1595

What drove tuna catches between 1525 and 1756 in southern Europe?
U. Ganzedo, E. Zorita, A. P. Solari, G. Chust, A. Santana del Pino, J. Polanco, and J. J. Castro
Ganzedo, U., Zorita, E., Solari, A. P., Chust, G., Santana del Pino, A., Polanco, J., and Castro, J. J. 2009. What drove tuna catches between 1525 and 1756 in southern Europe? ICES Journal of Marine Science, 66: 1595 1604.

From 1525 to 1756, catches of tuna in almadrabas (trapnets) uctuated greatly, but the overall trend was a downwards one. The aim of this study is to assess the potential inuence of climatic factors on tuna shing. We performed time-series analysis of the climate over the years 1525 1756 and determined whether such events can be related to historical data on bluen tuna catches in the almadrabas of Medina Sidonia. We used a generalized linear model to relate the tuna catches to climatic parameters. We carried out variance partitioning analysis of tuna catches to assess the relative contribution of climate from temporal autocorrelation. The temporal autocorrelation in tuna catches was used as a surrogate for the contribution of the population dynamics to variation in the catch series. The results indicated that climate accounted for up to 12.3% of the total variance, the temporal effects (autocorrelation) accounted for up to 38.8% of the total variance, and up to 35.7% of the catch was accounted for by the joint effect of the two components. The signicant variance accounted for by climate suggests that low temperatures during the Maunder minimum (the so-called The Little Ice Age, years 1640 1715) may have reduced both recruitment and abundance of tuna in the North Atlantic and the Mediterranean. Our ndings suggest that both environmental and population dynamic components played an important role in regulating the almadraba catches in Medina Sidonia.
Keywords: almadraba, bluen tuna, climatic factors, Maunder minimum, solar cycle. Received 15 August 2008; accepted 2 February 2009; advance access publication 28 March 2009. U. Ganzedo and J. Polanco: Department of Applied Physics II, Apdo. 644 University of Basque Country, 48080 Bilbao, Spain. E. Zorita: Institute for Coastal Research, GKSS-Research Centre, Geesthacht, Germany. A. P. Solari, A. Santana del Pino, and J. J. Castro: Dept. Biologa, Univ. Las Palmas de Gran Canaria, Edf. Ciencias Basicas (B-203), Campus de Tara, 35017 Las Palmas de Gran Canaria, Spain. G. Chust: AZTITecnalia, Marine Research Division, Herrera Kaia Portualdea z/g, 20110 Pasaia, Gipuzkoa, Spain. Correspondence to U. Ganzedo: tel: 34 94 601 3376; fax: 34 94 601 3500; e-mail: unai.ganzedo@ehu.es.

Introduction
Almadraba (tuna) trapnets have been used traditionally to catch migrating tunas, particularly bluen (Thunnus thynnus), in southern Spain since Phoenician times, without signicant changes in location or shing method (Rodrguez-Roda, 1983; Agudo, 1991; Regueira and Regueira, 1993; Lopez-Capont, 1997). Tuna catches by almadrabas, especially bluen, have uctuated over recent centuries (Ravier and Fromentin, 2001). For instance, in the middle of the 20th century, between 5000 and 6000 bluen tuna were usually harvested in June off the Atlantic coast of southern Spain (Lozano-Rey, 1952). However according to Martn Sarmiento (in Lopez-Capont, 1997), in 1552, some 73 000 99 000 bluen tuna were caught in the almadrabas of Conil and Zahara, which are considered to be the most important almadrabas along this coast. These catches appear reasonable if we consider that the tuna biomass today is only 10% of pre-industrial levels (Myers and Worm, 2003). In 1757, the monk Martn Sarmiento sent a letter to the Duke of Medina Sidonia explaining why the catches in the dukes almadrabas had been dramatically decreasing for several decades during that century. Although Martn Sarmiento suggested that the decline had probably resulted from overshing, he also
# 2009

pointed out that it could have been related to climatic variations (Lopez-Capont, 1997). Current knowledge has established that environmental variations can cause variations in sh recruitment (Cushing, 1982; Kawasaki et al., 1991; Santiago, 1998; Corten, 2001). The environmental conditions for tuna during their migration in oceanic waters can have a signicant inuence on both their local abundance and behaviour (Stretta, 1991; Wootton, 1992; Hazel, 1993; Jobling, 1995; Korsmeyer and Dewar, 2001). An analysis of long time-series of catches might allow us to discriminate between the effects of shing and the effects of climatic change, specically when variations in catches reect changes in abundance, as was pointed out by Fromentin et al. (2000) and Ravier and Fromentin (2001) for the tuna trap shery. In the letter mentioned earlier, Sarmiento compiled the annual landings that the Duchess of Medina Sidonia had recorded from 1525 to 1756 (Lopez-Capont, 1997). This time-series provides a unique opportunity to investigate possible effects of climatic events on the populations of tuna caught by the almadrabas. The aim of this study was to assess the effect of climatic factors on the decrease in tuna catches. First, to test this relationship, we performed time-series analyses of the climatic events that occurred

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between years 1525 and 1756. Then we determine whether bluen tuna catches of the Medina Sidonia almadrabas might have been related to these events.

U. Ganzedo et al. temperatures revealed consistently positive correlation with the number of sunspots and negative correlation with cosmic rays (Usoskin et al., 1998). Signicance levels as high as 99% were recorded, but they varied between the different datasets. The major part of the correlation was as a result of the similarity of the long-term trends in the datasets. The cosmic ray ux trend correlated better with terrestrial temperature than the sunspot number derived from the same cosmogenic isotope data did (Usoskin et al., 2005). The sunspot and solar irradiance time-series for the period 16101973 were extracted from Lean et al. (1995). Measurements of solar irradiance 15251756, based on the Beryllium-10 isotope index, were sourced from Crowley (2000).

Material and methods

Tuna catch series
The historical tuna catch series was extracted from a facsimile copy of a letter that the monk Martn Sarmiento sent to the Duke of Medina Sidonia in 1757 (Lopez-Capont, 1997). In this letter, annual landings (number of individuals) from the almadrabas that belonged to the Medina Sidonia Dukedom were compiled (Table 1) for the years 15251756. Gaps in the series (12 years missing) were either because records were not made in the notebooks for those years or because the nets were not used, particu larly after 1673 (Lopez-Capont, 1997). The number of tuna caught appears reasonable if we consider that the bluen tuna biomass currently is only 10% of pre-industrial levels (Myers and Worm, 2003). The almadrabas of Medina Sidonia were mainly beach-seines, which were used along the Atlantic coast of southern Spain (Figure 1). The catches consisted mostly of bluen tuna (Ravier and Fromentin, 2001), although other species were also caught in lesser quantities (Auxis rochei, Sarda sarda, and Thunnus alalunga). Atlantic almadrabas were exclusively used to target bluen tuna, and they were more productive than Mediterranean ones (De Buen, 1924). The species of major interest to the duke was also bluen tuna. The almadrabas in the historical period were deployed in accordance with the spawning migration pattern in this species (from the end of April to the middle of June). The catch by the two main almadrabas (Conil and Zahara) represents 95.2% of the total sh caught (41.6% in Conil and 53.6% in Zahara). They operated throughout the period studied. Therefore, the analysis was carried on the total catch series pooled from both almadrabas (data from the other almadrabas were not used).

NAO index
Modern evidence suggesting the NAO as a prominent mode of variability in the climate of the northern hemisphere (Hurrell, 1995; Cullen and De Menocal, 2000; Vauclair and Du-Penhoat, 2001; Pingree, 2002). Santiago (1998) reported that the relationship between the winter NAO index and bluen tuna catches was positive, but that it was negative for albacore catches. He found that the NAO accounted for 38 and 64% of the variability of bluen tuna and albacore recruitment, respectively. Historical records of the NAO index were obtained from Cook et al. (2002), who performed a multi-proxy reconstruction of the winter NAO index covering the period 14001979. This was veried against independent estimates of the winter NAO index from European instrument and non-instrument data, as far back as 1500. In addition, we used the estimates of monthly (1659 2001) and seasonal (15001658) NAO indices calculated by Luterbacher et al. (2002) from early instrument and documentary proxy predictors from Eurasia.

Atmospheric dust and GHG

Comparisons of observations with simulations results from an energy-balance climate model indicated that 41 64% of variation in pre-anthropogenic (pre-1850) decadal-scale temperature was as a result of changes in solar irradiance and volcanism (Crowley, 2000). An index of volcanic dust in the atmosphere for the northern hemisphere, from 1500 to 1969, was obtained from Hipel and McLeod (1994). Increasing atmospheric carbon dioxide concentrations cause global temperatures to rise (Came et al., 2007). Planktonic organisms play a dominant role in the CO2 budget of marine ecosystems, and their activity is inuenced by temperature (Vazquez-Dominguez et al., 2007). Furthermore, if warmer temperature enhances carbon demand (production respiration) of plankton and their efciency remains low (as it generally is), plankton would enhance the transfer of carbon from the ocean to the atmosphere. An increase in SST could cause positive feedback between coastal warming and CO2 production (Vazquez-Dominguez et al., 2007). Differences in water temperature are signicant factors inuencing the microbial loop in rearing tanks of sh larvae. Nakagawa et al. (2007) suggested that a microbial loop, established naturally, contributes to energy and nutrient gain in bluen tuna larvae reared in an articially controlled environment (Nakagawa et al., 2007). We also used data on the atmospheric concentration of GHG in CO2 from 1000 to 1998, obtained from Crowley (2000), in our analyses.

Climatic and climate-dependent dataseries

Dataseries of different climate variables for the years 1525 1756 were compiled from the literature, much of which is published on the Internet, and most have been derived from climate reconstruction models (Bradley, 1992; Van Oldenborgh, 1999) or obtained from the NOAA Paleoclimatology programme (http:// www.ncdc.noaa.gov/paleo). We used different types of data that could have a direct or indirect inuence on recruitment: the North Atlantic oscillation (NAO) index, sea surface temperature (SST), temperature of the air, solar irradiance, and greenhouse gases (GHG).

Air temperature
Annual global air temperatures at sea surface level from 1525 to 1756 were obtained by reconstructions from Mann et al. (1998, 1999). These reconstructions were based on multivariate calibration of widely distributed high-resolution proxy climate indicators that provide insight into both the spatial and temporal nature of climatic variations during the past six centuries.

Sunspots, solar irradiance, and Beryllium-10

Comparison of the sun-related datasets with various reconstructions of terrestrial northern hemisphere mean surface

Climatic events and the tuna shery in Europe

Table 1. Statistical characteristics of the catch series of tuna obtained in each almadraba of the Duke of Medina Sidonia from 1525 to 1756.
Parameter Years Years with data Years, traps not installed Years with gaps Range of sh caught Mean sh caught Fish caught 1525 1600 Conil 1525 1756 180 11 41 6 65 312 11 426 (s.d. 14 604, n 180) 2 35465 312 (mean 27 917, s.d. 18 471, n 53) 0 23 80 16 615 (mean 6 993, s.d. 4 475, n 76) 6 18 6 10 592 (mean 2 186, s.d. 2 330.0, n 51) 5 0 Zahara 1525 1756 158 36 38a 43 73 000 16 420 (s.d. 18 388, n 158) 2 60873 000 (mean 35 268, s.d. 21 581, n 51)) 0 25a 427 21 647 (mean 9 552 s.d. 4 918, n 75) 12 13 43 6 702 (mean 2 479, s.d. 2 052.6, n 32) 24 0 Conilejo or Castil novo 1525 1622; and in 1722 31 No data 201 473 15 922 4 640 (s.d. 3 658, n 31) 473 15 922 (mean 5 102, s.d. 3 985, n 24) No data 52 1 894 6 387 (mean 3 058, s.d. 1 511, n 7) Since 1623 No data Not installed Hercules and Santi Petri Ro del Terron 1552 1606 1741 1756 10 No data 45 253 7 954 2 081 (s.d. 2 499, n 10) 253 7 954 (mean 2 796, s.d. 2 716, n 7) No data 42 16 0 0 706 9 684 3 785 (s.d. 2 218, n 16) Not installed Tarifa 1743 1755 11 2 0 5 209 80.4 (s.d. 76.9, n 13) Not installed Carboneros 1743 1754 12 0 0 111 256 433 (s.d. 422, n 12) Not installed Total 1525 1756 215 5 12 9 125 388 24 222 (s.d. 30 439, n 215) 802 125 388 (mean 519 101, s.d. 38 603.8, n 70) 0 6 8037 467 (mean 14 062, s.d. 10 036, n 91) 3 6 9 15 194 (mean 4 749, s.d. 3 870, n 54) 2 0

Years not installed Gaps from 1525 to 1600 Fish caught 1601 1700

Not installed

Not installed

324 580 Not installed (mean 414, s.d. 144, n 3) Since 1607 No data Not installed 706 9 684 (mean 3 784, s.d. 2 218, n 16) 0 0

Years not installed Gaps from 1601 to 1700 Fish caught 1701 1756

5 209 (mean 80.4, s.d. 76.9, n 11) 0 0

111 252 (mean 433, s.d. 422, n 12) 0 0

Years traps not installed Gaps from 1701 to 1756

s.d., standard deviation; n, number of observations. a Fish caught in Zahara during 1534, 1536, 1540, 1551, and 1552 were reportedly added to that of Conil.

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U. Ganzedo et al. been several epidemic episodes of malaria (1590) and plague (15981602, 16471652, and 16761685; Coronas-Tejada, 1994; Fundacion Medina Sidonia, 2005). In addition, during the 16th, 17th, and 18th centuries, Spain had been involved in several wars, revolts, and pirate attacks, such as wars against France, England, the Ottoman Empire, and the Netherlands between 1521 and 1680, revolts between 1568 and 1570, and the Spanish War of Succession between 1702 and 1714, Algerian pirates in 1559, 1562, and 1646. Such events could have affected the almadraba shery on account of a lack of personnel or destruction of the shing gear. Furthermore, Spain had also suffered an economic downturn from 1599 to 1602, ascribable to the plague and the war against England. Several erroneous commercial strategies and the economic problems of the duke had caused a crisis for the almadraba shery until 1627, again from 1646 to 1648, coinciding with the bankruptcy of the Kingdom of Spain, as a consequence of the central European wars (Fundacion Medina Sidonia, 2005). From 1685 on, the efciency of the almadrabas had been very low, owing to a lack of investment in new nets and other gear during the previous years (this problem was resolved in 1700). Failure to maintain the shing gear had also occurred in 1712 and 1713 (Fundacion Medina Sidonia, 2005).

Figure 1. Geographic location of the almadraba traps owned by the Duke of Medina Sidonia, in southern Spain.

Air temperature and SST obtained from climate models

Air temperature and SST from a simulation of the past millennium with the global atmosphere ocean model ECHO-G were also included in the analyses. This model consists of the spectral atmospheric model ECHAM4 and the ocean model HOPE-G (Legutke and Voss, 1999). SST and air temperature values were averaged monthly within the geographic box 108E 158W; 328N428N. These model series were not able to reproduce the observed annual temperature sequence, but they did reproduce the trend in air temperature and SST over decades, provided that they were related to the external climate forcing. We also used annual near-surface air temperature anomaly averages, within 208W 408E; 508N208N, and anomalies with respect to 15001800 mean (ECHO-G simulation, Storch et al., 2004).

Statistical analysis
To analyse the relationship between the tuna catch series (without interpolation) and climate variables, we rst used the Spearman rank correlation coefcient (rs; Table 2) and cross-correlation (Table 3) to determine the degree of correspondence between the series. The partial correlation coefcient was calculated between each pair of variables after the effects of other variables had been removed. In this case, the control variable was time, which removed the effect of the temporal trends on the total explained variance (Legendre, 1993). Second, we tested the relationship between catches (Y ) and climate descriptors (Xi), with generalized linear models (GLMs), following Hastie and Tibshirani (1990). Non-linear relationships can also be tested with GLMs, by introducing appropriate polynomial terms of the predictors to improve the t of a linear model; however, this can be tedious and imprecise (Guisan et al., 2002). In linear regression, the dependent variable Y is modelled by a set of predictors variables Xi as Y a
p X il

Other natural and social events that could have inuenced the shery
Several socio-economic factors could have had an effect on the efciency of the almadraba shery by reducing shing effort (epidemics, wars and economical crises), which could help to explain some outliers and gaps in the catch series. For instance, there had

B i X i e;

Table 2. Correlation coefcients (Spearman) and the p-value, and the partial correlation value (the control variable is the time) between tuna catches and climate variables.
Climate variables Solar irradiance (from 1610 onwards) Beryllium-10 Air temperature anomaly (Mann et al., 1998) Air temperature anomaly (Mann et al., 1999) Air temperature anomaly (ECHO-G; Storch et al., 2004) Air temperature (Zorita et al., 2005) SST (Zorita et al., 2005) Volcanic dust veil index GHG rs (Spearman) 0.258 20.302 0.292 0.412 0.191 0.186 0.217 20.329 0.382 p-value ,0.01 ,0.01 ,0.01 ,0.01 ,0.01 ,0.01 ,0.01 ,0.01 ,0.01 r 2 (partial correlation) 0.324 20.214 0.260 0.276 0.220 0.159 0.218 20.128 0.484 p-value ,0.01 ,0.01 ,0.01 ,0.01 ,0.01 ,0.01 ,0.01 0.058 ,0.01

Climatic events and the tuna shery in Europe Table 3. Highest cross-correlation coefcient between catch and climate variables.
Climate variables Air temperature anomaly (Mann et al., 1998) Air temperature anomaly (Mann et al., 1999) Air temperature anomaly (Zorita et al., 2005) SST (Zorita et al., 2005) Cross-correlation coefcient 0.290 0.356 0.238 0.268 p-value ,0.01 ,0.01 ,0.01 ,0.01 s.e. 0.067 0.068 0.069 0.069

1599

Lag (years) 6 6 7 7

with an error eN (0,1). The model is tted using a maximumlikelihood estimation technique through deviance reduction, where the explained deviance, 1 (residual deviance)/(null deviance), is equivalent to r 2 in least-squares models (Guisan and Zimmermann, 2000). The construction of the model for our data was carried out with the mgcv package implemented in the R language (Wood, 2006). The catch was considered as the response (output) variable in the analysis, to facilitate the analyses and visual comparison of general trends. We used the following explanatory variables in the GLM model: (i) SST; (ii) Air temperature (data from Zorita et al., 2005, and reconstructed data from Mann et al., 1998). We used air temperature and SST because both parameters display a demonstrated direct relationship with the tuna sheries (Corten, 2001); (iii) GHGs, because they could be related to the marine microbial loop (primary production), which contributes energy and nutrient gain to bluen tuna larvae (Nakagawa et al., 2007). We constructed three models: Model 1 was used to explain tuna catch using GHG SST air temperature (air T8) from Mann et al. (1998). Model 2 was used to explain tuna catch using SST air temperature (air T8) from Mann et al. (1998). Model 3 was used to explain tuna catch using SST air temperature (air T8) from Zorita et al. (2005). Conversely, temporal structures in the time-series itself could incorporate other historical, biotic, or environmental effects not taken into consideration by external factors (Legendre and Legendre, 1998). Therefore, we used third-degree polynomial terms for time (T ), T, T 2, and T 3 (Legendre, 1993), to consider temporal effects as a surrogate for the inuence of tuna population dynamics. We proceeded in two steps. First, for each type of explanatory variable, we selected the signicant variables by a stepwise procedure. We then carried out a partitioning analysis of variance by partial regression analysis (Legendre and Legendre, 1998) to determine the relative contribution of climate variables compared with the internal population-dynamic factors described by the time polynomials. Thus, the total variation was decomposed into four different components: (i) pure effect of climate variables, (ii) pure effect of temporal variables, (iii) combined variation resulting from the joint effect of climate and temporal variables, and (iv) unexplained variation. We did not consider the sunspot data because of the large number of gaps in that series. Other variables (atmospheric dust and socio-economic events) were not considered either, because their effects, although potentially important, are presumed shortlived. For example, the most severe short-term northern hemisphere cooling event over the past 600 years occurred in 1601 (Mann et al., 1998), suggesting that either the effect on climate

of the eruption in 1600 of the Huaynaputina volcano in Peru had been greatly underestimated previously, or another eruption, as yet unidentied, had occurred at the same time (Briffa et al., 1998).

Results
Tuna catch series
The largest catch (125 388 tuna) was in 1559, after which the almadraba catches followed a uctuating downward trend, from 72 819 sh (15251570) to 1410 sh (1686 1724; Figure 2).

Climate data analysis

Although the Maunder minimum coincided with the least productive period of the almadraba trap shery, specically from 1672 to 1724, we found no relationship between the number of sunspots and tuna catches. The relationships between the number of sunspots and solar irradiance series with the temperature anomaly (Mann et al., 1998) were signicant (rs 0.24, p 0.003, and rs 0.27, p 0.001, respectively). In addition, there were signicant relationships between the number of sunspots and solar irradiance (Mann et al., 2005; rs 0.78, p , 0.001), and between catches and the Beryllium-10 dataseries (rs 20.30, p , 0.001; partial correlation r 20.21, p 0.001). Catches were also signicantly correlated with solar irradiance from 1610 on, the volcanic dust veil index, GHG, annual air temperature, air temperature anomaly, and SST (Table 2). The highest cross-correlation coefcient between SST and catches was found when the catch series was interpolated, with a lag of 6 years (Table 3). No signicant relationship was found with the NAO, but the relationship between GHG and air temperature (rs 0.35; p , 0.001) was positive and signicant.

Generalized linear models

The stepwise procedure in the GLM model of climate variables selected the term GHG as a unique signicant variable. For the GLM model using the temporal terms, the stepwise procedure selected all the variables introduced (i.e. T, T 2, and T 3; Tables 4 6). In model 1, the variance partitioning analysis indicated that climate accounted for 12.3% of the total variance in tuna catches; the temporal effects accounted for 12.3% of the total variance, and 35.7% of catches were accounted for by the joint effect of the two components (Table 4, Figure 3). In model, 2, the analysis indicated that air temperature (Mann et al., 1998) and SST (Zorita et al., 2005) accounted for 2.1% of the total variance in tuna catches, the temporal effects accounted for 38.8% of the total variance, and 9.2% of catches was accounted for by the joint effect of the two components (Table 5). In model 3, the variation partitioning analysis indicated that SST (Zorita et al., 2005) accounted for 1.4% of the total variance in tuna catches, the temporal effects accounted for 43.1% of the total variance, and 4.8% of

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U. Ganzedo et al.

Figure 2. Annual catches (number of individuals) between years 1525 and 1756 in the almadrabas of the Duke of Medina Sidonia and SST (left panel). Annual catches and GHG (right panel). The grey box indicates the Sporer and the Maunder minima. A linear lter has been applied to all series.

Table 4. Variation partitioning of the catch series, using GLM model (1).
Variable Climate Terms GHG (Hipel and McLeod, 1994) SST (Zorita et al., 2005) Air temperature (Mann et al., 1998) T T2 T3 Selected terms GHG Explained p-value deviance (%) ,0.0001 12.27

Table 6. Variation partitioning of the catch series, using GLM model (3).
Selected terms SST Explained deviance (%) 1.42

Variable Climate

Temporal T T2 T3 0.0389 0.0331 0.0284 12.28 Shared Unexplained 35.67 39.76

Temporal

Terms SST Air temperature (Zorita et al., 2005) T T2 T3

p-value ,0.0001

T T2 T3

0.0389 0.0331 0.0284

43.14

4.82 50.62

Shared Unexplained
T is the time in years.

T is the time in years.

catches was accounted for by the joint effect of the two components (Table 6).

Discussion
Table 5. Variation partitioning of the catch series, using GLM model (2).
Selected terms SST Explained deviance (%) 2.10

Variable Climate

Temporal

Terms SST (Zorita et al., 2005) Air temperature (Mann et al., 1998) T T2 T3

p-value ,0.0001

Air ,0.0001 temperature

T T2 T3

0.0389 0.0331 0.0284

38.84

Shared Unexplained
T is the time in years.

9.15 49.91

The almadraba catch series from 1525 to 1756 varied greatly, with a clear decreasing trend. Our results reveal climatic components that had a negative effect on the number of tuna caught. The extremely cold weather for almost a century could have resulted in a signicant drop in recruitment, with a consequent reduction in tuna populations in the North Atlantic Ocean and the Mediterranean. However, some of the variability in almadraba catches could have been ascribed to social, political, and economic events. Beyond the historical and social aspects, there is a scientic importance in the tuna catch series recorded by the monk Martn Sarmiento. Such series could become a key to estimating the effect of climate on the abundance of sh species during a period when shing pressure was low. Some of the changes in the climate during the period studied have been documented in the literature, especially regarding the cooling that affected Western Europe between 1640 and 1715, called the Little Ice Age. There was a clear relationship

Climatic events and the tuna shery in Europe

1601
in other sheries, like the signicant and high correlation between the temperature in the Barents Sea and both the 0-group index and recruitment of Arcto-Norwegian cod (Dippner and Ottersen, 2001). However, we should be cautious with this result, because the SST data were obtained from a model rather than from direct observations. The model SST could not reproduce the observed interannual variations in temperature, but they did reproduce the trend in air temperature and SST over several decades. Variability in the long time-series of the bluen tuna catches in Mediterranean almadrabas was probably caused by the longer term periodicity in solar activity and the 22-year cycle for the reversal of the suns magnetic eld, the so-called double-solar cycle described by Reid (1988) and Friis-Christiansen and Lassen (1992). According to Ravier and Fromentin (2001), these factors explained between 45 and 80% of the variability in tuna catches in the Mediterranean. They also identied a 100-year periodicity in bluen catches. The 11-year cycles of sunspots were too short to produce a signicant change in the atmosphere, owing to the climate inertia. In addition, the variations during these cycles were weak. Nevertheless, solar activity exhibited an 80-year cycle (7283 years), the so-called Gleissbergs cycle, and the variation caused by this phenomenon could be more important on the atmosphere than shorter cycles because of the greater periodicity. The Maunder minimum is attributed to this phenomenon (Gleissberg, 1958). Our results indicate that climate accounted for up to 12.3% of the total variance in tuna catches, possibly through the strong effect of CO2 on the decrease in the primary production which could have affected larval survival. Population dynamic components (temporal effects) undoubtedly played an important role, representing variances of 12.3 43.1% in an autocorrelated process. In addition, we found that up to 35.7% of the variance was accounted for by the joint effect of climate and population dynamics. We could not ascertain whether part of the shared variance was the result of external climate forcing that inuences the environmental conditions (food, predators, natural competitors, climatic conditions) feeding back onto recruitment, or simply because of the time-scale needed by natural resources to recover after anomalous periods. We think that, in this case, environmental conditions (radiation changes, primary productions changes, cold years) affected recruitment negatively. Fishing effort during this period was too low to have affected the population dynamics signicantly. We did not nd a signicant relationship between the NAO index and tuna catches, but this may be the result of the lack of consistency in the NAO reconstructions (Schmutz et al., 1999). As already mentioned, Santiago (1998) reported a relationship between the winter NAO index and bluen tuna catches. Conversely, given that almadrabas have not undergone signicant changes in the past ve centuries (Lopez-Capont, 1997) and that they capture a proportion of the migratory populations of tuna, we can consider that the shing effect was almost constant, at least during the period studied, in the Mediterranean and in the Atlantic coast of Spain, Morocco, and Portugal (Ravier and Fromentin, 2001). We believe that piracy and other social factors could have had sporadic effects on the shery, although of lesser importance, given the long-term downward trend in the catch series. Even the recruitment of active shers to prepare for the Journey to England could not have had a long-lasting effect on the shery, because it did not need a specialized workforce

Figure 3. Almadraba tuna catch series and predicted values from a GLM model. between solar radiation and climate during the Maunder minimum; this implied a low temperature period in Western Europe and over the whole world (according to Lean, 2000). During this cold period, rivers and lakes that were normally ice-free froze and the snow cover did not melt at any time of year, even at low latitudes. In the middle of the 18th century, temperatures dropped so low that the Baltic Sea and the Thames and Ebro Rivers froze regularly. In addition, the Maunder minimum was related to the least productive period of the almadraba shery, specically from 1672 to 1724. Volcanic eruptions (Huaynaputina in 1600 and Mount Parker in 1641) contributed to colder temperatures in part of the world within the Maunder minimum (Fagan, 2000; Search, 2004). However, during this period, various social events inuenced the shery, e.g. plague outbreaks and the Spanish War of Succession, and these reduced the number of shers. The extremely low catches in 1703/1704 are a good example of this socio-political situation, probably owing to the effect of the EnglishDutch military campaigns in Cadiz and Gibraltar. Nevertheless, the strong oscillations observed in the catches had an important climatic component. The negative effects of the Maunder minimum were also reected in similar sheries off Sicily, Sardinia, and northern Africa (Fromentin et al., 2000; Ravier and Fromentin, 2001, 2004; Fromentin, 2003). For instance, in the longest series from the almadrabas of Favignana Formica in Sicily, it is possible to detect the effects of the periods with low sunspot numbers denoted as Dalton and Modern. In addition, the relationship between SST (Zorita et al., 2005) and catches could have been affected by a lag of 6 7 years between larvae hatching and the age of recruitment to the shery. According to Rodrguez-Roda (1964), bluen tuna caught in the Spanish trap shery were between 5 and .15 years old (50 to .400 kg), and with a state of similar sexual maturation every year (ICCAT, 1999). Similar relationships have been described

1602
(it was continuously augmented by non-specialized men, called ventureros or adventurers, and even by prisoners; Fundacion Medina Sidonia, 2005). If we assume that variations in shing effort as a result of wars, epidemics, or economic crises had not signicantly inuenced the general trend (except perhaps for short periods), we can identify the relative climate effects on the tuna populations. These changes were, in part, negative for the shery and could have occurred because of two principal mechanisms: (i) a reduction in the survival rate of larvae and early juveniles, and (ii) a change in migration patterns between the Atlantic Ocean and the Mediterranean. In our opinion, the second hypothesis is unlikely to be valid, because bluen tuna (the main species in the shery, according to Martn Sarmiento; Lopez-Capont, 1997; Ravier and Fromentin, 2001) and other tuna species were caught in the Mediterranean almadraba traps even during the coldest years, indicating that the migratory routes had not changed, at least, for a part of the populations. However, partial changes in migration could be enough reason to explain large changes in catch, specically if changes in the climate variations affected nearshore waters more strongly than offshore ones, and sh migrated out of the almadraba shing grounds. In addition, as inferred from the results reported by Polovina (1996), tuna spawning areas might not have changed, but there could have been an important reduction in the numbers of larvae or juvenile recruits if there had been climatically induced changes in prey availability (Sundby, 2000; Sirabella et al., 2001). In this sense, water temperature may have played an important role in governing tuna metabolism, food availability (Chambers et al., 2001), and survival rates and larval distribution (Richards et al., 1989; Pepin, 1991; Polovina, 1996). Moreover, in the Mediterranean, bluen tuna and albacore generally spawn when the SST reaches 24 25.58C (Rodrguez-Roda, 1964; Ueyanagi, 1971; Bard, 1981; Mather et al., 1995; ICCAT, 2003; Rooker et al., 2003). We reached the same conclusion as reached for the Icelandic Fisheries for a similar period (Ogilvie and Jonsdottir, 2000). Socio-economic factors were partly the reason for the decrease in catches. However, severe climatic conditions from 1680 to 1760 must have had more direct effects on sh abundance in Icelandic waters. Cold ocean temperatures would almost certainly have reduced sh stocks (Ogilvie and Jonsdottir, 2000). Low temperatures could have affected an important part of the bluen spawning areas during the coldest years, especially during the Little Ice Age, thus affecting recruitment negatively. A signicant reduction in recruitment during several years (especially during the Maunder minimum) could have reduced the tuna populations sufciently to impede the recovering of the sheries. It begs the question, though, why the tuna catches never recovered to the levels observed before the Maunder minimum after the climate had been restored to its earlier state? The reason is probably that tuna had not changed their migration behaviour during the past millennia and that climate changes reduced their populations to critical levels. The current continuous effect of shing is preventing rehabilitation of the Atlantic tuna stock. The increase in shing capacity and technology from the Industrial Revolution to the present (from mid-1800s until today) has had a signicant negative effect on tuna populations worldwide, which has impeded the rehabilitation of tuna stocks (Myers and Worm, 2003; Pauly and Maclean, 2003).

U. Ganzedo et al.

Acknowledgements
We are grateful for the support of the EKLIMAXXI Group (Basque Government, Department of Industry and Basque Meteorological Service-Euskalmet, Project ETORTEK07/01-IE07-190), and to the Angel Borja from AZTI (Marine Research Division). We dedicate this study to the memory of Professor F. Lopez Capont for his compilation work and publication of historical, highly valuable documents, such as the letters of the monk Martn Sarmiento.

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