Estimation of annual fecundity in indeterminate spawners
Based on: C. Nunes, A. Silva, V. Marques, K. Ganias. Integrating fish size, condition,
and population demography in the estimation of Atlantic sardine annual fecundity.
Ciencias Marinas (in pressb).
The annual (population) fecundity is the total number of eggs produced by female (or
by the population) in one year’s breeding season (Murua et al. 2003). Depending on the
fish reproductive strategy, the methodology to be adopted differs. For batch spawners
with determinate fecundity (e.g., cod, herring, plaice, etc…), fecundity is fixed prior to
the onset of spawning and thus annual fecundity (or total egg production, TEP) can be
estimated from potential fecundity (the ovarian standing stock of advanced yolked
oocytes) corrected for atretic losses (Hunter et al. 1992). For batch spawners with
indeterminate fecundity (sardine, anchovy, hake, etc…), potential fecundity is not fixed
prior to the beginning of the spawning season as oocytes carry on recruiting during the
spawning season. Consequently, annual fecundity can only be calculated taking into
account the number of oocytes released by female at each spawning event (batch
fecundity), the number of spawning events taking place during the spawning season
(derived from the spawning fraction), the duration of the spawning season and the
number of mature females (Hunter et al. 1985, Murua et al. 2003).
Sampling strategy and data acquisition
For determinate spawners, unbiased estimates of fecundity have to be obtained from
pre-spawning ovaries, not too early before all oocytes have recruited into the annual
advanced stock to be spawned, and not too late when oocyte batches have already been
ovulated (Figure 1). Additionally, samples are collected later during the spawning
season in order to monitor the incidence and intensity of atresia, to be then discounted
from the potential fecundity (Witthames and Greer Walker 1995, Kraus et al. 2008,
Kennedy et al. 2009. On the contrary, in indeterminate spawners, the sampling strategy
to be adopted is distinct (Figure 1).
The duration of the spawning season (n) is determined by regular sampling over the
year, e.g. from the commercial fleet, and estimation of the variation of the proportion of
reproductively active females in the samples collected. This activity can be assessed by
means of histological analysis of the ovaries sampled (Macchi et al. 2004, Mehault et al.
2010), or in case this is not possible, from the macroscopic maturity stage of the ovaries
(Parrish et al. 1986), or from the gonadosomatic index (GSI: ratio of the gonad weight
over the female weight) (Claramunt et al. 1994, Roumillat and Brouwer 2004). The use
of the GSI can be previously validated by establishing a relationship between the GSI
and the gonad activity (assessed histologically): a logistic curve is fitted, a GSI50 (i.e.
the value of GSI for which 50% of the females are reproductively active) is identified,
and the latter is then applied to the individual GSI data from the samples collected to
estimate the proportion of reproductively active females (Ganias et al. 2007).
Commonly, individual batch fecundity (F) is measured by the gravimetric method
applied to the hydrated oocytes in ovaries with no signs of recent spawning (post-
ovulatory follicles, POFs) (Hunter et al. 1985). In species where the oocyte spawning
batch is already clearly distinguishable (in size and shape) from the subsequent batches
at an earlier oocyte stage (e.g., migratory nucleus), the gravimetric method can also be
applied to these non-hydrated ovaries (Witthames et al. 2009, Ganias et al. 2010).
Important advances in recent years using automatic particle counting, stereology and the
development of the autodiametric method (Thorsen and Kjesbu 2001, Kurita and
Kjesbu 2009, Aragon et al. 2010) have considerably facilitated the acquisition of
fecundity data. The latter are then modelled against length or weight, the sampling of
females for fecundity estimations should thus cover a wide range of fish sizes in order
to obtain significant fecundity-length or fecundity-weight relationships (Figure 2).
Spawning fraction (S), i.e. the daily fraction of spawning females, is in indeterminate
spawners commonly estimated by means of the POF (Hunter and Macewicz 1985). This
parameter is the most complex to obtain, as it requires the collection of a significant
number of samples (Picquelle 1985) and an accurate knowledge of POF degeneration
and unbiased POF staging/ageing system (Ganias et al. 2007, Uriarte et al. in press).
Bias in this parameter estimation may also exist due to particular fish behaviours (as,
e.g., segregation of spawning schools: Alheit et al. 1984, Picquelle and Stauffer 1985,
Ganias 2008), and thus the selection of fishing gear and sampling timing of the day are
important decisive factors in order to obtain population good representative samples.
Similarly to batch fecundity, S estimates can also be modelled against female size.
The parameters described previously are to be obtained by fish length - and thus the
sampling is recommended to be length-stratified. Both the duration of the spawning
season (n), the batch fecundity (F) and the spawning fraction (S) are known to be size-
dependent (Parrish et al. 1986, Macchi et al. 2004, Silva et al. 2006, Claramunt et al.
2007), and these should then be amplified to the population abundances by length to
obtain the annual population fecundity. Batch fecundity and spawning fraction are
known as well to vary during the spawning season (Zwolinski et al 2001, Claramunt et
al. 2007, Korta et al. 2010): accordingly, it is recommended to collect samples regularly
along the spawning period to assess the seasonal variation of these parameters (Figure
1) so as to correctly integrate the production of eggs over the entire spawning period.
In indeterminate batch spawners, the incidence of oocyte atresia is usually low during
the spawning season, and becomes important only at the cessation of spawning, with the
reabsorption of the oocyte surplus production (Hunter and Macewicz 1985, Ganias et al.
2003, Nunes et al. in pressa). Atresia is thus not directly used in the calculation of
annual fecundity in those species. However, females with highly atretic ovaries
(assessed histologically) sampled during the main spawning season but clearly in post-
spawning stage, should not contribute to the annual fecundity.
The number of mature females (Nm) is obtained from data of population abundances
(numbers of individuals at length) and biological information (maturity stage, sex ratio),
available from scientific surveys and/or resulting from assessment models (e.g., ICES
2010). In case population abundances are available by age, the reproductive parameters
(n, F, S) by length can be converted to age using age-length keys (Mehault et al. 2010).
Annual population fecundity estimation
The annual population fecundity (APF) is calculated as follows:
where Pd is the population daily egg production, n is the duration of the spawning
season (in days) and Isp is the inter-spawning interval (i.e., the time elapsed between
two consecutive spawning events). Isp corresponds to the inverse of the spawning
fraction (S), so the expression used is:
APF Pd n S .
The population daily egg production (Pd) is estimated as follows, assuming that 100%
of the mature females are spawning every day:
Pd Fb, l Nm, l
where Fb,l are the individual batch fecundities per length (predicted from the batch
fecundity model and using mean weight at length data) and Nm,l the number of mature
females per length class within the sampled population, calculated as:
Nm, l Nt , l Sr, l Pm.l ,
where Nt,l is the total numbers of fish per length class in the sampled population
(available from population abundances data), Sr,l the sex ratio for each length class, and
Pm.l the percentage of mature females (assessed macroscopically from the ovaries
appearance) for each length class.
The resulting APF estimated for indeterminate spawners can present geographical and
inter-annual variability, in part due to spatial and temporal fluctuations in female’s
individual productivity (annual fecundity, Macchi et al. 2004, Nunes et al. in pressb) and
in part due to the demographic abundance and age/size composition (Parrish et al. 1986,
Mehault et al. 2010) (Figure 3).
Number of oocytes in the ovary
Number of oocytes in the ovary
Sampling for duration of spawning season
Sampling for fecundity
Sampling for fecundity and spawning fraction
Sampling for atresia
Sampling for spawning fraction
Figure 1: General sampling scheme to estimate annual population fecundity in species
a) with determinate fecundity and b) with indeterminate fecundity. Shaded area
represents the main spawning season of the species. The seasonal variation of the
number of oocytes in the fish the ovary was adapted from a) Kjesbu et al. 2009 and b)
20 40 60 80
Female gutted weight (g)
Figure 2: Plot of the observed and model-predicted values of Sardina pilchardus
individual batch fecundity (number of oocytes per female) against gutted weight (in g)
for the southern Atlantic Iberian coast at the peak spawning time in 2002 (, green),
2005 (, blue), and 2008 (, red). Full or dashed lines: model-predicted curves; dotted
lines: ± two standard errors (From Nunes et al. in pressb).
300 a 40 Egg prod. per b
APF (x10 ) mat. fem.
4th 1st 4th 1st 4th 1st 4th 1st 4th 1st 4th 1st
2001/02 2004/05 2007/08 2001/02 2004/05 2007/08
Figure 3: Estimations of a) the annual population fecundity and b) the annual female
fecundity for Sardina pilchardus off the southern Atlantic Iberian coast for each half of
the 2001/2002, 2004/2005 and 2007/2008 spawning seasons (corresponding,
respectively, to the 4th quarter of one year and the 1st quarter of the following year) and
for each group of fish length (, length < 16 cm; , 16 ≥ length > 19 cm; ,19 ≥
length > 22 cm; , length ≥ 22 cm) (From Nunes et al. in pressb).
Alheit et al. 1984
Aragon et al. 2010
Claramunt et al. 1994
Claramunt et al. 2007
Ganias et al. 2003
Ganias et al. 2007
Ganias et al. 2010
Hunter and Macewicz 1985
Hunter et al. 1985
Hunter et al. 1992
Kennedy et al. 2009
Korta et al. 2010
Kraus et al. 2008
Kurita and Kjesbu 2009
Macchi et al. 2004
Mehault et al. 2010
Murua et al. 2003
Nunes et al. in pressa
Nunes et al. in pressb
Parrish et al. 1986
Picquelle and Stauffer 1985
Roumillat and Brouwer 2004
Silva et al. 2006
Thorsen and Kjesbu 2001
Uriarte et al. in press
Witthames and Greer Walker 1995
Witthames et al. 2009
Zwolinski et al 2001