..

MonthlySpawning Stock and EggProduction of Peruvian Anchoveta(Engra~/is ringens), 1953 to 1982*

D. PAULYM. SORIANO

International Center for LivingAquatic Resources Management (ICLARM)

MC P.O. Box 1501

Makati, Metro Manila

Philippines

PAULY, D. and M. SORIANO. 1987. Monthly spawning stock and egg production ofPeruvi.an anchovel3 (EngrauJis rillgens). 1953 to 1982, p.167-178./11 D. Pauly and L Tsukayama (cds.) The Peruvian anchoveta and iLsupwelling ecosystem: ~ decades of change..ICLARM Studies and Reviews IS, 351 p. Instituto del Mar del Peru (IMARPE), CalIao, Peru; Deut.sche Gesellscbaft flir Tecbniscbe

2J:s3lJlI!1enaIbeit (GlZ), GmbH, Eschbom, Feder2l Republic of Gennany; and International Center for Living Aquatic ResourcesManagement (ICI..AR..\1), Manila, Philippine!.

Abstract

Available data on the reproductive biology of the Peruvian anchoveta (ElIgrauJis ringens, nonhem/caltral stock, 4-1405) are reviewed andlUed to estimate monthly spawning size and egg production iran January 1953 to December 1982. Basic information used are: (a) monthlybiomass by length class (4 to 20 em), (b) a model relating the shape and position of the matUration ogive to sea surface tcnperatUre, (c) seasonalpatterns of matUrity, (d) batch fecundity estimates of fcnales anchoveta and (e) various ancillary information woven into a coherent whole.Potential uses of the time series derived are discussed along with sources of errors and ways of reducing these.

Introduction

The reproductive output of the Peruvian anchoveta (Engraulis ringens) has been earlierreponed either in the form of relative egg densities, as estimated from egg surveys, or computed

..throughthe "egg-production methoq.",applied once to data from the 1981peak reproductive. season (Santander et al. 1984).'-,',:. In this contribution, the literature on anchoveta reproduction is reviewed. Available~information is used to estimate parameters used subsequently to compute monthly egg output by~Jhestock of anchoveta from 4 to 140Soff Peru, from January 1953 to December 1982, based on~.monthlybiomass data derived by Pauly, Palomares and Gayanilo (this vol.) and ancillaiy data

. !;presentedin detail furtherbelow...

Materials and Methods

t

r

fl!~ Model Structure

h' . .. Reproductive output (RO) in a given month (i =1-360) can be .viewedas the ultimate:~upt of different Jactors summed up over all length classes, Le.,

. -"'- ,.IClARM ContribuUon No. 382.

167

- - -

168

nROi= .k Bij.Pij'Aj.Sk"PFj'RF

J=1

. whereBijis the biomassof maleandfemaleanchovetain lengthclassj, Pij is thefractionofmature fishes in length class j, Aj is a size-specificempirical factor relating anchoveta fecundityper unit weight to length j, Sk is the average number of times a female anchoveta spawns permonth, with k = 1 (January) to k = 12 (December), PIj is the fraction of females of length j inthe population and RF is the relative batch fecundity {eggs/bodyweight in g) of a femaleanchoveta whose value of Ai is equal to unity.

The following sections aocument each of the variables and constant used in implementingequation (1).

...1)

l!iomass by Length Class..

. ... ..The estimates of monthly biomass by length class used here were taken from Pauly,

Palomares and Gayanilo (this vol.). The median lengths considered ranged from 4.25 to 20.25cm. As will be seen below, only fish above 12em contributed significantly to egg production.However, all computations were performed with all length classes included.

The Fraction of Mature Fish as Function of Length

Fig. 1 presents maturation ogives for anchoveta, based on data gathered by various authorsin the 1950s and 1960s. As might be seen, these data suggest that under average conditionanchoveta have a mean total length at first maturity ofL50 =14 cm. The mean maturation range(i.e., the length where 75% of the anchoveta have reached first maturity minus the length where25% have) is 1.8 cm. As will be noted from Fig. 1 and Table 1, the latter estimate is not veryreliable, being based on three authors whose work suggest a mean range of about 2.9 cm, andanother group of three authors whose work suggest a mean range of about 1.1 cm.

Tsukayama and Alvarez (1981) showed that in "wanner years" (i.e., in years during EI Niiioevents), mature fish were usually smaller than during cold years. Their figure has been redrawnhere as Fig. 2, and temperatures added, together with estimates of L50 based on the median ofthe class immediately preceding the model class - in analogy with length-converted catch curves,where the length class immediately to the left of the sample mode usually provides reasonableestimate of mean size at first capture (see Ingles and Pauly 1984).

The mean of these rough estimates of L50 is, in colder years indeed higher than the mean ofwarmer years (Table 1). Moreover, the mean of the 10 values of L50 in Fig. 1, corresponding toan intermediate mean temperature, fits neatly between the points for the "cold" and "warm" years(Fig. 3), confmning that the estimates of L50 in Fig. 2 are indeed reasonable.

These 3 sets of averages, representing a total of 25 pairs of L50 and temperature values,along with the mean maturation range of 1.8cm provide the key elements of our model forestimation of the factor Pij in equation (1). This model is structured aroul'!dthe logistic equation,which generates curves resembling the graphs in the-lower panels of Fig. 1, and has the form

P = 1!(1+exp(-rm(Lp-L50») ...2)

Given a knowledge of L50 and L25 (or L75) as obtained from the relationships in Fig. 3, theparameters rm of equation (2) can be estimated from

rm =loge(0.75/0.25»1L5o-L25 ...3)

or through the equivalent equation pertaining to L75.The model was implemented using the mean monthly temperaniies for 1953 to 1982 in

Pauly and Tsukayama (this vol.)

- -- - -

169

,.:;

CallaoMar.'61-Feb.'62T= 16.3 'C

L75=14.9L~=14.5L25 =14.0

CallaoMar. '62- Feb. '63T= 15.7 .C

L75= 15.1L~ =14.7L25=14.1

CallaoMar. '63-Feb.'54T=16.8.C

L7~=14.8L~o=14.2L25=13.7

8 9 10 II 12 13 14 15 16 r7

1.0

0.9

.0.8

.".,< . f 0.7::'t ;.:1 .

y.:j '0.6

:.;:S0.5

c" : ~ 0.4t

,

< ~ 0.3

.<;;~'..: 0.2,,;~\., 0.1

it.'.< ',:'r °£:..: . 7 8 9 10 II 12 13 14 15 16 r7 7;f;;.~;< Total length (em).f:r.."~"r.;.;..~",'

~;~'"F~. 1. Relationship between the fraction of mature anchoveta (E. ringens) and their total length off Peru (1953-1964).~;S'.; A: ba3ed on CJark (1954, Fig. 5, both sexes combined)~;.B: based on Clark (1954, Fig. 5, males only)'~2f:.: C: based on Jordan (1959, Fig. 9, erroneous values < 130 mm SL omitted)~Jc::~b: based on MiDano (1958, Table VDI, females, n = 6,142)

~~:~:(~:~a.sed on Einarsson et al. (1966, Fig. 8, both sexes combined) n = 726, 686, 565,508,929 and 614 for D-J, respectively.Ij(j~

.

.

..

'_r. r: "..;. .."'~,,..;I ~.

'I~~~::' .~~;.~~~:' .C~ .~.J4c.~~~ :

,

I

{.

.

..j

.

.'."

'l

..

12 13 14 15 16 17 7

Total length (em)

8 9 10 II 12 13 14 15 16 17 7 8 9 10 II

Total length (em)

ChimboteMar. '61-Feb.'62T=18.9.C

.L75=15.0":L~=14.5.L25 =14.0 :

H

Chimbote

Mar. '62 - Feb. '63T=18.5 'CL75 ~15.4L~ =14.8L25 =14.1

I

Total length (em)

ChimboteMar. '63- Feb. '64T= 19.0 'C

L75=15.1L~= 14.5L25 =13.9

J

8 9 10 II 12 13 14 15 16 17 7 B 9 10 II 12 13 14 15 16 17

Total length (em) Total length (em)

-- - ---

1.0 ....I I I ...... I I I I I I I ....f

0.9 Chimbote-Pisco Chimbote-Callao Islo don Mertin(Huaeho) ChimbateNov.1953 May 1954 .

....'.-,..;

Jon.'55 - AUQ.'570.8 T.16.8.C

T'17.9'C IT'I7.9.C T'18.9 'C. 0.7 L75=12.4 L75=15.1 L3'14.1 · L7'16.1...

::JLeo=11.1 L= 13.8 L0=12.3 L=15.1'0 0.6 .

e L25'9.8· L25=12.4 L2 =10.5 L25=13.4c 0.50U 0.40Il: 0.3

n2f /.A

j',

B / c / 00.1

I /.. I ,0

I , , .....1.. , , ...... I I I , I ....

7 8 9 10 II 12 13 10 II 12 13 14 15 10 II 12 13 14 15 7 8 9 10 II 12 13 14 15 16 17

Total lenQth (em) Totol lenQth (em) Totol lenQth (em) Total lenQth (em)

1.0

0.9

0.8. 0.7...::Ic; 0.6ec 0.5.2U 0.4aIl: 0.3

0.2

0.1

07

170

Table 1. Summary of data on anehoveta maturation as a function of length and temperature (see aUo Figs. 1and 2).

Code in Temp fC)Fig. 1 or 2

A 16.8. B 17.9

C 17~D 18.9E 16~F 15.7G 16.8H 18.9I 18.5J 19.0K 16.4L 17.2M 16.5N 17.6O. 16.1P 16.2Q 17.4R 17.3S 19.5T 1BU 17.2V 20.7W 19.9X 17.7y 17~

mean 17.7n 25s.e. 0.25

.Cold years"

Ctne<W\remo.16.84 .C; mean L5O"J4.38cm)

40 Jul-Sop 1964 f'I. 40

_: T-16.4.C 30?f!. 10 L"", 14.2~ fo~ 0 0

~;g oM-Sop 1966 L 40

~ 20 T- 17.2 "C :10 10 L50" 14.2~ 10~ 0 0

.I: :~ JuI- Sop 19672 20 T" 16.~ .C 4010 10 L,.,. 14.2~ 30U 0... 20

c:: Jul- Sop 1968 10- 20 T - 17.6 .C 0.. 10 L!IQ- 14.2~ 40o 0 ~- 40 20

~ 30 Jul- Sop 1970 10~ ~ T-16.I.C 0... 10 L!IQ" 14.2~ 40o 0 ~~ ~ 20- ~1O;g Jul-Sop 1973 0E 20 T -16.2.C

'0 10 l5Q- 13.2~ ~~o ro

c:: Jul-Sop 1974 Q 10~ 20 T. 17.4 .C 0iii 10 L!IQ- 14.2~ 60o 0 ~

E 40 Jul-Sop 197~ 40o ~ T - 17.3 .C :o 10 L!IQ. 16.2~ 10

o 0~ 10 I~

Total length (em)

TL50 (em)

Maturation

range (em)

~5-L25

Remarks

ILl13.812.315.114.514.714.214.514.815.514.25

. 14.25'14.2514.2514.2513.2514.2516.2514.2514.2512.2512.2511.2512.2512.25

2~233~23O~1~1~1~[~1.2

etlTlyyean:

mean temp = 17 .6~oC

mean L50 =13.95 emn= 10

(see Fig. 1)

coldyears:

mean temp =16.840C

mean L50 =14.38 emn =8 (see Fig. 2)

wann years:

mean temp =18.640C

mean L50 = 12.68 em

n =7 (see Fig. 2)

13.7725

0.26

.Worm yeof'-(meantemp.-IS.64-c;mecn~"68 em)

\

Jul-Sop 196~T.19.~ .C

L!IQ" 14. 2~

Jul-Sop 1969T " 17.9 .C

l5Q" 14.2~

Jul-Sop 1971T- r7.2 .CL!IQ- 12. 2~

Jul-Sop 1972T-20.7.C

L~a - 12. 2~

Jul-Sop 1976T-19.9.C

L~o" 1I.2~

Jul- Sop 1977T-17.7.CL~a- 12.2~

Jul-Sep 1978T-17.6 .CL!IQ-12.2~

~ 10

Total 1'"911'1 (em)

---

1.81100.31

T

w

Pig. 2. Relationship between two groups of est~

mates of mean length at fIrst maturity. (LSO I-'approximated by position of arrows, see text) aDd

environmental temperature. Note that L5Q valuesduring "warm years" are lower than durmg c:oJdyears. The letters K to Y refer to the rows of Table 1(adapted from Tsukayama and Alvarez 1981 andI. Tsukayama, IMARPE, pers. camm.).

171

15

L7S' 33.2 -1.046 T

LW31.1 -Q981 TL:zs'29.1 -Q917T

,.,~,i',,~,I ""f '"t ""! '~~,I ",I "": ""I '~~

(IO.C ranoa used

) I "~'.~ for modalllno ~ ~,I :I II

o15 20 25 30

Sea surfoca 'amparatura reI

Fig. 3. Model used to estimate values of L2S' LSOand L7S in anchoveta for temperaturebetween 14 and 24oC. The points refer to the means LSO values in Figs. 1 and 2 (seealso Table 1 and text).

Relative Fecundity and Spawning Frequency as aFunction of Anchoveta Size

Not all anchoveta are equal. Major differences occur in the relative fecundity of matureanchoveta as well as frequency of spawning (parrish et al. 1986). As no data on these size-specific differences are available for Peruvian anchoveta, data presented by the abovementionedauthors have been assembled and analyzed (see Table 2). These data yielded values of the factor

. Aj in equation (1) ranging from near zero for very small fish (which are likely to be immature in'any case), 1 in fish of 26 g (the mean weight of Peruvian anchoveta used by'Santander"etaL;'i.i.1984for estimatingbatch fecundityandspawningfrequency)and about6 in anchoveta.ofSQg.

(fable 3). ; "',: . .

As presented and used here, these values of the factor Aj account for the fact that larger.anchovetaspawn more frequently, have a longer spawning season and produce more eggs perspawning than smaller ones, a feature also reported for numerous fishes other than engraulids(see Parrish et al. 1986 and references therein). .

Table 2. Data on the size dependence of fecundity in northem anchovy {E. mordax}.a

a Adapted from Table 3 in Parrish et al. (1986).b Estimated relationship between relative fecundity (R.F. and body weight is R.F. :a 0.582 W2.64 (r2 =

.0.981,2 d.f.).

E

oJ!:

€:::I

100E

0.<:C.c.

5oJ

Spawning se:uon 1st 2nd 3rd 4th plus

Range of weights (g) 11.0-15.4 IS .5-18.3 18.3-22.7 20.9-26.6. Mean weight (g) 12.38 16.71 19.76 23.23Spawnings per season 5.3 11.9 19.2 23.5Eggs/g female per seasonb 2,803 6,550 11,434 13,386

172

Table 3. Multiplication factor ("A") accounting for the size-related variability of reproductive outputin Engraulis morr:Lzxfemales. a .

Meanc

weight (g)Fraction of female anchoveta

in catch samplese

4.255.256.257.258.259.25

10.2511.2512.2513.2514.2515.2516.2517.2518.2519.2520.25

0.5170.9751.652.573.785.337.269.60

12.415.719.523.928.934.641.048.156.0

0.000030.000180.000700.002260.006260.015500.035050.073290.144040.268540.475920.814351.344472.162733.385255.160657.71006

0.5000.5000.5000.5000.5000.5000.5000.5000.5150.5400.6000.7100.8350.9450,9901.0001.000

a Based on R.F. - W relationship in Table 2, footnote (bJ .b Median of length cb..sses in the anchoveta catch (see Tsukayama and Palomares, this vol.).

c EStimated through the mean relationship W =0.00674L3.d ;'he mean weight offemales in Santander et al. (1984) was 25.84 g; the relationship A =

0.000I87W2.64 generates a factor A =1 when W =25.84 g.e From Fig, 4.

The Seasonality of Anchoveta Spawning

Numerou.sau~~rs give accounts of the ~eas<?~a.LP~tternof maturation of anchoveta and itslink to spawning (see e.g., Simpson and Gil1967; Vildoso and Alegre 1969; Santander andCastillo 1969). Here, graphs showing seasonal patterns in the percentage of mature females ofanchoveta caught off Chimbote and Callao and presented by Jordan (1980) were used to relatethe monthly change in the fraction of mature fish in the stock as a whole to the fraction mature inSeptember, i.e., of the only month for which an estimate of spawning frequency is available (seeTable 4). This procedure allows scaling of every month of the year in terms of the Septemberspawning frequency, leading to an estimate of annual number of spawnings (for females of about26 g) of 24 per year. TIrisvalue is sufficienlly close to the estimate of 20 times per year innorthern anchovy (Hunter and Leong 1981) to be acceptable. The estimated mean number ofspawnings per month in Table 4 shall thus be used here as estimates of Sk in equation (1).

The Fraction ofF emale Anchoveta in the Population

Data are available from three different authors showing that the proportion of females inanchoveta catch samples increases rapidly from about ().5at 12 em (fL) to about unity near 17-18 cm (Fig. 4). Moreover the data from two of these authors (Clark 1954; Minano 1958)contradict Jordan's contention that "the sex ratio is moderately in favor of females in the smallfish" (Jordan 1980, based on Jordan 1959 and see Fig. 4). Santander et aI. (1984) show that theproportion of females in anchoveta of mean weight 26 g may range from 0.1 to 0.9. Thus, smallsamples such as will occur when fish of very small sizes are considered separately, may suggesttrends that are difficult to explain. A gradual increase of the proportion of females such assuggested by the line superimposed on the data points of Fig. 4 would be, on the other hand, very

-

a Mean for the years 1966 to 1970.b Asread ofC Fig. 3 in Jordan (1980).c As computed with reCerence to September value.dBased on Santander et al. (1984) who report that 16.04% of the Cemalessampled in September 1981 had been spawn-

ing during the previous 24 hours. (The values in this column correspond to the values of Sk in equation I, see text).e Note that 24.2 spawnings per year per female (of 26 g, see text) is close to the value of 20 estimated by Hunter and

Leong (1981) for northern anchovy (E. mordaxJ.

.,

;.

1

A Clark (I954,Tobie m). Miiiono0958,Tob.I-m)

. Jordon (1959,Fig.6)

sex ratio of.embry.os ?

. .. . ..~c~ '5 0.6- -

CIa 0 0.5. c:.c: .- .

'.S! 0 0.4'0 -;

. ~ 1) 0.3II... .t:o

5 0.2

. ..

A ...

'.."::"".. 0.1

o I 2 3 4 5 6 7 8 9 10 II 12 13 14 15 16 17 18 19 20

Total length (em)

Fig. 4. Relationshipbetween length of anchoveta catch samplesand the fraction of Cemales.With theexception of four less credible data points (dots) between 7 and 10 em, all availabledata suggestanincre:ue of femalestoward largersizes.

~y to explain, as the result of a slightly lower mortality among the females, ultimately linked~f9slight differences in growth parameters. The eye-fitted curve in Fig. 4 assumes that the seX';!a!io.of anchoveta embryos is 1:I, as shoUldbe assumed when no information is available'

. ~~ggesting otherwise (Conover and Heins 1987). The curve was used here to provide estimates~!.the mean proportion of females in the anchoveta population by length class, i.e., of thei~eter PFj in equation (I), (see also Table 3).',\' .

----

173

Table 4. Selected information on the seasonalityof spawningin Peruviananchoveta (Engraulisringens).

% mature femalesin catch % mature as Absoluteno.samples fraction of of spawning

Montha Callaob Chimboteb Mean September value per monthC

Jan 11 10 10.5 0.157 0.755Feb 15 19 17 0.254 1.222Mar 7 18 12.5 0.187 0.900Apr 2 4 3 0.045 0.217May 1 1 1 0.015 0.072Jun 9 7 8 0.119 0.573Jul 20 25 22.5 0.336 1.617Aug 53 50 51.5 0.769 3.700Sep 73 61 67 1.000 4.812dOct 74 78 76 1.134 5.457Nov 43 70 56.5 0.843 4.057Dec 12 11 11.5 0.172 0.828

-: 24.210e

1.0

0.9'"

0.8C.E

0.7CI..

174

Tire Batch Fecundity of Female Anchoveta

As mentioned above, only one estimate of batch fecundity in the Peruvian anchoveta ispresently available (Santander et al. 1984).It pertains to fish with a mean weight of 25.84 g andis of 15,401 eggs per feinale. Expressed as relative fecundity, this amounts to 596 eggslg female,similar to values for the northern anchovy, where relative batch fecundity values rangingbetween 556 and 720 have been reported (Hunter and Goldberg 1980;Lyczkowsky-Laroche andRichardson 1980)

The reader will notice that the form of equation (1) makes monthly egg output of anchovetadirectly proportional to the relative fecundity (RF) value used here. Hence, use of another valueof RF would imply a rather straightforwardrescaling of final results but no change in theappearance of any of the graphs presenting these results.

Computation of Reproductive Output

A BASIC program available on request from .theauthors was used to compute, for eachlength class (from ML =4.25 to ML =20.25 cm) and every month (from January 1953 toDecember 1982) multiplicators which were subsequently applied to the biomasses by lengthclasses in Pauly, Palomares and Gayanilo (this vo1.)to give estimates of egg production.

Results and Discussion

Fig. 5 shows the total biomass (from Pauly, Palomares and Gayanilo, this vo1.),spawningbiomass (females and males) and mature female biomass, for every month from January 1953 toDecember 1982 (see also Tables 5 and 6). All of these display strong seasonal and interannualoscillations, reflective of spawninglrecruitrnent seasonality and of major events such as the1971/1972 collapse of the fishery.

Year

Fig. 5. Total biom:us, parent (mature) stock and biomass of mature anchoveta females off Peru, 4-14°S, 1953 to1982. Note strong, regular seasonal oscillations and aOO very good match with independent spawning stocli:estimate in August-September 1981 by Santander et aL (1984).

---

22 r- I - TOlolanchovelabiomass

Malure males20 I- I I and females

lal- II. /I I \ I I . MaTure females

I!I SpawninQ srock eslimaTebased on Ihe .egg

16 r I V\ M\ I rA\ I

production method.N

14-'"Q

12)(--.. 10..cE0 aCD

6

4

2

0

On the other hand, our estimate of spawning stock size for August/September 1981 of 1.14 tx 106, is extremely close to the independent estimate of 1.2 t x 106 (with 95% conf. interval =S~.8%) obtained by Santander et al. (1984) for the area between 4 and 140S (see Table 5,footnote [a] and Fig. 5). TIrisextremely good match between two estimates that were obtained.~ on completely independent data sets. assumptions and models is extremely encouraging..~ l~suggests that our approach for estimating past spawning stock size may be realistic.

175

Table 5. E"im1l<d biomass or ma.ure re:na1..nd nuJ..ncho....(EnvouIlHinf'nr) ocr Peru (4.14.S), 1953 '0 1981 (in .onnesl.

Dal. Jan Fob Mar Apr May Jun Jul Alii Sop Oct SOY Dee

1953 1.101,937 2,231,080 3,317 ,855 2,955,131 1,115,232 887,920 802.925 481,772 432,953 299,084 355.906 547.272

1954 1,114,237 l.362,158 1,669,903 900,324 663,342 393,733 633,657 245.535 270.727 278,579 465.742 1,830,94

1955 3,818,367 2,990,407 1,640.273 2,312,623 1.269,131 1,214,193 1.084,533 718.045 741,423 514,055 677,972 1,008,368

1956 2,022,882 3,436,052 3,811.1S7 2,769,103 2,261.131 1.904,923 1,665.332 1.227.079 851,891 674,239 703.180 576.115

1957 934,906 1,953,957 1,958,200 1,923,840 1,935,852 1,626.589 1,226,208 708,169 357,478 382,458 359,280 823,295

1958 1.033.769 1,397,276 1,526,377 646,861 523.424 366,572 360,117 145.397 1.659,263 1,632.507 1,769.059 1,505,579

1959 1,937,039 3.167,238 3.002,390 2.641.178 1,964.495 1,563,931 1,176,471 979,052 741.835 863,5 18 996,828 1,335.4.47

1960 1,398.188 1,893,285 1.941,318 1,393,424 1.006.903 1.082,592 897,994 1.025,889 914,385 854,318 847.712 1.649.447

1961 3,185,292 6.091.497 4,624,528 4,260,150 3,700,503 2,324.159 1,610.900 1,582,807 1.485.906 '1,517,057 1.415.162 1,648,559

1962 4,986,926 5,524.700 4,304,486 3,326,390 3,785,605 2,644,778 2,128,486 1,959,337 2,227,742 1,522,194 1,810.225 1,596,590

1963 1,855.765 3,009.503 4.083.481 2,197,470 2,985,038 1,479,294 1,796.051 1.470,197 1.397,778 1,275.029 1,281,386 2.085,961

1964 2,995.569 4,135.050 4,803,659 2.160.991 1,159,568 880.377 810.130 1,186,305 1.301,322 1.545.419 1,731.584 1.470,287

1965 2,579,329 3,678,943 4,245,975 4,775,363 3,838,356 2,391.526 1.960,683 1.594,674 1,080.843 1,276,406 1,856,835 2.195.117

1966 4,277,278 6,773,214 5,067.000 3,856,401 3,577 ,115 2,406,994 2.l96,815 2,1S9.686 1.529,259 2,243,032 2,300,820 2.664,493

1967 3.624,301 3,916,894 4,397,793 2.429,393 1,770,207 1,473,478 1.573.797 1.128.436 1.252.839 1.098.865 1,127,815 2.514,322

1968 3,438,439 3.015,294 5.082,356 2.601,436 2,404,957 1,489,790 2.086.114 2.510.095 3.021.141 2,045,513 1.979,449 1.654.563

1969 1,614,892 1,749,620 4,587,486 4,943,181 5,772,725 3.090.998 1,401,138 1.527,544 1,576,925 1,477,807 1,451,568 2.003.091

1910 4,269,720 7.065,151 9,532.422 7,719,537 6,643,855 5.061,111 3,669,402 3,966,850 4,102.173 3,638.361 2,242.982 1,665.952

1911 1,154,127 3,895,876 1.126,115 7.635,624 5,552.118 4,607,634 5,871.848 6,468,841 5,120.592 3,911,640 4,331,058 3,814,441

1972 4.080,428 4,733,777 4,950,483 2.461,541 904,159 695,461 591,351 468.269 305.053 377.667 546,811 1,924,012

1973 2,390,139 2381,910 3,289,321 1.069,764 491.190 443.296 408,980 311.737 444.619 693,043 1.173.970 1.068,288

1914 1,494,7.18 2,287,D48 3.080.939 2,881.127 1,932,834 1,721.473 1,506,453 1,365.201 1.356,463 1,379,513 1.1S1,494 642.609

1915 947,723 1.804,664 2,611.611 2,238,619 1,414,223 520,599 518.336 439.006 770.811 760.153 623,191 804,357

1976 861,315 1,831348 2.796,199 1.613,161 2.955,161 2.780.036 2.030.119 1.990.957 1,120,121 1.142.474 1,231.079 1.211.618

1917 685,150 689,810 711,919 659,494 231.035 63,979 47,870 33,868 24.036 21.408 29.775 57,493

1978 79.513 379,191 710.600 669,427 356,495 180.114 235,518 198,581 238.450 334,968 509,D41 629,390

1979 911,162 1.074,841 1,276380 900,820 290,680 208,938 212,094 196,876 155,692 127.843 79,159 114,943

1980 149,524 223,371 362,472 280,497 312,954 181,906 158,261 114,113 104,313 108,903 138.160 273.256

1981 212.684 132,513 1.035.224 1,390338 2,104,529 1,513,989 1,213.016 1,302.127' 967,981' 1.548,488 1.527,565 1,938,022

" "ne mean or tho va1u.s ror Au&U"and S.ptemb.r 1981 is 1.302.727 + 967,981(2 . 1.135,354 . or roushlY 1.14 . x 10'. .r:ry close '0 th. ;;;;s.-pond.n....im... or 1.2 tx 10'or SutbDdor .. al. (1984).

"

'J.

;-Table 6. Esim..od biomass or m..un remal. uadto..u (EiHinl'fU) orr P.ru (4.14.S). 1953 10 1981 ,in ,0Mes).y..

Oat. Ian Fob Mar Apr M.y Jun Jul Alii Sop Oct Noy Dee.,

1953 615,827 1.195,172 1,746,176 1.579,691 952,366 528,122 483,260 298,056 255,258 116,814 210,933 319,2161954 619,042 1.019,209 936.109 532,104 398,314 243,341 390,367 153,989 168,490 174,619 293,512 1,106,9431955 2,102,940 1,125.540 1,015325 1,395,691 839,801 823,599 743.283 506,431 492,227 349,381 453,805 652.1631956 1,204,884 1387,935 2,239,360 1,688,618 1,437.081 1,247,581 1.114,805 850,116 590,174 4f6,461 514,749 429,6101957 659,363 1.175.588 1,180,478 1,166,533 1,125.296 911,329 758.680 483,311 233.449 216.108 233,716 411.7231958 556,477 740,904 802.036 347,326 293,339 210,726 207,139 88,171 1.202.768 1,!89,938 1.288,487 1.139,2981959 1.298,637 1,944,351 1,89O,D45 1.732.905 1,312,675 1,102,878 869,291 738,760 518,156 608,704 702,702 885.9481960 897,964 1,156,378 1,216,551 936,361 688.785 730,515 627.003 707,929 610,415 566,382 550.639 1.010,3061961 1.803,530 3,306,876 2,582,563 2,432,481 2.154,049 1,408,025 1,004,056 995,503 946.035 911,338 900,793 1.022.9461962 2,865,660 3,168,473 2,574,768 2.058.058 2,341.634 1,686,657 1,392.822 1,310.750 1.492337 1.048.169 1,231,766 1.080,9191963 1.180,530 1,779,473 2,364 ,620 1,689,052 1,777.134 885,558 1,070,337 885.941 845,779 779,355 790,169 1,226.490

--1

1964 1,662,957 2,231,810 2,617.670 1,298.227 699,003 548,477 518,564 767,702 853,077 1.024,011 1.150,214 978,3961965 1.650,085 2,214,192 2,507.260 2,653.662 2,100,665 1,313.116 1,070,955 891,108 624,621 747,579 1.080.974 .1,584,0041966 2,295,652 3,565,841 2.744.425 2,177.035 2,111,526 1.491,288 1,411,529 1,427.034 1.D44,861 1,549,580 1.609,084 1,896.141..... t967 2,436,599 2,334.488 2,614,873 1.498,499 1.078,631 917,369 998,251 741.759 837,119 ".752.685 . "78i,682 1.715.421

: 1968 . 2,222,367 1,923.715 3,D93,793 1,743,305 1,617,222 1.048,551 1,486.107 1.803,690 2.177,900 1,507,961 1.452.011 1.185,8301969 .: 1,055,306 1.016.052 2,509,428 2,716,689 3,115,582 1,729,460 857.072 953,507 1.001.667 . 940,335, .. 930,858 1,233,50;41970 . 2,409,218 3,933.168 5,357,801 4,570,454 4,132,194 3,356.075 2,596,775 2,865,352 3,021,776 2,648.402 ',647,051 1.189,665

_ 1971 1,131,605 2,302,287 4.058,420 4,227,804 3,224,927 2,776,311 3,616.858 4.067,276 3,359,786 2,741,999 3,D04,173 2,663,0191972 2,735,506 3,289,209 3,602,592 1.790,756 554,684 394,682 329,180 269,242 195,745 232,479 320,698 1,036.3421973 1.257,987 1.601.170 1,825,469 647,634 309,359 295,932 285.064 268,286 324,868 508,249 853,686 820,983

.1974 1,155,108 1,731,812 2,340,212 2,175,286 1.425,581 1,266,740 1.188,521 1.124,136 1,150.822 1.192,959 947.942 515.2981975 732.287 1.254,699 1.746.167 1,575,113 1.015 ,652 385,496 394,168 348.143 614,395 619.606 521.352 667.123

. 1976 700,702 1,147,345 1,634,760 995.073 1,724,294 1.600.457 1,186.017 1,191,105 727,369 746.791 815.008 741,7951977 392.412 380,355 410,443 402.287 152,140 43,395 33.726 24,341 17,233 14,480 18.082 33,7711978 45,800 200,144 375,241 363,658 206,234 108,776 144,651 127,302 152,809 217.194 330,686 410,9971919 550,627 673,443 818.801 587,381 182,D48 141,044 145,140 139,119 114,046 93,754 55,598 65,8791980 85,702 129,989 210,861 169,394 199.410 114,365 100,586 76,519 70,606 74,298 92.702 173,8421981 129,919 418,334 600,842 821,279 1,240.078 933,408 783,706 856,102 663,872 1,046;769 1,058.028 1,374.739

176

Tsukayama and Alvarez (1981) reported a range of 0.067 to 0.244 and an overall mean of0.133 for the ratio of spawning stock to total anehoveta biomass, for the period 1964 to 1978.Our results (Fig. 6), expressed on a fmer temporal scale than those of Tsukayama and Alvarez(1981) not only have a greater range, but a higher overall mean of 0.254, due to our differentdefinition of mature biot;naSs(Tsukayama and Alvarez 1981 defined this as "the biomass of allfish> 14 em"; our definition is "Bij.Pij", see equation 1).

Fig. 7 presents our estimates of monthly anchoveta egg production, from January 1953 toDecember 1981 (1982 was excluded because the VPA ill estimates of anchoveta biomasses forthe last year of the series are questionable, see Pauly, Palomares and Gayanilo, this vo1.).Asmight be seen, monthly egg production had, during the period covered, several peaks, notably in1968, 1970, 1971 and 1974. However, these peaks of egg production did not lead to peak

1.0monthly values12 mont".runnin9 means--- overall meon(i.O.2~)

0.9

0.8. ::"

E.S!.0<5(;,...~cocC~"a.

en 0.2 ~ ~\I, WI U ~ \I t\1'pj)9\JLn~jVIWJi/ ~ ~ ~ V L i1 V! ~

O.I~d~V ,VVU ~VV Q U ~j V'0'" . . . . . . . , , . . . , , . . , . , . , . , . . , . . . ,

1953 ~ !iT 59 61 63 ~ 67 69 71 73 75 77 79 81

Year

Fig. 6. Relationship between spawning stock and total

biomass of Peruvian anchoveta.. 195.3_~0 1981. Notestrong oscillations, with two peaks per year. corres-ponding to the main (September-November) and the .lesser (February-April) spawning seasons.

Fig. 7. Total monthly egg output by Peruviananchoveta (4-14°S), 1953 to 1981. Above: 12months running average to cnIphasize interycarvariability. Below: monthly values, to illustrateexistence of two spawning seasons, September-November and February-April, of which theformer leads to higher production. The drawingof eggs added to this graph are UOffi Santanderand Castillo (1973) and illustrate an initial. anintermediate and an advanced stage, respectively.

...:

7

rear

- - -

. Albeit et al. (1983, Table 1, Figs. 1-4)presented data on the size-dependence of batchI fecundity of E. ringens, based on fish samples from January 1970 to September 1981. AlthoughJ . theanalysispresentedby theseauthorsi~somewhatconfused,the keyresultdoesemergethatl:~argeranchoveta have higher batch fecundities than small ones. However, we could not use anyL of theregressionlinesexpressingthisrela~o!1ship,becauselargeengraulidfemalesnot onlyi. ~ave higher batch fecun~ties, ~ut also Spa..ynmore often than ~mallerones. This is the reason( why we have used a relatlonship between SIZeand egg productlon based on data for E. mordax~ (see Table 2); Fig. 4 in Albeit et al. (1983) shows that E. ringens and E. mordax are similarr_~~ough,at least as far .~~_~~ir batch fecundi~ ~ concerned, to jus~fy o~ a'pp'~o~ch.f~'~~.;.Temporal changes m anchoveta fecundity may be expected, gIven die denSIty-dependentL:.£hangesin growth and related parameters discussed in Palomares et al., this vol.). However,'~;~Iicreteevidence for such changes is scanty. .

f.tr':~'r:Wareand Tsukayama (1981) write that "in the winter of 1962, the anchovy population wasrp~~~.order of 24 t x106. According to Miiiano (1968, Fig. 5), the gonad weight of a 21-gr~chovy at that time averaged 1.1 g. By 1974, the stock declined to 4.5 t x 106 and the~~~nding gonad weight of a 21-g anchovy was 1.7 g. This fmding clearly contradicts the~.JOng'standing assumption of classical theory that fecundity of marine fish is not affected by;;"fl1!~tions in population size (Hanis 1975)."~J~' Albeit et al. (1983), commenting on ~eir fecundity estimates suggested similarly that "thet~y remarkable feature is the difference between the relatively low values for the seventies and~~e.high values from 1981". They also noted that "obviously, the fecundity values from thej,~~thern Peruvian anchovy stock are higher than in the centtal and northern stock batchi!~dity increases with increasing latitude".~

_T'''' .'.". ..

.:w:~_ .~.'." .

177

recruitment In fact, the annual season of peak egg production (September-November) is usuallynot followed, a few months later, by a recruitment peak. Rather, it is the minor egg productionpeak occurrin in February to pril which usually leads to massive recruitment (see Mendelsohnand Mendo, thISvo1.;Pauly, this vo1.).

Assessing the overall reliability of the egg production estimates in Fig. 7 and Table 7 isdifficult. Assuming $at the biomass estimates used here were reasonable, we think that theweakest point in our analysis are:

i) lack of data on size-specific egg production in E. ringens, andii) lack of readily quantifiable evidence on temporal changes in the fecundity of anchoveta.

tabl.1. Eslim..ed monthly," ou.put by .ho aneho.o.. Slockorr Peru (4.14')/), 195310 1982 in billions (10').

Year ]an Fob !ofu Apr May ]on ]ul Aue Sop Oct Noy Dee

1953 65,661 162.924 143,223 39,231 10.315 62.991 111,452 214,100 221,913 190,765 169.988 41,987

1954 65,63 I 161.086 135,885 23,885 6.198 33,196 148,440 149.104 182,401 211.144 228.999 140.146

1955 192.594 240.819 115,6\8 43,099 11,391 \80,024 419,611 826,324 118,989 108,193 640,9 IS 110,'18

1956 \85,661 45 \,958 315.879 84,843 22,344 114,638 491,583 1,004,831 829,386 1,061,622 935.160 I 72,8001951 204,811 382,666 309,286 84,519 21,132 119,258 419.960 918,112 393.580 460.125 361,908 94,9401958 54,819 106.952 86,201 13,090 4,919 34,385 93,898 139,860 2,482,968 2.960.861 2.553.911 554,4061959 352.261 121,599 624,069 166,804 41,560 336.522 880,939 1,852.922 1,123.983 1,318,462 1,084.233 257.:"91960 194,393 384.033 417,941 100,548 24,580 198,923 556,461 1,445,520 1,328,413 1.402,991 911,491 210,5511961 265,612 511,954 350,565 89,147 28,205 161,973 341,365 790,464 943,793 1,127.001 743.430 160,5771962 369,270 673,979 447.320 88.255 33,125 210,403 541.311 1.332.815 2.003,316 1,798.188 1,480,403 266.0111963 215,052 450,209 395.373 76,407 24.766 104.455 340.737 677,512 807.5 3\ 861,704 633.174 178.5271964 \85.516 345,n8 323,110 46.753 10,022 68,209 193,212 681.985 951,820 1,328,338 1,124,598 193.8201965 281.012 496,123 374,679 71.605 18,473 105,038 248,51\ 535,486 556,161 767.545 821,748 2:2.1611966 211,101 444,150 336.152 83,111 30,041 112,146 461,883 1,186,560 1.340.525 2.535,393 2,032.511 505.6101967 527,859 592,172 542,334 95,179 20.401 130,624 412.685 825,421 1,214,606 1.367.367 1.060,139 400.3931968 355,580 519.640 639.489 127,538 39,366 253.279 1,019,190 2,832,135 4,39 L.395 3,773.991 2,609.660 354.2491969 250,636 272.443 311,636 101,184 30,764 168,017 315.9'8 814.015 1.117,203 1,185.641 915.506 23<&03.&7

r 1970 299,953 738,752 827.515 212.524 11,546 574.098 1,624.611 4.518,802 6,767,713 6.487,205 3,309.029 478.1731971 327,886 815,886 879,106 166.311 52,.56 381.554 1,383,763 3.781.583 4,593.975 5,193.788 4,23\,701 781.1741972 591,728 1,476.866 1,576.613 201.265 12.865 60,192 136,170 315.314 490,235 551.012 423.117 140.356

, 1973 98.994 248,777 270,108 32,774 5,897 60.655 203.664 510.825 769,852 1.304.407 1,528,727 403.0H1974 562.590 1.464,.95 1.6\8.032 312.631 69,119 517,784 1,611,192 4,155.449 6,004.290 1.610,760 3,774.9'9 4:6..59-'1915 496,852 926.545 811,.228 193.338 41,250 124,851 396,629 973,372 2.301,755 2,916,507 2,0'1,944 520.5791976 485.582 678,107 556,313 105,273 39,677 242,818 .82,420 1,170.903 1,169,387 1.293.856 1.056,285 162.5161911 58,380 70,885 70.325 19,859 2.877 9,'8} 25,432 48.306 47.870 39,427 21,388 6,6301978 5.154 25,332 38,220 11,586 2,988 14,639 57,307 136.089 200.618 340,920 373.673 98.5651979 92,5 II 208,889 216,418 40,457 4,053 30,931 86.501 226,553 281.842 212.974 130,618 10,9821980 13,015 30,723 31,614 8,492 4,315 18.812 47.003 91,868 120.321 1';],237 154,013 50,2951981 22,550 90.111 113,924 42.434 19,706 129,853 369.512 1.029,983 1,222,403 2.014,030 1.707,866 516,859

178

Combining the temporal and the latitudinal trends mentioned above leads to the conclusionthat the Peruvian anchoveta may be undergoing, with respect to its fecundity, the same processof IIsouthernization"that is apparent with regard to its growth (see Palomares et al., this vo1.).

We have not accounted for "southernization" when deriving our estimates of egg productionfor the period January 1953 to December 1981. Explicit consideration of this process wouldobviously have improved our estimates and this should be taken into account in future analyses.

References

Albeit. 1.,B. Alegre, V.H. Alarcon and B. Macewicz. 1983. Batch fecundity and spawning frequency ofvarious anchovy (genus:Engraulis) populations from upwelling areas and their use for spawning biomass estimates.,p. 977-985. In G.D. Sharpand J. Csirlce(eels.)Proceedings of the Expert Consultati.onto Examine Changes in AbuncLmceand SpeciesComposition of Neritic Fish Species, San Jose. Costa Rica, 18-29 April 1983. FAO Fish Rep. No. 291 Vol 3.

Clark, F.N. 1954: Biologia de la anchoveta.Bol. CienL Cia. Admin. Guano 1(1):98-132.Conover, D.O. and S.W. Heins. 1987. Adaptive variation in environmental and genetic sex determination in a fish. Nab.1re

326:496-498.Einar.;son, H...~AFlores and.J. Minano. 1966. E1cicIo de madurez de la anchovetaperuana (Engraulis ringens 1.).p. 128-135.In

. I Seminario Latinoameri<;anosobre el Oceano Pacifico Oriental, Univ. Nacional Mayor San Marcos Lima, Peru.Harris, J. 1975. The effect of density-<iependentmonality on the shape of stock-recruitment curves. 1.Cons. Int. Explor. Mer

36:144-149.Hunter, J.R. and SR. Goldberg. 1980. Spawning incidence and batch fecundity in nonhe:m anchovy, Engraulis mordax. U.S.

Fish. Bull. 77:641-652.Hunter, J.R. and R. Leong. 1981. The spawning energetics of female nonhem anchovy, Engraulis morda:J:.U.S. Fish. Bull

79:215-230.Ingles, J. and D. P:.uly:'1984. An atlas of the growth. mortality and recruitment of Philippine fishes. ICLARM Tech. Rep. No. 13,

Manila, 127 p.Jordan.,R. 1959. Observaciones sobre la biologia de la anchoveta (Engraulis ringens 1.) de la zona Pesquera de Huacho. BoL

CienL Cia. Admin. Guano 35(11):3-22 + app.Jordan, R. 1980. Biology of the anchoveta. I: Summary of the present knowledge, p. 249-276. In Proceedings of the Workshop

on the Phenomenon known as 'El Nino', Guyaquil, Ecuador, 4-12 December 1974. United Nations Educational,Scientific and CultUralOrganization. Paris, 284 p.

Lyczkowsky-Laroche, 1.L and S.L Richardson. 1980. Reproduction of nonhem anchovy, Engraulis mordax, off Oregon andWashington. U.S. Fish. Bull. 78:603-618.

MUiano,J. 1958. Algunas apreciaciones relacionadas con la anchovetaperuana y su fecundidad. Bol. CienL Cia. Admin. Guano34:11-24.

Mii'lano,J. 1968. Estudio de la fecundidad y cicIo sexual de la anchoveta (Engraulis ringens 1.) en la zona de Chimbote. BolInst. Mar. Peni-Callao 1(9):507-533.

Panish, R.H., D.L. Mallicoate and R.A. Klingbeil. 1986. Age dependent fecundity, number of spawnings per year, sex ratio, andmaturation stages in nonhem anchovy, Engraulis morda:r.U.S. FISh.Bull. 84:503-517.

Santander, H. and O. Sandoval de Castillo. 1969. El desove de la anchoveta (Engraulisringens J.) en los periodos reproductivosde 1961 a 1968. SereInforme Esp. InsL Mar Peni-Callao 40:1-6.

Santander, H. and O. Sandoval de Castillo. 1973. Estudio sobre las primeras etapas de vida de la anchoveta. Informe Inst. MarPeni-Callao (41)1:28.

Santander, H., 1. Albeit and P.E. Smith. 1984. Estimacion de la biomasa de la poblacion desovante de anchoveta PeruanaEngraulis ringens en 1981 por aplicacion del "metodo de produccion de huevos". Bo1.Inst. Mar. Peni-Callao 8(6):213-250.

Simpson, J. and E. Gil. 1967. Maduracion y desove de]a anchoveta (Engraulis ringens J.) en Chile.-BoLCient. InsL Fom.Pesquero, Santiago, Chile 4:1-21.

Tsukayama, 1. and M.A. Alvarez. 1981. Fluctuaciones en el stock de anchovetas desovantes durante las temporadas reproductivasde primavera 1964-1978, p. 50-54. In L.M. Dickie and J.E. Valdivia (eds.) Investigacion cooperativa de la anchovetaofsu ecosistema -ICANE -entre Peru y Canada. Insl Mar. Perii-CaJlao. Volumen Extraordinario. 288 p. (a preliminaIyversion of this paper, with a longer English abstract than in the final version may be found in IOC Workshop Rep.(28):233-240)

Vildoso, A.C. and B. Alegre. 1969. La madurez sexual de la anchoveta (Engraulis ringens 1.) en los periodos reproductivos1961/1968. Bo1. Inst. Mar. Perii-Callao 2(3):112-125.

Ware, D.M. and I. Tsukayama. 1981. A possible recruitment model for the Peruvian anchovy, p. 55-61. In L.M. Dickie and J.E.Valdivia (eds.) Investigacion coope:rativa de la anchoveta y su ecosistema -ICANE -entre Peru y Canada. Inst. Mar.Pen1-Callao. Volumen Extraordinario. 288 p.

"oJ

- - - -