature can affect the functioning of marine ecosystems, the abundance and distribution of fish populations and their interactions. Some examples are found in the Baltic Sea where increasing temperatures favor the strength of sprat recruitment (MacKenzie and Koster, 2004). Stenevik and Sundby (2007) found that there was a positive correlation between temperature and cod recruitment in the Barent Sea (the lower part of its temperature range) and a negative relationship for the North Sea. In the Mediterranean Sea, S. aurita has extended northward its geographical distribution because of increasing temperatures (Sabatés et al., 2006) and many other alterations could be undergoing in the Mediterranean Sea because of global warming (see CIESM, 2008 and references therein). From 1987 to 2007 octopus landings decreased being the mean annual decrement or linear trend −8.6 t/year (significant at the 0.1 significance level). Fuengirola temperature in spring and winter increased at a rate of 0.06 ◦ C/year and 0.01 ◦ C/year, only the spring trends being significant at the 0.05 significance level. Autumn temperatures also showed warming trends although as in the case of winter ones, not statistically significant. The lack of significance in surface water temperatures simply indicates that the null hypothesis of zero linear trend cannot be rejected with the data at hand. This is usually the case in noisy short length time series. The real pattern or long term behavior of surface temperature appears when longer time series are obtained or when wider geographical areas are considered in order to average and filter out mesoscale high frequency variability. Several works report very strong and significant warming trends in the Western Mediterranean upper layer. Salat and Pascual (2006) obtained a significant and intense warming trend of 0.03–0.04 ◦ C/year in the Catalan coast from 1974 to 2006, these figures being very similar to those reported in the present work. Rixen et al. (2005) obtained a very steep temperature increase for the Western Mediterranean upper layer from the ˜ et al. (2008) present a review beginning of the 1980s. Vargas Yánez of works dealing with warming trends in the Spanish Mediterranean continental shelf and concluded that the surface layer was warming from the 1940s with an acceleration during the 1990s decade. Therefore we consider that the lack of significance in winter Fuengirola temperature and autumn SST simply reflects the large variance of the upper layers and the short length of time series. The multivariate linear model has shown a detrimental effect of warm anomalies on octopus abundances which can be expressed by means of the linear coefficients in expression (4). These relationships together with the long term warming trends estimated in temperature time series would yield a long term decrease in octopus landings of −9.26 t/year, which is in agreement (within the trend uncertainty) with those estimated for the 1987–2007 octopus landings. In summary, a first attempt has been made to detect which environmental variables could affect O. vulgaris variability in the northern Alboran Sea. This work can be considered as an exploratory one, but has already demonstrated some interesting features such as the lack of correlation between octopus landings and rainfall rates, which could be explained by the absence

166

M. Vargas-Yᘠnez et al. / Fisheries Research 99 (2009) 159–167

of important rivers draining into the Alboran Sea. There is no correlation with Ekman transport and we hypothesize that primary production and its delayed transference to higher trophic levels in the Alboran Sea could be modulated by other process different from wind-induced upwelling. Temperature seems to be the main factor controlling octopus abundance variability, both at the inter-annual and long term time scales. Low temperatures produce higher abundances during the following year while warm anomalies would have the opposite effect. It is not clear yet which are the mechanisms responsible for this negative temperature–abundance relationship and further research is needed. Special attention should be paid in the future to the effect of long term warming associated with climate change, as this could be responsible, at least partially, for the long term decrease in octopus landings. Acknowledgements ˜ We are grateful to Instituto Espanol de Oceanografía for its support under the research program RADMED (Series Temporales de Datos Oceanográficos). This work has been partially funded by project DESMMON (Spanish Science and Innovation Ministry, CTM2008-05695-C02-01/MAR). We also thank financial assistance of the European Union under DG Mare Data Collection Regulation. We also thank to J.M. Ortiz de Urbina, the editor and two anonymous reviewers for their comments and suggestions. References Balguerias, E., Hernández-González, C., Perales-Raya, C., 2002. On the identity of Octopus vulgaris Cuvier 1797 stocks in the Saharian bank (Northwest Africa) and their spatio-temporal variations in abundance in relation to some environmental factors. Bull. Mar. Sci. 71 (1), 147–163. ˜ Bazzino, G., Quinones, R.A., Norbis, W., 2005. Environmental associations of shortfin squid Illex argentinus (Cephalopoda: Ommastrephidae) in the Northern Patagonian Shelf. Fisher. Res. 76, 401–416. Belcari, P., Cuccu, D., González, M., Srairi, A., Vidoris, P., 2002. Distribution and abundance of Octopus vulgaris Cuvier 1797 (Cephalopoda: Octopoda) in the Mediterranean Sea. Sci. Mar. 66 (Suupl. 2), 157–166. Bellido, J.M., Brown, A., Valavanis, V.D., Giráldez, A., Pierce, G.J., Iglesias, M., Palialexis, A., 2008. Identifying essential fish habitats for small pelagic species in Spanish Mediterranean waters. Hydrobiologia 612, 171–184, doi:10.1007/s 10750-0089481-2. Boyle, P., Rodhouse, P., 2005. Cephalopods: Ecology and Fisheries. Blackwell Publishing, Oxford, 464 pp. Burnham, K.P., Anderson, D.R., 2002. Model selection and multimodel inference: a practical information-theoretic approach, 2nd edition. Springer-Verlag, New York, NY, USA, 488 pp. Caddy, J.F., 1983. The cephalopods: factors relevant to their population dynamics and to the assessment and management of stocks. In: Caddy, F.J. (Ed.), Advances in assessment of world cephalopod resources. FAO Fisheries technical papers, pp. 416–449. Caverivière, A., Domain, F., Diallo, A., 1999. Observations on the influence of temperature on the length of embryonic development in Octopus vulgaris (Senegal). Aquat. Living Resour. 12 (2), 151–154. CIESM, 2008. Climate warming and related changes in Mediterranean marine biota. No. 35. In: Briand, F. (Ed.), CIESM Worshop Monographs, Monaco, 152 pp. Faure, V., Inejih, C.A., Demarcq, H., Cury, P., 2000. The importance of retention processes in upwelling areas for recruitment of Octopus vulgaris: the example of the Arguin Bank (Mauritania). Fisher. Oceanogr. 9 (4), 343–355. Fernández, A.M., Esteban, A., 2003. La pesquería artesanal de Santa Pola (S.E. de la Península Ibérica). Descripción y actividad en el periodo 1992–2000. Inf. Téc. Inst. Esp. Oceanogr. 181 (2003), 49. Fogarty, M.J., 1989. Forecasting yield and abundance in exploited invertebrates. In: Caddy, J.F. (Ed.), Marine Invertebrate Fisheries: their Assessment and Management. John Wiley and Sons, New York, pp. 701–724. Francis, R.I.C., 2006. Measuring the strength of environmental–recruitment relationships: the importance of including predictor screening with cross-validation. ICES J. Mar. Sci. 63, 594–599, doi:10.1016/j.icesjms.2006.01.001. González, A.F., Otero, J., Guerra, A., Prego, R., Rocha, F.J., Dale, A.W., 2005. Distribution of common octopus and common squid paralarvae in a wind-driven upwelling area (Ria de Vigo, northwestern Spain). J. Plankton Res. 27 (3), 271–277. Katsanevakis, S., Verriopoulos, G., 2006. Modelling the effect of temperature on hatching and settlement patterns of meroplanktonic organisms: the case of the octopus. Sci. Mar. 70 (4), 699–708. Katsanevakis, S., Verriopoulos, G., 2005. Seasonal population dynamics of Octopus vulgaris in eastern Mediterranean. ICES J. Mar. Sci. 63, 151–160.

Lavín, A., Montero-Ventas, X., Ortiz de Zárate, V., Abaunza, P., Cabanas, J.M., 2007. Environmental variability in the North Atlantic and Iberian waters and its influence on horse mackerel (Trachurus trachurus) and albacore (Thunnus alalunga) dynamics. ICES J. Mar. Sci. 64 (3), 425–438, doi:10.1093/icesjms/fsl042. MacKenzie, B.R., Koster, F.W., 2004. Fish production and climate: sprat in the Baltic Sea. Ecology 85 (3), 784–794. Mangold, K., 1983. Octopus vulgaris. In: Boyle, P.R. (Ed.), Cephalopod Life Cycles Volume I Species Accounts. Academic Press, New York, pp. 335–364. Morán, X.A., Estrada, y.M., 2001. Short-term variability of photosinthetic parameters and particulate and disolved primary production in the Alborán Sea (SW Mediterranean). Mar. Ecol. Prog. Ser. 212, 53–67. Otero, J., González, A.F., Sieiro, M.P., Guerra, A., 2007. Reproductive cycle and energy allocation of Octopus vulgaris in Galician waters, NE Atlantic. Fisher. Res. 85, 122–129. Otero, J., Álvarez-Salgado, X.A., González, A.F., Miranda, A., Groom, S.B., Cabanas, J.M., Casas, G., Wheatley, B., Guerra, A., 2008. Bottom-up control of common octopus Octopus vulgaris in the Galician upwelling system, northeast Atlantic Ocean. Mar. Ecol. Prog. Ser. 362, 181–192, doi:10.3354/meps07437. Parrilla, G., Kinder, y T.H., 1987. Ocenografía física del Mar de Alborán. Bol. Inst. Esp. Oceanog. 4 (1), 133–165. Pierce, G.J., 1995. Stock assessment with a thermometer: correlations between sea surface temperature and landings of squid (Loligo forbesi) in Scotland. ICES CM 95/K 21, 8. Pierce, G.J., Bailey, N., Stratoudakis, Y., Newton, A., 1998. Distribution and abundance of the fished population of Loligo forbesi in Scottish waters: analysis of research cruise data. ICES J. Mar. Sci. 55, 14–33. Pierce, G.J., Valavanis, V.D., Guerra, A., Jereb, P., Orsi-Relini, L., Bellido, J.M., Katara, I., Piatkowski, U., Pereira, J., Balguerias, E., Sobrino, I., Lefkaditou, E., Wang, J., Santurtun, M., Boyle, P.R., Hastie, L.C., MacLeod, C.D., Smith, J.M., Viana, M., González, A.F., Zuur, A.F., 2008. A review of cephalopod–environment interactions in European Seas. Hydrobiologia 612, 49–70. Quetglas, A., Alemany, F., Carbonell, A., Merella, P., Sánchez, P., 1998. Biology and fishery of Octopus vulgaris Cuvier 1797 caught by trawlers in Mallorca (Balearic Sea Western Mediterranean). Fisher. Res. 36, 237–249. Rixen, M., Bakers, J.-M., Levitus, S., Antonov, J., Boyer, T., Maillard, C., Fichaut, M., Balopoulos, E., Iona, S., Dooley, H., García, M.J., Manca, B., Giorgetti, A., Mazella, G., Mikhailov, N., Pinardi, N., Zavatarelli, M., 2005. The Western Mediterranean deep water: a proxy for climate change. Geophys. Res. Lett. 32, L12608, doi:10.1029/2005GL022702. Roberts, M.J., van den Berg, M., 2002. Recruitment variability of chokka squid (Loligo vulgaris Reynaudi): role of currents on the Agulhas bank (South Africa) in paralarvae distribution and food abundance. Bull. Mar. Sci. 71 (2), 691–710. Rosenzweig, C., Casassa, G., Karoly, D.J., Imeson, A., Liu, C., Menzel, A., Rawlins, S., Root, T.L., Seguin, B., Tryjanowski, P., 2007. Assessment of observed changes and responses in natural and managed systems. In: Parry, M.L., Canziani, O.F., Palutikof, J.P., van der Linden, P.J., Hanson, C.E. (Eds.), Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK, pp. 79–131. Rubín, J.P., 1997. Las larvas de peces mesopelágicos del mar de Alborán Resultados ˜ Ictio. Alborán 0793 y revisión histórica. Publ. Espec. Inst. Esp. re la campana Oceanogr. 24, 43–52. Sabatés, A., Martín, P., Lloret, J., Raya, V., 2006. Sea warming and fish distribution: the case of the small pelagic fish, Sardinella aurita, in the western Mediterranean. Global Change Biol. 12, 2209–2219. Salat, J., Pascual, y.J., 2006. Principales tendencias climatológicas en el Mediterráneo ˜ de observaciones oceanográficas en Noroccidental, a partir de más de 30 anos la costa catalana. In: Cuadrat Prats, J.M., Sánchez, M.A., Vicente Serrano, S.M., Lanjeri, S., de Luis Arrillaga y, N., González-Hidalgo, J.C. (Eds.), Clima, sociedad y ˜ Medio Ambiente. Publicaciones de la Asociación Espanola de Climatología (AEC), pp. 284–290 (serie A, num 5). Sánchez, P., Martin, P., 1993. Population dynamics of exploited cephalopod species of the Catalan Sea (NW Mediterranean). Sci. Mar. 57 (2–3), 153–159. Sánchez, P., Obarti, R., 1993. The biology and fishery of Octopus vulgaris caught with clay pots in Spanish Mediterranean coast. In: Okutani, T., O’Dor, R.K., Kubodera, T. (Eds.), The Recent Advances in Cephalopod Fishery Biology. Tokai University Press, pp. 477–487. Sarhan, T., García-Lafuente, J., Vargas, M., Vargas, J.M., Plaza, F., 2000. Upwelling mechanisms in the northwestern Alboran Sea. J. Mar. Syst. 23, 317–331. Silva, L., Sobrino, I., Ramos, F., 2002. Reproductive biology of the common octopus, Octopus vulgaris Cuvier 1797 (Cephalopoda: Octopodidae) in the Gulf of Cadiz (SW Spain). Bull. Mar. Sci. 71, 837–850. Sobrino, I., Silva, L., Bellido, J.M., Ramos, F., 2002. Rainfall, river discharges and sea temperature as factors affecting abundance of two coastal benthic cephalopod species in the Gulf of Cadiz (SW Spain). Bull. Mar. Sci. 71 (2), 851–865. Stenevik, E.K., Sundby, S., 2007. Impacts of climate change on commercial fish stocks in Norwegian waters. Mar. Policy 31, 19–31. Suda, M., Akamine, T., Kishida, T., 2005. Influence of environmental factors, interspecific-relationships and fishing mortality on the stock fluctuation of the Japanese sardine Sardinops menostictus, off the Pacific coast of Japan. Fisher. Res. 76, 368–378. ˜ Vargas Yánez, M., García Martínez, M.C., Moya, F., Tel, E., Parrilla, G., Plaza, F., Lavín, A., García, M.J., Salat, J., Pascual, J., García Lafuente, J., Gomis, D., Álvarez, E., García Sotillo, M., González-Pola, C., Polvorino, F., Fraile, E., 2008. Cambio Climático en

M. Vargas-Yᘠnez et al. / Fisheries Research 99 (2009) 159–167 ˜ Editado por Instituto Espanol ˜ de Oceanografía, Madrid, el Mediterráneo espanol. ISBN: 84 95877 39 2, 171 pp. ˜ Vargas-Yánez, M., Sabatés, A., 2007. Mesoscale high frequency variability in the Alboran Sea and its influence on fish larvae distributions. J. Mar. Syst. 68, 421–428. ˜ Vargas-Yánez, M., Chasles, A., Berthelemot, A., Ramírez, T., Cortés, D., García, A., Carpena, A., Serna-Quintero, J.M., Sebastián, M., Mercado, J., Cortés, J., Álvarez, ˜ J.P., Caminas, J. A., 2005. Proyecto Ecomálaga 1992–2001. Parte I: Oceanografía Física. Inf. Técn. Inst. Esp. Oceanogr. n◦ 183, ISSN: 0212-1565, 73 pp.

167

Wang, J., Pierce, G.J., Boyle, P.R., Denis, V., Robin, J.P., Bellido, J.M., 2003. Spatial and temporal patterns of cuttlefish (Sepia oficinalis) abundance and environmental influences—a case study using trawl fishery data in French Atlantic coastal, English Channel, and adjacent waters. ICES J. Mar. Sci. 60, 1149–1158. Zar, J.H., 1984. Biostatistical Analysis, 2nd edition. Prentice-Hall Inc., London, ISBN 0-13-077925-3, 718 pp.