ICES C.M. 1996
THIS PAPER NOT TO BE CITED WITHOUT
PRIOR REFERENCE TO THE AUTIIOR
PAPER 5:45 - Theme Session S
•
RELATIONSHIPS BETWEEN ANCHOVY (Engraulis encrasicholus) RECRUITMEl'\TT AND THE
UPWELLING IN THE BAY OF BISCAY DURING THE PERIOD 1967-1994
BORJA, Angel; URIARTE, Andres; MOTOS, Lorenzo and VALENCIA, Victoriano
AZTI; Avda. Satrustegui, 8; 20008-San Sebastian (SPAIN)
Tel: 34-43-212503,jax: 34-43-212162, E-mail: angel@;oc.azti.es
ABSTRACT
Oceanographical conditions in Spring and Summer, caused by Northerly-Easterly \\1nds of medium and low intensity, in the Bay ofBiscay induce good levels ofrecruitment to the anchovy population. This
\,ind regime produces upwelling conditions with, generally, low degrees ofturbulence. Indices ofthese two environmental variables, upweIIing and turbulenee, were buiIt by the authors, sho\\ing whieh were significantly correlated \\ith an index ofannual recruitment ofancho\y (p<O.OOOI) for the period 1967-
1989. In this paper the authors present new data for the period 1967-1994, \\ith three different sources of recuitment data. The upwelling index could be responsible of about 70% ofthe variance in the index of recruitment ofthe Bay ofBiscay anchovy, being the turbulence less important in the recruitment. The likely explanations to this relationship are outlined and discussed in the frame of eurrent hypothesis about the processes determining recruitment ofmarine populations. Enhancement ofthe productivity and increased availability of food to the early life history stages of ancho\y seem to be the main consequence of the prevalenee ofweak upweIling conditions in this area during Spring.
KEY WORDS: anchovy, Engraulis encrasicholus, recruitment, environment, upwelling, turbulence, Bay ofBiseay
INTRODUCTION
Understanding the mechanisms involved in determination ofrecruitment in marine fish populations is a major challenge in fisheries' research. In the last years, the relevance of meso-seale ocean proeesses, and the climatie conditions driving them, in setting recruitment levels has become increasingly apparent
(BAKUN & PARRISH, 1982; BAKUN et al., 1991). Natural selection implies that reproductive strategies are the reply to the most crucial environmental factors regulating reproductive suecess (BAKUN, 1995).
Consequently, fish populations set their spa\\TIing periods and areas so that survival through early life history stages is enhanced and recruitment levels are increased under weakly cIimatic conditions.
Some different hypothesis have been put forward tI)1ng to explain the main meehanisms leading to recruitment variability (see review in HEATH, 1992). Namely, physical and biological (food and predation) processes are the bases ofthe different hypothesis. HJORT (1914) suggested that first feeding was a critical period and that coincidence ofhigh prey abundance during this life period was a necessary condition for survivaland recruitment sueeess ("critical period" hypothesis). CUSHING (1975), noted that
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the timing of both peak spa\\ning acthity of fish and the Spring ph)10plankton bloom could be a major determinant of interannual survival variability (lmO\\TI under the "match-mismatch" theory).
SINCLAIR (1988) argued against predominance offood-chain processes in determining spa\\nirig strategies. Some authors (ILES & SINCLAIR, 1982; SINCLAIR, op.cit.) postulate that physics predominates over food chain processes in the control of population biology ("member/vagrant" hypothesis). Maintenance ofthe spatial integrity ofany marine population is regarded as the most important faetor, and spa\\TIing times are adapted to the physical dispersh'e eharaeteristics of an area rather than to biological production characteristies. Retention of early life history stages by a favourable oeeanographic eondition is fundamental for survival. However, there is evidenee in the literature ofboth dispersal and food chain processes having influenee in year-class survival (HEATH, op.cit.).
Lasker's "oeean stable" hypothesis aecounts for physical processes affeeting food ehain eharaeteristies ofthe emironment (LASKER, 1978). Long periods ofstable oeeanie conditions lead to fme seale partiele aggregations enhancing food availability and survi\'al of larval stages. PETEIUvIAN &
BRADFORD (1987) found that mortality oflarval anchovy, Engraulis ringens, was inversely related to the number of ealm periods during the spa\\ning season. BAKUN (1985) found that the spa\\ning peak of pelagic fishes in upwelling areas coincides \\ith a seasonal minimum in offshore Ekman transport.
CURY & ROY (1989) have shO\\TI that reeruitment seem to be maximized at the "optimal emironmental
\\mdow" for moderate "mds in upwelling systems and \\ith detrimental effeets on lower and higher values.
SEPHERD et al. (1984), elaim that the problem arising when correlating c1imatic and fisheries variables (reeruitment prineipally), owes to the fact that there is no limit
the arnount of eorrelations to earry out and in many cases it is diffieult to establish whieh eorrelations are simply a matter ofluek.
The reason for this lays
the fact that the parameters affeeting the sueeess of a fisher)', ean follow one another or overlap in time, and even interaet against eaeh other. Thus, for example, temperature works better as apredietor in speeies living elose to the limits oftheir ranks, whilst \\iod veloeity and direetion are important in as much as they affeet the eurrents and are critical during the drifting period ofthe larvae
(BAKUN et al.,1991).
The fishery for aneho\y in the Bay of Biseay has changed dramatically during this century.
JUNQUERA (1986,1988) reIates the inerease (1920-1960) and drop (1967-1986) of eatehes ofanehovy, as weil as other biological events in the Bay ofBiscay, to general oceanographic changes in the Northem hemisphere. The rising period of the fishery was eoneurrent \\ith a regime of sea surfaee temperature warming, while the deereasing period coincided \\ith a cooling trend of surfaee temperatures and a lowering of salinity.
VALENCIA,
(in press), stud)ing time series (over 40 years), of sea surface temperature,
\\md and irradiance, have demonstrated that some environmental phenomena developed in the SE Ba)' of
Bisea)', e.g. lo\\' sea surfaee temperature (0.5
oe under the mean) in the 70's, are a loeal response to great scale oceanographic and meteorological events in the NE Atlantic.These authors have shO\\TI a relationship .
between these environmental phenomena \\ith the dominanee ofnortherly ,,,iods, whieh produee upwelling that eooled dO\\TI the surfaee waters in the southem area ofthe Ba)' ofBisca)'.
Anehov)' is a short li\mg speeies for whieh reeruitment plays a major role in setting the level ofthe stock. Spa\\ning of anehovy in the Bay of Biseay oceurs eaeh year during Spring (FURNESTiN, 1945;

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ARBAULT & LACROIX-BOUTIN, 1977; CORTel al.,1986; LUCIO & URIARTE, 1990; MOTOS et
31., in press), and the population spa\\TIS mainly in areas where inereased biological produetiori potentially oeeurs (MOTOS et al., in press): river plumes, shelf 3Ild shelf break fronts 3Ild oeeanie g)Tes
(SWODDIES)(Figure 1). In general, spa\\TIing is limited to the Freneh and Spanish coasts (South of
46°30'N rind East of 5°W).
Aneho"y spa\\ners eontinuously produee eggs from April to July, although there is some marginal sPa\\TIing in Mareh and in August-September. Spa\\TIing aetivities are triggered by the Spring warming up ofsea surfaee waters and the major part ofthe reproduetive eITort coincides with its ma.ximum warming rate, whieh normally oeeurs in May-June (CORT et al., 1979; MOTOS et al. in press). Therefore, most eggs are produced at peak spa\\TIing, during May and June.
The time SP3I1 for development of eggs and larvae depends on temperature (BLAXTER &
HUNTER, 1982). At the prevalent temperature in the area during peak sPa\\TIing, egg development lasts for three days (MOTOS, 1994) and larval development takes as much as 60 to 90 days (SMITH, 1985;
PALOMERA et al., 1988). Data from the tuna live-bait fleet indicate that early juvenile stages start sehooling as early as August and they oecur during Summer and Auturnn in SE Bay ofBiseay (CORT et al., 1976; MARTIN & LUCIO, 1988; MARTIN, 1989; URIARTE & MOTOS, 1991). Consequently, anchovy eggs and larvae develop from March-April to July.
Mter metamorphosis, anchovy juveniles oecur from August up to next Winter when they disperse in the area. Oceanographical events happening in eoneurrent periods :md areas should playa primordial role in the d)namics ofthis early life history stages
:md in the subsequent reeuitment strength.
BORJA et al. (in press) have shO\\TI, for the period 1967-1989, that oce3I10graphieal eonditions eaused by Northerly-Easterly \\inds ofmedium arid low intensity in Spring-Summer in the Bay ofBiscay seem to induce good levels of reeruitment to the anehovy population. This \\md regime produces weak upwelling conditions \\ith generally low degrees of turbulence. Indices of these two environmental variables, upwelling and turbulenee, were shO\\TI to be significantly correlated \\ith 3I1 index of annual reeruitment ofthe anehovy (p<O.OOOI) for that period. Both physieal parameters explained about 70% of the vari:mee in the index ofreeruitment ofthe Bay ofBiseay ancho\y.
In the forementioned paper the authors stated that the relationship between reeruitment of aneho\y in the Bay ofBiscay:md oee:mographical eonditions (upwelling:md turbulenee) needed to be cheeked \\ith the most reeent years ofdata in order to exclude espureous eorrelations. The possible eonfirmation ofthis relationship would largely enhanee the comprehension of the d)namies of this resouree in the Bay of
Biseay, \\ith potential use for the future m3I1agement.
The eurrent paper eompletes the series of data up to 1994 and review the consistency of the relationships between the environment :md the anehovy recruitment.
;\IATERIAL AND METHODS
Reeruitment variability of the Bay of Biseay anehovy population was studied by means of a reeruitment index (IR), ealeulated by URIARTE (1993) for the period 1965-1994.
It derives from the matrix of Spanish purse seine eatehes of aneho"y (in numbers at age) for the first half of eaeh year. The index ofthe level ofthe reeruitment produeed from the spawning of eaeh year is eaIeulated by summing up all eatehes (eorreeted by eITort) obtained from the eohort born in eaeh year (BORJA et al., in press),

and expressed as number ofindividuals (in thousands) per cohort per vessel.
Anchovy sPa\\TIing occurs in Spring and first catches included in the recruitment index happen in
February-March ofthe following year, onee anchovies are one year old. Spanish catches from the first half of each year account for about 95% ofthe total annual eatch.
In this paper, for the most recent period 1986-1994, two new measures of reeruitment were studied: the DEPM population estimates in numbers of one year old anchovies and the 1996 ICA
Assessment estimates of anchovies of 1 group (ANON., in press). The one year old anchovies of 1993 were not measured by any DEPM or acoustic survey, but for the purposes of this analysis it has been assurned that the nurnber ofthis anchovies were the same than those deteeted by the DEPM in 1992. This is based on the fact that the cumulative catches of the year classes of 1991 and 1992 (YCC) were approximately equal (table 10.10 of ANON., 1996) and the recruitment at age 1 estimated by the ICA assessment performed in 1995 (ANON., 1996) were equal for the 1991 and 1992 year classes.
The upwelling and turbulence were calculated from the time series ofwind stress and direction in the Bal' of Biscay, between 1967 and 1989 (SMITH & BAKUN, 1989) . This series is a spatial mean of the geostrophical pressure field derived from sateIIite data, in a 3°x3° rectangle eentered in 45°N and 2°W, therefore, located in the inner part of the Bay ofBiseay which is the main spa\\ning area for anchovy
(MOTOS et al., in press). The wind index gives direction and intensitl' averaged over six hours for the area ofreference. The data for the period 1990-1994, for the same area, has been provided by the Data Manager
Head Services from PEFG ofthe NMFS (USA).
Turbulence was calculated as the cube Of\\1nd stress (BAKUN & PARRISH, 1982), from May
(sPa\\ning season) to Januar)' ofthe next year; the period which showed for the turbulence index the highest correlation with the index ofrecruitment for 1967-1989 (BORJA et aI., in press). This provides information on \\md induced turbulent mixing, giving an idea ofvertical stability ofthe sea
UpweIling is related to surface transport generated by \\ind. The SE region ofthe Bay ofBiscay presents a striking change in the coast orientation. The French eoast shows a N-S orientation, while the
Spanish coast has an E-W orientation, being the Basque Count!)' a transitional region (Figure 1). Northem
\\inds produce upweIling on the French coast, whereas Eastem winds produce it on the Spanish coast.
UpweIIing values for every 6-hour-observation were calculated by means of the algorithrns provided by BAKUN (1973), being expressed as m 3 .sl .km1 ofcoast. Monthll' upweIIing was calculated as the mean of available daily data.
BORJA et al. (in press) established that the expected time period where environmental conditions are critical for survival of early life stages is from March to July because it contains the peak spa\\ning and most ofthe developmental period ofancho\y eggs and larvae up to late larvae or even early juvenile stages.
Assuming that upwelling conditions could in general favour the reeruitment of anchov)', the
S)nthetic upwelling index created by BORJA et al.(in press) for a given year is based on the addition ofthe upweIling values ofthe months showing on average positive upweIling events behveen March and July.
For the same reason, given that the spa\\ning area ofanchovl' extends along the French and Spanish eoasts ofthe Southeastem bal' ofBiseny, the authors decided to add up the upwelling values [ound
both coasts.
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FRANCE
47
46
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45
6
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AIN
5
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4 3
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AN SEDASTI..AN
.2
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1
1992
16
13
al.,1995
Spa\~l1ing
44

•
RESULTS
Figure 2 plots the interannual variability in the recruitment and upwelling indexes from 1967 to
1995. Upwelling values over
800-900 m
3
.s·
1
bet\veen
March and July, favour good
8 0 0 0 . , - - - - - - - - - - - - - - - - - - - - . . , . 1 6 0 0
7000 1400 recruitments thous.indiv.
(>2000 captured cohort and vessel).
per
The parallelism of both series holds for the most recent years of data as weIl as
XC;
~
Z :-
;::~
Z,r: w
0
::;: u
!:::;;
;:) c:
0:"" o:!
5
6000
5000
4000
3000
2000
\ ....
.
.
I ....
...
....
.
,
1200 x w
1000 ~ _
800
600
(;~
~ ~
..J
E
~-
0-
400 ;:) for the whole period. The extension of the data series with 5 new years up to 1994
1000
'"
'"
•
....
'"
0>
'" c;;
~
'"
~
'"
~
200
0 confirm the previously found relationship between the recruitment and upwelling
YEARS
FIGURE 2: Plot ofthe interannual variability ofrecruitment and upwelling indexes indexes (Table 1), with a slightly increase ofthe correlation coefficient.
Table 1: Comparison between the results obtained by BORJA et al (in press) for the period 1967-1989 and the results obtained in this paper for the period 1967-1994. The results refer to the correlation between upwelling and recruitment and upwelling+turbulence \\ith the recruitment (n:number of data, df: degrees of freedom, R2 : explained variance).
Years
Upwelling (U)
U + Turbulence n
23
23
BORJA et al. (in press)
1967-1989 df
22
21
R'
60.42%
67% n
28
28 df
27
26
This Paper
1967-1994
R'
61.15%
64.72%
800J . , - - - - - - - - - - - - - - - - - - - - ,
..
Gi
=
6000 w >:
:E'I::
....
0
Il::
~
U
4QCX)
•
Il:::i
2000
E.
o
.1--_
"--_-+'-----''--_ _
_>___ _
- _ > - - _ - 1 o
200 400 600 800 1000 1200 1400 1600
UPNaLING
(m3ls .km)
FIGURE 3: Linear regression model between recruitment and upwelling indexes for the 1967-1994 period.
5
On the other hand, 1994 year has not a definitive value of this variable, because of the lack of 2 years old data corresponding to 1996.
Table 2 shows the results of fitting a lineal regression model of upwelling on the index of recruitment to the complete
1967-1994 data set, whilst Figure 3 shows the fitted model.

Table 2: Linear model of a regression analysis between recruitment (dependent variable) and upwelling (independent variable), \\ith 27 degrees of freedom. Tbe correlation coefficient was 0.78 and the R~=61.15%.
PARAMETER
Intercept
Siope
ESTIMATE
-1820.65
4.93
SOURCE
Model
Residual
Total (Corr.)
SUMOFSQ.
4.95.e
7
3.14.e
7
8.09.e
7
Regression analysis
STANDARD ERROR
670.15
0.77
Analysis of Variance
MEANSQ.
4.95.e
7
1.21.e
5
T- statistic
-2.717
6.397
p.
value
0.0116
0
F- Ratio
40.92
0
P- Value
On the other hand Table 3 shows the regression analysis for both upwelling and turbulence. With the complete set of data the inclusion ofturbulence in the analysis does not seem to reduce significantly the residual error ofthe regression model.
Therefore the role ofthe turbulence on determining the recruitment is not significant statistically, suggesting a minor role in the determination ofthe recruitment compared \\ith the upwelling index. Here, as in BORJA et al.
(in press) it is found that turbulence could affect negatively the index ofrecruitment.
Table 3:Multiple regression analysis between recruitment (dependent variable), upwelling and turbulence (independent variables), with 27 degrees offreedom. The correlation coefficient was 0.80 and the R~=64.72%.
•
PARMffiTER
Constant
Upwelling
Turbulence
SOURCE
Model
Residual
Total (Corr.)
ESTIMATE
74.99
4.89
-14.67
SUMOFSQ.
5.24.e
7
2.86.e
7
8.09.e
7
Regression analysis
STANDARD ERROR
1358.17
0.75
9.22
Analysis of Variance
MEANSQ.
2.62.e
7
1.14.e
5
T- statistic
0.055
6.525
-1.59
22.93
F-Ratio
0.956
0
0.124
P-value
0
P- Value
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I-
-
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,...--
:.:~""
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.........:' ,'\ i
. '
'" 'DEPM ' . "
...,.
....
.
,
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.,
"
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-1~
\L
'. '.
\
....
,'_
FIGURE 4: Plot ofDEPM, ICA assessmcnt and upwelling between 1986 and 1994
...
-
...
:1
The comparison between the DEPM estimates of one year old anchovies and the upwelling index of the year before (period
1986-1993) is represented in the Figure 4 and the regression model and Anova test are shO\\TI in Table 4. Figure 4 shows also the comparison between the recruitment estimates at age 0 provided by ICA assessment and the upwelling index ofthe same year (period 1987-1994). The respective regression model and Anova test are shO\\TI in Table 5.
Table 4: Linear model of a regression analysis between DEPM (dependent variable) and upwelling (independent variable), with 7 degrees offreedom. Tbe correlation coefficient was 0.89 and the R2=78.93%.
PARAMETER
Intercept
Slope
SOURCE
Model
Residual
Total (Corr.)
-2876.66
7.53
ESTIMATE
SUMOFSQ.
3.09.e
7
8.25.e
5
3.92.e
7
Regression analysis
STANDARD ERROR
1285.27
T- statistic
-2.238
1.59
Analysis of Variance
4.741
3.09.e
7
1.37.e
5
MEANSQ.
22.48
F- Ratio
0.0665
0.0032
0.0032
P- value
P- Value
Table 5: Linear model of a regression analysis between ICA assessment at age 1 (dependent variable) and upwelling
(independent variable), \\ith 8 degrees offreedom. The correlation coefficient was 0.88 and the R2=78.4%.
PARAMETER
Intercept
Slope
SOURCE
Model
Residual
Total (Corr.)
ESTIMATE
-2798.6
9.14
SUMOFSQ.
4.71.e
7 l.3.e
7
6.01.e
7
Regression analysis
STANDARD ERROR
1490.8
1.81
Analysis of Variance
MEANSQ.
4.71.e
7
1.86.e
5
-1.88
5.03
T- statistic
25.34
F· Ratio
0.1026
0.0015
P- value p.
0.0015
Value
7

DISCUSSION
The addition of new data ofrecruitment and upwelling indexes to the series ofBORJA et al (in press) has confirmed that this two variables are positively correlated. On average, about 61 % of the historical variability ofthe recruitment inde.x is explained by the upwelling index. The role ofthe turbulence is ofless relevance in the determination ofthe reeruitment, but it could be important to explain some years with unexpected recruitments. Here, as in BORJA et al. (in press), it could have a negative influenee.
Spring upwelling conditions and the recruitment 0/ anchovy in the Bay 0/ Biscay.
The highest correlation between the reeuitment and the upwelling indexes was found when the whole period from March to July was considered. This time span coineides \\ith the development period of anehovy eggs and larvae. Therefore, this correlation says that Northern and Eastern "inds produeing upwelling conditions in Spring favour anchovy reeruitment.
In the Bay of Biscay offshore transport of surface waters and upwelling events result when
Northerly and Easterly "inds blow a10ng the French and Spanish coast, respectively. According to
VALENCIA et al. (in press), during the Spring-Summer transition, ,,,md speed and direction are quite variable in the SE region of the Bay of Biseay. During this period, Northerly and Easterly \\inds are prevalent instead ofSoutherly and Westerly "inds, which prevail in the Auturnn-Winter period. Whilst the mean wind speed show maximum values in Winter, it decreases in Spring and even drops significantly dO\m from Spring to Summer.
The rather variable direction ofthe \\md, and reduced \\ind speed, together \\ith the dramatic change in the orientation ofthe French and Spanish coasts, elearly differentiates this region from typieal upwelling areas such as California, Peru or, in a local companson, from the western Iberian eoast.
In regions of intense upwelIing, turbulence are considered low if they stay under 400 m
3
.s·
3
NELSO~,
1982) or 200 m
3
.s·
3
(CURY &
(HUSBY &
ROY, 1989), depending on the areas. In the bay of Biseay, Spring values ofturbulence over 155 m 3 .s· 3 are considered high by BORJA et a1. (in press), because turbulenee over 200 m
3
.s·
3 are only found in Winter and Autumn. Values over 400 m
3
.s·
3 are "ery scarce in trus urea
The low intensity ofthe \\inds producing upwelIing eonditions in the bay ofBiscay does seldom imply a breakdo\,TI of surface water layers by eolder and rieher deep waters. The upwelling effect can be restricted to pushing up the thermoeline elose to the surfaee (VALENCIA, et al., in press), making light more accessibly to the plankton coneentrations at this fringe and increasing the subsurface chlorophyll ma\:imum. In this way, productivity can be enhanced around the thermocIine \"ithout cold subsurface waters being detectable at the surface. For instance, in May upwelling conditions are generated by a mean
\\ind veloeity of 4,5 m.s·t, which causes low turbulence (90m 3 .s· 3
).
Therefore the Northern and Eastern regimes of\\ind in Spring \\ill produce weak upwelling processes, associated \\ith stability and shallow but pronouneed stratification of surface waters.
The offshore horizontal transport of coastal waters produced by the Northern and Eastern regime of\\inds may play by it selfanother relevant role in the enhaneement ofthe productivity in the bay. The influenee of the low salinity plumes of several rivers in the Bay of Biscay (Gironde, Adour, and many smaller Spunish rivers) are apparent in surface water layers along importunt shelf ureas. Those areas are kno\\TI as spa\ming grounds for ancho\y (MOTOS
in press), probably due to the enrichment produced by the outflow of those rivers. \Vhen the offshore advection of coastal \Vaters under upwelling
•

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J e conditions are relevant in the Spring, there is a spreading out ofthe influence ofthe river plumes over \vider areas than normal, and the effect of enrichment of sea surface waters is expanded. Eggs moving in those waters wiII remain in a rather stable, nutrient rich environment.
Therefore, two factors of enrichment of global productivity in the Bay of Biscay may be linked to prevalent Northeastem wind conditions: Weak upwelling conditions and extension ofthe area influenced by the river outflows. Both factors, together "ith low turbulence and stability, may act to enhance the probability ofanchovy early life histor)' survival by means ofincreasing food availability.
These Spring upwelling eoriditions are, in general, coincident \\ith the suitable environment described for the small pelagic recruitment in the literature: The weak upwelling coriditions, the relative stability and expected enhancement of food availability matches weIl \\ith the "Ocean stable" hypothesis of LASKER (1978). This hypothesis states that food quality is also improved as dinoflagelates are better food for ancho\y larvae than diatoms. The latter are produced in the presenee of intense upwelling, whilst dinoflagelates appear in ealm and stable eonditions (LASKER, 1981)
The low wind speed and turbulences assoeiated to the upwelling eonditions during the spa\\ning of ancho\y in the bay are in agreement \\ith the BAKUN & PARRISH (1982) statement about the pelagie fishes in upwelling regions which are deemed to ehoose for spa\\ning areas of lowest turbulenee and mixing. MENDELSSHON & MENDO (1987) and CURY & ROY (1989) suggest 5 m.s· l as the \\iod speed for emironmental
Y..
indows leading to maximum reeruitment of small pelagicfishes. VALENCIA et al. (in press) fmd that the upwelling conditions in the bay take place elose to this threshold velocity.
CDRY & ROY (1989) indicate that nonlinear statistic methods should be used to eope \\ith the expected dome shape relationship betweeri recruitment and upwelling in Ekman-type upwelling systems.
Othemise, the relationship eould be masked.
In the Bay ofBiseay we have sho\\TI that a linear model can sufIiciently explain the relationship between both variables. This may be due to the fact that the maximum upwelling indices found during the spa\\ning period of anchovy in this area (between 1200 and 1400 m
3 l
S'l.km· ) are about the range suggested by those authors for the optimal environmental \\indows. Therefore
• in the Bay ofBiscay, the weak upwelling conditions limits the study to the left side ofthe dome shape curve
(the inereasing branch ofthe eurve), where the eurve can be approach by a linear relationship.
Transport from spa\\nmg centres \\iU vary depending on the \\md direction that induces upwelling.
Thus, a northerly \\ind \\iU make that waters elose to the Gironde estuary move towards Cap-Ferret, and those elose to the Adour towards the Spanish self edge and coasts (Figure 1). On the other side, Easterly winds blo\\ing in the Northem areas will eause a Northeastward displacement over the eontinental shelf, which will eventually move towards the shelf edge on its northern side, while in the Adour and Cantabrian coast the transport \\ill be towards shelf edges ofthose areas.
Emerging 3 mm larvae ean only s\\im at speeds of 0,1 to 0,2 ern.s"!, depending on water temperature, and they are not capable of overcoming typical surface currents. of this weak upwelling eonditions, ofthe order of 10-15 em.s· l
.
Therefore, the larvae \\ill need food dose to them to survive..
Fortunately, llOder those regimes of\\ind, eggs and larvae \\ill be transported in a "nourishing environment" which facilitate food availability to them. During this transport towards the outer shelf or, in eases, further beyond it, eggs and larvae \\ill be dispersed. This dispersion may imply areduction oflarval eompetition
9

and cannibalism by adults since they \\iU continuously be moved out ofthe spa\\ning centres.
SrNCLAIR (1988) states that retention of early life history stages by a favourable oceanographic system is fundamental for survival. The advection and dispersion of eggs and larvae towards offshore and along the Cantabrian sea, under the Northerly-Easterly \\ind regime, do they imply an increase ofmortality of the anchovy larvae? There are no direct studies ofthis subject available by the time being. However, some authors reported that anchO\y juveniles can be detected occurring both in offshore and inshore areas
(CORT et al.
1976, URIARTE & MOTOS, 1991) at the end of Summer and Autumn in years of good recruitment, indicating that good survival was general in all areas. Taking into account the weak strength ofthe Northerly-Easterly regimes of\\ind in this region and the limited geographical area ofthe SE corner ofthe Bay ofBiscay, it is not clear that Ekman transport towards offshore areas \\iU imply any detrimental for the sUfvival of larvae. Enhanced biological production resulting from prevalent oceanographical conditions could assure good survival rates over most ofthe area. In addition, the vertical environment of anchovy early life history stages -layers above the thermocline - would be more stable, reducing the risk ofvertical dispersh'e processes and related losses towards the bottom.
Downwelling conditions in the Bay
0/
Biscay in Spring
In the Bay ofBiscay, the usual speeds ofWestern and Southern \\inds are in general stronger than those coming from the North or East In general the former predominate in the Autumn and Winter seasons producing relative high turbulence and dO\\TIweIIing along the Spanish and French coasts (BORJA et al., in press). Years \\ith those \\inds prevailing in Spring and early Summer show dO\\TIwelling conditions and coincide in general \\ith low recruitment levels ofanchovy. The most relevant example of dO\\TIwelling conditions in both coasts in Spring happened in 1983, which resulted in subsequent bad recruitment.
The consequences ofthe dO\\TIwelling conditions and relative high turbulence are: low stability and stratification, and less intense and deeper thermoclines than under weak upwelling conditions. Plank10n \\iII be transported and dispersed \\ith the eggs and larvae within a \\ide column ofwater. In that sense food availability \\iII be reduced to the larvae. In addition the areas of influence of the river plume \\iII be diminished due to tpe advection ofwaters towards the coast. All these features would probably imply a general drop of productivity in the SE Bay ofBiscay during the periods of prevalence of that regime of \\ind and a reduction ofthe suitable environment for the success ofthe early life history stages of anchovy.
Balance beMeen Downwelling and Up'r1:elling conditions in the Bay o/Biscay in Spring
Upwelling events are usual in the French Coast during Spring, while those events are less frequent along the Spanish coast in that period. By the end of Spring and in Summer weak upwelling conditions become also frequent along the Cantabrian coasts. The major spa\\ning grounds of ancho\)' are knO\\TI to expand between May, June and July (CORT et al., 1976~ MOTOS el al.
in press), extending from the
French shelftowards the West along the Spanish shelfand towards the North. That expansion has been related to migration ofsuccessive size classes ofaduIts triggered by temperatures (CENDRERO ed., 1994).
In the years of best recruitments, like in 1975, 1976, 1982, it is observed that upwelling conditions along the Cantabrian coast were already prevalent during the Spring (BORJA et al., in press). These observations emphasize the idea that recruitment of anchov)' in the Bay of Biscay is enhanced by the opening of spatial and temporal \\indows ofweak upwelling conditions. The traditional spa\\ning centres elose to the major rivers und along the continental shelf edge \\iII always assure a minimum level of recruitrnent for the population, but the major variations ofrecruitment \\ill depend on the conditions induced by the regimes
10
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.

,
•
I
(
I
· 0
,.~ ~ ~.
" ofwind during the early lire history stages.
It is a common feature in the bay ofBiscay that Winter do\\nwelling conditions last until April followed by weak upwelling conditions afierwards. Aiichovy takes profit ofthis change for spa\\ning. In general, SP3\\TIing acti\ities of anchov)' in March and at the beginning of April are low. However we ha\'e found that the indusion ofMarch in the computation ofthe upwelling index improved the correlation with the recruitment index. This improvement is principally due to the influence ofyears 1970 and 1973.
Both years produce good recruitment, in which more than 50% ofthe Spanish annual captures occurred between
March arid April (BORJA et cl., in press). This phenomenon can be interpretated to be linked to an earlier onset of the Spring season (URIARTE 1988), which rnight indicate an early spa\\ning in those years.
Therefore, upwelling conditions at the beginning ofthe Spring may induce early spa\\ning. Altematively, it may happen that earlier upwelling conditions playa role in setting the condition factor of spa\\ners during the incoming spa\\ning season, with potentially impoi:umt implications in the future survival ofthe offspring
(BLAXTER & HUNTER, 1982).
Injluence 0/ turbulence on the recruitment 0/ anchovy.
Another factor affecting recruitment is the turbulence set up from May to January.
It includes the developmental time of most egg and larvae and all the juvenile phases up to Winter dispersion. Turbulent rnixing may disrupt food aggregations at the subsurface chlorophyll maximum and may affect the vertical distribution of eggs, larvae andjuveniles, leading to higher rates of mortaliiy
(01' losses towards the bottom).
The addition ofthe turbulence index between May and October to the regression ofupwelling index on the recruitment index did not imply an increase ofthe explained variance ofthe regression model. This rnay be partly due to the fact that, in general during the Spring and Summer seasons turbulence is always low and the interrinnuaI variation is minima compared to the Autumn and \Vinter seasons or to the recruitment index. Ouring Spring and most ofthe Summer the early life history stages of anchovy are unable to beat and overcome the currents, so that they are transported by them approximately until they reach 80 mm (THEILACKER & OORSEY, 1980).
Juveniles ofthe Bay ofBiscay anchovy reach those lengths about the end ofAugust and September when schools ofjuveniles ofthat length are observed and caught for live bait purposes in the tuna fishery (MARTiN, 1989).
The indusion ofAutumn and Winter rnonths in the index ofturbulence improved the fitting ofthe recruitment index by the regression model. In these periods the pelagic schools ofjuveniles approach the
French and Sparush coasts foroverwintering (CORT et al.
1976, URIARTE & MOTOS, 1991, PROUZET
& LURO, 1991).
The above results suggest that during Auturnn and Winter, turbulence rnay affect the survival ofjuveniles. This may be due to a disruption of particle food aggregations around the thermocline,
01' to disturbing the normal spatial migration pattern ofjuveniles.
JUNQUERA (1986, 1988) suggested that environment may have driven the major changes in the fishery and the population ofthe Bay ofBisea)! aneho\:y during the eurrent eentury. Our study provides a link between the environment and the population since 1967: The positive relationship between the level ofancho,,)' recruitment and an index ofupwelling induced by the prevalence ofthe Northerly and Easterly wirids in the Bay ofBiseay during Spring and early Summer. Lo\v turbulence up to the next Spring seems to help the success of recruitment too. Oceanographic processes linked to this regime of wind seem to enhanee stability and general productivity in .the Bay of Biseay and therefore increase the availability of larvae and juveniles to food, increasing their survi\'al expectations. Several direct oeeanographie and
11

- - - - - - - -
- - ecological mechanisms have been discussed in order to explain this finding (weak upweIling conditions,
\,idening of the influence of river outflows, stability and stratification of the water profile, etc.). These mechanisms fits weIl \,ith the ideas ofBAKUN & PARRISH (1982) and ROY (1993) about the physical factors driving recruitment and \\ith the LASKER's ideas (1978) about mortality variability of early life history stages by food chains. However these or other underlying mechanisms should be further identified and studied in future field research.
The obtained results suggest the potential use of this upwelling index to forecast the recruitment ofthe Bay ofBiscay anchovy, calculated either by direct (DEPM) or indirect methods (from captures).
ACKNOWLEDGEMENTS
This paper is a summary of the most relevant results obtained [rom a broader work about the recruitment of anchovy and oceanographic conditions in the Bay of Biscay undertaken \,ithin the frame of an UE project (CENDRERO, ed., 1994) carried out in cooperation \\ith IFREMER, AZTI and IEO. This work was sponsored partly by the Basque Government (Spain) and by the Cornmission ofthe European
Communities (DG XIV), \\ithin the frame of an International EC FAR Project (1991-1993) entitled
"Improvement of stock assessment by direct methods, its application to the ancho\y (Engraulis encrasicholus) in the Bay ofBiscay", (Contract No. MA 2495 EF).
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