ICES Journal of Marine Science (2021), 78(8), 2684–2699. https://doi.org/10.

1093/icesjms/fsab161

Original Article
A novel approach for estimating growth and mortality of fish

Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022

larvae
,*  , 
Charles Hinchliffe , Pierre Pepin , Iain M. Suthers , and Daniel S. Falster

1
Evolution and Ecology Research Centre and School of Biological, Earth, and Environmental Sciences, University of New South Wales, Sydney, NSW,
2052, Australia
2
Northwest Atlantic Fisheries Centre, Fisheries and Oceans Canada, 80 East White Hills, P.O. Box 5667, St. John’s, NL A1C 5X1, Canada
3
Sydney Institute of Marine Science, Chowder Bay Road, Mosman, NSW 2088, Australia
∗
Corresponding author: e-mail: c.hinchliffe@unsw.edu.au
Hinchliffe, C., Pepin, P., Suthers, I. M., and Falster, D. S. A novel approach for estimating growth and mortality of fish larvae. – ICES Journal of
Marine Science, : –.
Received  March ; revised  August ; accepted  August ; advance access publication  September .

Accurate estimates of growth and mortality are needed to understand drivers of production and cohort success. Existing methods for estimating
mortality rates, such as catch-curves, require large sample sizes, as they work by grouping individuals into age-bins to determine a frequency
distribution. Yet, sampling enough larvae is often not possible at fine scales within the constraints of research projects, due to low density of
larvae in pelagic environments. Here, we develop a novel method to simultaneously estimate growth and mortality rates of fish larvae as a
continuous function of size using theory of size-structured populations, eliminating the need to group data into age-bins. We compare the
effectiveness of our model to existing methods by generating data from a known distribution. This comparison demonstrates that while all
models recover correct parameter values under ideal circumstances, our new method performs better than existing methods when sample sizes
are low. Additionally, our method can accommodate non-linear growth and mortality functions, while also allowing growth and mortality to vary
as functions of environmental co-variates. This increased accuracy and flexibility of our method should improve our ability to relate variability
in larval production to environmental fluctuations at finer spatial scales.
Keywords: catch-curve, larval fish, population dynamics, recruitment potential, size-structure, survival.

1984). Yet, despite advances in our understanding of key processes,

Introduction
Forecasting productivity of fish stocks has been a primary goal of
fisheries science for over 100 years (Dannevig 1907; Hjort 1914);
however, our ability to make accurate forecasts of abundance from
adult stocks is often hindered by the high rates of demographic
variability in the early life stages (Pepin 2015a). Various hypothe-
ses have been developed to explain what determines the success of
fish from egg to juvenile stages (Hare 2014), based on the variabil-
ity of migratory pathways, adult abundances, parental investment,
prey abundance and distribution, dispersal (Hjort 1914), predation
(Bailey and Houde 1989), physiological responses to the environ-
ment (Fry 1971; Neill et al., 1994), growth and mortality trade-
offs (Anderson 1988), fishing mortality (Beverton and Holt 1957),
and adult trophic interactions (Odum and Odum 1955; Polovina

C The Author(s) 2021. Published by Oxford University Press on behalf of International Council for the Exploration of the Sea. All rights
reserved. For permissions, please e-mail: journals.permissions@oup.com
the low availability of information on population metrics such as
spawner biomass and high variability in survivorship limits relia-
bility of model fits and prevents meaningful predictions of recruit-
ment (Pepin 2015a).
To improve our understanding of environmental effects on the
larval period and cohort success, we need to better resolve popula-
tion dynamics, which is difficult in marine ecosystems. The relative
importance of growth and mortality in determining survivorship is
known to be potentially equal (Houde 1987; Beyer 1989), but es-
timating growth is both more accurate and easier than mortality,
which has led to an unequal focus on growth in empirical stud-
ies (Takasuka et al., 2017). This discrepancy is likely caused by the
nature of oceanographic studies, where temporal resampling of a
cohort is impractical or in many cases, impossible for pelagic larvae.
A novel approach for estimating growth and mortality of fish larvae
Moreover, current “snapshot” techniques require large sample sizes,
which may be difficult to collect as a result of financial or time con-
straints on research projects. Estimating mortality rates at different
relative scales in contrast to growth rates (e.g. population versus
individual) compounds the problem (Govoni 2005). This imbal-
ance of focus is made more problematic as high rates of predation-
driven mortality have been shown to positively bias sampling of
growth rates (Takasuka et al., 2003; Tian et al., 2007). We therefore
need to improve our ability to estimate mortality and increase ef-
forts to incorporate both these vital rates into empirical research
if we hope to enhance our ability to make predictions of cohort
success.
Well-resourced longitudinal studies can follow cohorts through
space and time to estimate changing rates of growth and mortality
(Rutherford et al., 1997; Vanalderweireldt et al., 2019), though these
methods are heavily dependent on spawning seascape and often not
possible outside of estuaries or semi-enclosed bays. Alternatively,
many currently used methods estimate growth and mortality based
on a standardised snapshot of a population (i.e. a survey or program
level estimation that does not incorporate time), using subsequent
otolith microstructure analysis where age is estimated from daily
growth rings (Stevenson and Campana 1992). Growth can be mea-
sured at the individual level, while mortality is estimated at the sam-
ple or population level. Sampling mortality requires a large number
of observations to achieve adequate resolution. Typically, growth is
determined from length-at-age relationships using linear or non-
linear models, such as a Gompertz (Gompertz 1825) or von Berta-
lanffy growth equations (von Bertalanffy 1938). Weight-specific in-
stantaneous growth may also be estimated using exponential mod-
els (Sassa et al., 2014). Mortality is most commonly estimated from
an age-frequency distribution, where the relationship between the
abundance of individuals in adjacent age-bins is used to determine
an instantaneous mortality coefficient (Pepin 2015b). Early research
commonly used length data (rather than ages) directly to estimate
mortality, where length was considered to be representative of age
based on a linear age–length relationship (Pepin 1991; Houde 1997;
Pepin 2015b). Remarkably, these approaches enable researchers to
measure demographic rates, based only on a one-off snapshot of the
population from a single survey.
The scale of such snapshots commonly varies between studies,
from estimates derived by combining multiple tows for a single sur-
vey (e.g. Sassa and Takahashi 2018) to estimates determined from
a database comprised of several surveys across multiple years (e.g.
Bailey et al., 1996; Rutherford et al., 1997). In some cases, such as
for plaice (Pleuronectes platessa) in the North Sea (Bannister et al.,
1974), survey-level mortality rates of larvae have accurately pre-
dicted subsequent year-class strength when hindcast, although suc-
cessful forward predictions of recruitment remain a rarity. To max-
imise the utility of sampling data, we need to estimate rates of mor-
tality and growth across all possible spatial scales. For example, one
can imagine a situation where age-size data from an extensive sam-
pling survey comprised of many tows are used to estimate a sin-
gle rate of mortality and growth for a given seascape. Based on the
outcome of this work, the ratio of mortality to growth is high (or
growth to mortality is low), thus one concludes that the recruitment
potential for the species is low for that survey period (e.g. Sassa
et al., 2014) and may predict the number of individuals likely to
reach the juvenile stage is also low (Secor and Houde 1995; Houde
1997). If variability in the ratio of mortality to growth across the
seascape is more easily observed, it is possible that larvae of some
areas are experiencing a much lower mortality to growth ratio, and

as such, that area may provide a disproportionate number of sur-
vivors to the juvenile stages. This could mean that interpreting the
mortality to growth ratio estimate for the entire seascape alone pro-
vides a more dire assessment of potential success than exists.
The minimum spatiotemporal scale at which variance in mor-
tality and growth could be estimated will vary between species
and seascapes. To sample enough larvae to fit catch-curve models
appropriately (Ricker 1975), the volume of a tow or the number of
collated tows should reflect the in situ abundance of the species be-
ing investigated, which will influence the spatial resolution of out-
puts. The stability of the seascape may also limit spatial resolution,
factoring in bias on mortality estimates caused by aberrant drift
(Houde 2002), as scale dependency may largely be restricted owing
Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022
to losses via advection (Helbig and Pepin 1998). A significant issue
which needs considering is variation in the hatch-rate of individ-
uals, which could violate a key assumption of catch-curve models.
Variability in the flux of individuals into the system can propagate
error in estimates of mortality, which if fluctuating around a mean
daily value can be largely ignored (Ricker 1975); however, if the
variance in hatch-rate is non-random, for example, shifting because
of a spawning season ending, estimates of mean mortality may be
skewed. For this reason, a good understanding of a species spawn-
ing ecology and habitat is needed. Attempts to resolve mortality and
growth at finer scales should probably be limited to species who ex-
hibit protracted spawning times, such as Pacific sardine (Sardinops
sagax) in coastal waters of south-eastern Australia (Sexton et al.,
2019) or Atlantic cod (Gadus morhua) in inshore bay areas of
southern Newfoundland (Rose and Rowe 2020), and applied to
samples from areas that spatially overlap spawning locations.
There are, however, other shortcomings in the way mortality
rates are estimated using current methods, which prohibit detailed
inferences. First, data are typically divided into relatively large age
or length bins, making the methods sensitive to the choice of bin
widths and sample size (Figure 1). This is true for a variety of com-
mon methods such as catch-curves (Ricker 1975; Maceina 1997)
and the Chapman–Robson method (Chapman and Robson 1960),
described further in the "Estimators" section. Second, to obtain
larger sample sizes, researchers often combine multiple samples
across large temporal or spatial distributions to determine a mean
mortality rate (Watanabe et al., 1997; Sassa et al., 2014; Sassa and
Takahashi 2018), which hinders our ability to resolve environmen-
tal effects on cohort success at fine scales relevant to the drivers of
instantaneous vital rates (i.e. at the tow/sample level). Third, sepa-
rate models are used to estimate growth and mortality rates which is
problematic in two ways. First, data from the same specimens must
be handled in multiple steps using multiple models. Second, un-
certainty in one model may not be incorporated appropriately into
the other. As length-at-age is typically only known for a subset of a
sample population, which are then used to determine the ages of all
individuals in a sample (i.e. using a growth rate) (Pepin 2015b), un-
certainty in the length-at-age relationship is not conserved in the es-
timation of mortality. Combined, these shortcomings suggest new
techniques that simultaneously estimate both vital rates from an ob-
served size distribution are needed.
Size distributions capture the demographic consequences of
growth and mortality rates (Muller-Landau et al., 2006) (Figure 2).
A formal link between growth and mortality rates with size distri-
butions is described mathematically by McKendrick–von Foerster
equation (6) (Von Foerster 1959; Sinko and Streifer 1967), where
the number of individuals at a given size is related to the flux of
individuals into a population (i.e. hatch-rate or recruitment rate)

Figure 1. Schematic demonstrating the influence of bin size on the
slope of classic catch-curve. Data were generated with sample size
varying from  to , and a classic catch-curve model was run
using the same data with -day and -day bin width sets. z̄ set at .
for all model runs, represented by dotted black lines. Solid black line
represents a slope of  (i.e. -day model = -day model).
and the integral of mortality over growth. This equation has been
widely used in fish and plankton research to numerically describe
trophic and disturbance dynamics (Ebert et al., 1993; Smith et al.,
1998; Law et al., 2009; Datta et al., 2011; Heneghan et al., 2016; Blan-
chard et al., 2017; Law and Plank 2018), and to compare/estimate
rates of recruitment, mortality, and growth from changes in plant
density with size within forest plots (Coomes et al., 2003; Kohyama
et al., 2003; Muller-Landau et al., 2006). As the theory is not taxon
specific, similar methods can be applied to empirical fisheries, par-
Figure 2. Schematic demonstrating size-structured population dynamics metrics of a larval fish cohort. The x-axis shows the size s of individual
fish, which can be described in either terms of length (mm) or weight (mg). Growth ḡ drives individuals across the x-axis from left to right, from
their size-at-hatch s towards their size-at-recruitment into the fishery. The y-axis describes n, the abundance of individuals per unit size per
unit volume (e.g., abundance mm- m ). Mortality z̄ determines the decrease on the y-axis from no (the n of individuals at s ), which is itself
determined by the larval hatch rate R.
C. Hinchliffe et al.
ticularly for the early life stages, given we can quantify the size, age,
and density of larvae based on the estimated volume of a plankton
tow. This approach could help to improve upon shortfalls of com-
mon mortality estimation; first by modelling growth and mortal-
ity within a single framework thereby conserving uncertainty from
the length- or weight-at-age relationship in mortality estimates, and
second by removing the need to arbitrarily set age-bin sizes, thereby
making the approach less sensitive to sample size (Muller-Landau
et al., 2006).
Here, we develop variants of a size distribution model to deter-
mine rates of growth and mortality for three data handling scenar-
ios common in fisheries literature: (i) the age of every fish in a sam-
ple is known; (ii) the size of every fish in a sample is known and
Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022
a literature-derived growth rate is applied, and (iii) the size of ev-
ery fish in a sample is known and the age of fish is estimated for
a subset of the sample. We then test the efficacy of applying our
size distribution model to empirically derive rates of growth and
mortality by generating populations with known values of larval
hatch rate, growth, mortality, and size-at-hatch. We compare the
skill of our model in estimating these values accurately, compared
to three other commonly used methods of mortality estimation
(Nelson 2019a): the classic catch-curve (Ricker 1975); a weighted
catch-curve (Maceina 1997; Maceina and Bettoli 1998), and the
Chapman–Robson method (Chapman and Robson 1960). We sys-
tematically test the bias of each of these models by adding variability
to individual rates around mean values used in the data generating
population model.
Methodology
Our goal is to estimate the mean mortality (z̄) experienced by fish
caught in a one-off sample (i.e. not tracked over time). All the meth-
ods applied here achieve this by comparing the abundances of fish
at different size and/or ages, assuming that the temporal pattern in
A novel approach for estimating growth and mortality of fish larvae 

Table 1. Notation used for models, data generation, and output from analyses of the catch-curve, weighted catch-curve, Chapman-Robson
method, and all three variants of the size distribution models.

Parameter Description Units

n Abundance as a continuous measure from a Individuals per unit size or age per volume
density function, with respect to size or age
N Abundance with respect to a size- or age-class. Individuals per unit size or age per volume
a The age of each fish  day
s Size of an individual Standard length (mm)
s0 Size-at-hatch for an individual. Standard length (mm)
s0 Sample or population mean size-at-hatch. Standard length (mm)
g Instantaneous growth rate. mm day−
ḡ Sample or population mean growth rate. mm day−
day−

Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022

z Instantaneous mortality rate.
z̄ Sample or population mean mortality rate. day−
p The probability an individual will survive to the –
specified day. Used in generating sample
populations.
q The age of each fully recruited age-bin (i.e. fully days
vulnerable to sampling gear), defined as each
age-bin in a sample that is equal in age or older
than the most abundant age-bin (i.e. the modal
age). Used in the Chapman-Robson estimator.
u The oldest age-bin in a sample, used in the
Chapman-Robson estimator.
R The rate at which new individuals arrive in a Individuals day− m−
sample/population (i.e. the larval hatch-rate or
recruitment rate).

spawning is constant over the time interval from the smallest to
largest sizes. Note that while length is the most common metric of
size used in larval fish studies, we use the more generic notation
of “size” because weight measurements can also be applied using
the same models. Weight is often used when assessing the “recruit-
ment potential” of a cohort (Houde 1997; Sassa et al., 2014; Sassa
and Takahashi 2018).
The following notation is used (Table 1). For an individual, we
let a be age, s be size, s0 be size-at-hatch, g be instantaneous growth
rate, and z be instantaneous mortality rate. Within a population, let
R be the larval hatch rate, z̄ be the mean mortality rate, ḡ be the
mean growth rate, and n(a) be the abundance of fish with age a.
Note n(a) is a continuous measure with respect to a, and so gives
the number of fish per unit age per unit volume (or area) of water.
Several of the methods require estimates of total abundance within
an age class, which we indicate by Na .
Assuming larval hatch rates are relatively constant with time, fish
abundances naturally decline with time, according to the classic sur-
vival equation
n(a) = n0 exp (− z a) . (1)
Equation (1) works when abundance is measured as a continu-
ous density function (i.e. n(a)), or as counts in age classes (Na ) and
underpins all of the methods applied.
in the “Estimators” section. The first scenario is entirely age-based,
while scenarios 2 and 3 use a size-based approach in combination
with a growth rate estimated from the literature or a subset of age-
at-size data.
Scenario 1—age is known
The first scenario is where the age of every individual larval fish
is known. Most commonly, ages are obtained through otolith mi-
crostructure analysis of daily growth rings (Stevenson and Cam-
pana 1992; Quiñonez-Velázquez et al., 2000).
Scenario 2—age is estimated from a published relationship
In scenario 2, ages are estimated as a function of size using pub-
lished or estimated growth equations from the literature (Houde
2002; Pepin 2015b). In this case, the size of every individual in a
sample is measured, and a species-specific growth rate ḡ and size-
at-hatch s0 (estimated from the intercept of a published growth rate
model) are used to calculate ages. For the case of linear growth rates,
age is estimated as
s − s0
a = . (2)
ḡ

Scenario 3—age is known for a subset of fish

Data handling scenarios
In fisheries research, there are a variety of data handling procedures
that may be used when trying to determine stock or population dy-
namic rates. Here, we consider three data handling scenarios that
are used to estimate mean rates of instantaneous mortality from a
sample of either adult or larval fish, using the methods described
Scenario 3 is perhaps the most common when trying to estimate
growth and mortality. When obtaining age information for an entire
sample is too costly, the size of every individual in a sample is mea-
sured and a subset of the sample is processed to obtain ages through
otolith microstructure analysis (Coggins Jr et al., 2013). The rela-
tionship between age and size from the subset of the sample is then

used to determine a mean growth rate, and this mean growth rate
is then used to estimate ages of the remaining sample via (2) (Sassa
et al., 2014; Sassa and Takahashi 2018).
Estimators
To assess the efficacy of our size distribution models, we compare
them to three commonly used methods for estimating z̄. These in-
clude the classic catch-curve based on a simple linear regression
(Ricker 1975), a weighted catch-curve based on a weighted linear
regression (Maceina and Bettoli 1998), and the Chapman–Robson
method (Chapman and Robson 1960).
Simple catch-curve
The basic catch-curve is based on a loglinear relationship between
the number of fish caught in age classes (Na ) and their age. Log
transformation of (1) gives
log (Na ) = log (N0 ) − z̄ a. (3)
Weighted catch-curves
The weighted catch-curve uses a two-stage process, where a simple
catch-curve (3) is first used to estimate log abundance-at-age. Us-
ing the same data, a weighted linear regression is then fit, using the
fitted values of log abundance-at-age from the simple catch-curve
C. Hinchliffe et al.
Size distribution models
Our model involves two innovations. First, we use the theory of age-
and size-structured populations to derive exact predictions of n, for
a given combination of growth and mortality functions. In this anal-
ysis, we restrict ourselves to the simplest possible functions: linear
growth (2) and constant mean mortality. This is so that our results
are directly comparable with the existing methods outlined above,
where these assumptions also apply. In other words, our focus is on
improving the statistical fit of the model and not on changing as-
sumptions about the dynamics of the system. We therefore make
the same assumptions as the catch-curve with the aim of demon-
strating that our size distribution model provides more accurate and
precise statistical estimates of the underlying parameters. However,
Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022
it is worth noting that more complex functions can be used with
the new approach, which we address in the "Discussion" section.
Second, we use an improved statistical technique to estimate the
parameters of the models (including z̄) without having to group in-
dividuals into larger bins.
There are three variants of our model, one for each of the dif-
ferent data handling scenarios. For scenario 1, the model is simply
that shown in (1). The other two models are derived from the gen-
eral McKendrick-von Foerster partial differential equation (PDE)
for size structured population dynamics (Von Foerster 1959; Sinko
and Streifer 1967). Further, n is written as a function of size s, not
age (i.e. we consider how the abundance of larvae changes with size
rather than age). Assuming constant larval hatch rate, the PDE can
be solved to give an equation for the density individuals of size s as
as weights. Mortality is estimated from the slope coefficient of this a(s)  
δg (s (a ) , E)

 
second weighted regression (Nelson 2019a). This technique has the n(s) = n(s0 ) exp − ∫ + z s a , E da ,
effect of assigning smaller weights to older, rarer fish reducing their 0 δs
contribution to the regression sum of squares (and has the oppo- (6)
site effect for younger, more abundant fish) (Maceina 1997; Maceina
and Bettoli 1998) such that where g(s, E) and z(s, E) are the growth and mortality rates of in-
dividuals of size s in environment E, n(s0 ) is the initial density of
log (Na ) = log (N0 ) − z̄ · b1 (a) , (4) recruits, s(a ) is the size of individuals age a , and a(s) is the age of
individuals size s. By linking the flux of individuals across the lower
where b1 is the partial regression coefficient estimated from the pre- bound, s0 of the size distribution to the rate R at which new individ-
dicted natural log of abundance-at-age using (3). uals arrive (i.e. larval hatch or recruitment rate), we can substitute
R
n(s0 ) = . (7)
Chapman–Robson method g(s0 )
The Chapman–Robson method is commonly applied to adult Note that the age distribution in (1) can be derived as a special
stocks to estimate annual mortality rates, and has recently been case of the more general distribution in (6), where size is measured
shown to be robust to sampling biases driven by gear-type (Nelson as age a (i.e. s = a), such that g = 1 and δg δs
= 0. This serves as
2019a). This method models age as a geometric distribution, giving the basis for our size distribution model used for scenario 1.
(Chapman and Robson 1960; Nelson 2019a) For scenarios 2 and 3, we can reorganize (6) so that the integral
⎛ u ⎞ is expressed in terms of size, not age. Following equation (22) of de
q=0 qNq
Roos (1997), we get
z̄ = log ⎝   ⎠ 
u s z (s , E)
N+ q=0 qNq − 1
R 
n(s) = exp − ∫ ds . (8)
s0 g (s , E)
g (s, E) 
⎛ ⎞
(N − 1) (N − 2)
−⎝       ⎠, Substituting in functions for z and g then leads to exact equa-
N N+ u
q = 0 qNq − 1
u
q = 0 qNq +1 tions for n(s). Assuming z(s, E) = z̄ and g (s, E) = ḡ leads to a
predicted size distribution (Muller-Landau et al., 2006)
(5) 
R (t ) z̄
n(s) = exp − (s − s0 ) . (9)
where q is the age of each fully recruited age-bin (i.e. fish that are ḡ ḡ
considered to be fully vulnerable to sampling gear), which is defined In scenario 2, ḡ is specified based on available literature values.
as each age-bin in a sample that is equal in age or older than the For scenario 3, ḡ is estimated alongside z̄, by fitting the growth
most abundant age-bin (i.e. the modal age), and u is the oldest age- model (2)
bin. The ages of the fully recruited fish are standardized to begin at
q = 0. s = s0 + ḡa (10)
A novel approach for estimating growth and mortality of fish larvae
using a subset of the sample with available age a and size s. This oc-
curs simultaneously alongside fitting of the size distribution model
(using the size s of all individuals in the population), which esti-
mates ratios of Rḡ and z̄ḡ . With ḡ constrained by the growth model
this leads to an estimate of R and z̄. The advantage of fitting both
models simultaneously is that uncertainty in the growth rate is
preserved.
To fit (1) and (9) to data, we use the following likelihood model.
First, we count the number of individuals recorded at each size
along the measurement scale, binning only at the scale of measure-
ment resolution, i.e. Nsi , where si for i = 1, . . . , n are the size in-
tervals. We limited the precision of size measurements to 0.1 mm,
so individuals are counted in 0.1 mm bins. Note that while we have
selected 0.1 mm as our measurement resolution, the model imple-
mentation is identical for data which may have a coarser resolution
(e.g. 0.5–1 mm). With small sample sizes, most values of Nsi are
zero. The expected number of individuals in each interval is ob-
tained by integrating the density function from si−1 to si . For sce-
narios 2 and 3, integrating (9) gives the number of individuals in
each size class Nsi as

ures as worked examples are available at https://github.com/charlie
hinchliffe/models_for_larval_fish_growth_and_mortality.
The catch-curve, weighted catch-curve, and Chapman–Robson
estimates of z̄ were obtained using the "agesurv" function from
the "fishmethods" package (Nelson 2019b), applying the "lr", "wlr",
and "crcb" methods, respectively. Age-bins used in these models
were set at 1-day widths. Size distribution models were built in the
Bayesian inference language Stan and implemented in R using the
package "rstan" (Stan Development Team 2019). Model param-
eters were estimated using Markov chain Monte Carlo (MCMC)
sampling, with three chains and 999 iterations. For each variant
of the data generation parameters described, models were run 500
times. For all models, age resolution was set at 1-day integers, and
Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022
size resolution was set at 0.1 mm, to reflect appropriate finest scale
measurements made on fish larvae under laboratory conditions
(Mullaney and Suthers 2013). Prior values for z̄, ḡ , and R were
drawn from a Cauchy distribution with mean of 10 and wide
variance, truncated to positive values.
To observe the influence of variability in each parameter on
model efficacy, we simulated populations such that ideal conditions
 
R z̄ z̄
Nsi = − exp − (si − s0 ) − exp − (si−1 − s0 ) . tigated (i.e. large sample size and no variability in parameters). For
z̄ ḡ ḡ
(11)
These estimates are then compared to the observed counts using a
Poisson probability distribution
 values here (z̄r ), where z̄r is the percentage difference between the
Nsi ,obs ∼ Poisson Nsi .
In scenario 3, ḡ is simultaneously constrained by comparing the
predicted sizes (from 10) to observed sizes, using a Gaussian prob-
ability distribution.
A similar approach is used to fit data to scenario 1, but using age-
bins integrating (1) gives
R
 To investigate the influence of R, we simulated populations with
Nai = − exp (−z̄ ai ) − exp (−z̄ ai−1 ) . (12)
z̄
Data generation
To test the efficiency of the different models, we generated data
with known values for z̄, ḡ , and R, and assessed how well the four
models could recover the known values. We used a basic popula-
tion model that allows for daily larval hatch (or recruitment), in-
dividual growth, and survival to vary around specified mean val-
ues. The daily number of recruits was randomly generated from a
Poisson model with rate R. These individuals were then grown to
time of sampling according to (10). At this point, a random num-
ber of individuals were allowed to survive, with probabilities p =
exp(−z̄ a). Each individual was initiated with values for z, g, and
s0 drawn from normal or log-normal distributions with a speci-
fied mean and standard deviation. This data generation method
assumes that individual-level mortality rates and individual-level
growth rates are serially correlated through time—assumptions
that are also implicit in the common catch-curve methods investi-
gated here (Chapman and Robson 1960; Ricker 1975; Maceina and
Bettoli 1998).
Simulations
All statistical analyses were performed using R version 3.6.1 (R Core
Team 2019). Source code for reproducing all the analyses and fig-
were evident in all parameters except for the parameter being inves-
each simulation, R was set at 500 (when not being investigated), s0 at
3 mm, ḡ at 0.21, and z̄ at 0.25. Models that returned estimates closer
to z̄ = 0.25 and ḡ = 0.21, with less variability in estimates, were
considered more skilful than those that gave either biased or more
variable estimates. For ease of interpretation, we present relative z̄
estimated z̄ and the true z̄ used to simulate the population (i.e. an
estimated z̄ of 0.25 is equivalent to a z̄r of 0%, an estimated z̄ of 0.2
is equivalent to a z̄r of –20%, and an estimated z̄ of 0.3 is equivalent
to a z̄r of 20%). The same applies to growth estimates. Performance
is greatest when mean z̄r and ḡr estimates are closer to 0% and the
standard deviation in z̄r and ḡr is smaller.
R equal to 5, 10, 20, 50, 100, and 500. To investigate the influence
of variability around log10(s0 ), log10(ḡ), and log10(z̄), the standard
deviation (σs0 , σg , and σz , respectively) was set at 0, 0.005, 0.01, 0.02,
0.03, 0.05, and 0.1. These standard deviations were set across this
range such that the level of variance that bias was introduced into
model estimates was able to be observed for each parameter.
To observe the effect of applying a theoretical species-specific
growth rate from published literature that differs from the “real”
growth rate of a sampled population in scenario 2, we increased the
bias between the theoretical literature g in the models and ḡ used to
simulate data by 0% (i.e. 0.21), 1, 3, 5, 10, 25, and 50% (i.e. 0.315).
To understand how the number of individuals that are selected for
aging in scenario 3 affects estimates of ḡ and z̄, we set coarse size
bins of 1.5 mm and then randomly selected 1, 3, 5, 10, 20, 40, and
80 individuals (Ngrowth ) from each size bin to be used in the growth
estimation models. We consistently applied variability of σ = 0.3
to individual ages, and σ = 1 for individual sizes within growth
models, while maintaining ideal conditions for each generated
population.
While running the analyses presented here, we observed that
generating populations with even low levels of variance in size-at-
hatch (i.e. σs0 > 0) caused model estimates of z̄ to quickly diverge
from the true value of z̄ used to generate populations (see the "Sce-
nario 2" section under "Results"). We therefore added a function
into our data generation methods to subset data by removing all
individuals smaller than the modal size class when specified. The
 C. Hinchliffe et al.

(a) R
5 10 20 50 100 200 500
200

100
zr
0

−100

Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022

−200

(b) σz
0 0.005 0.01 0.02 0.03 0.05 0.1
20
zr

−20

Figure 3. Distribution of z̄r estimates from scenario 1. Horizontal red lines at z̄r = % represent the “true” . z̄ used to generate populations. In
each cell from left to right, violins represent z̄r estimates from the catch-curve, weighted catch-curve, Chapman–Robson, and size distribution
models, respectively. Horizontal lines within violins represent , , and % quantiles. (a) Larval hatch rate R per day. (b) Values show σ of
individual z around log(z̄).

modal size class is defined as the most abundant 0.1 mm size bin
in the population (i.e. where N is at its maximum across the dis-
tribution of sizes). This function was used where variability in s0
created size structured populations in which the modal size class
was not the smallest size class in the population (i.e. 3–3.1 mm),
with the aim of returning more accurate z̄ estimates (i.e. closer to
z̄ = 0.25).
Results
Under ideal conditions, all models across the three data han-
dling scenarios perform well, returning accurate and precise
estimates of ḡ and z̄. The bias and standard deviation of all the
size distribution model z̄r estimates ranged from –71.57 to 20.59%
and ±0.01 to ±32.52%, respectively. The Chapman–Robson
method had a range of z̄r estimates from –65.06 to 56.45% and a
range in standard deviations from ±1.40 to ±64.32%. The catch-
curve had a range of z̄r estimates from –58.57 to 10.46% with a range
in standard deviations from ±0.01 to ±36.65%, while the weighted
catch-curve had a range of z̄r estimates from –73.42 to 19.96% and a
range in standard deviations from ±2.14 to ±71.43%. The estimates
and standard deviation from every configuration of the models run
here can be found in Supplementary Table 1.
Scenario 
As expected, the general trend across all four models demonstrated
more precise and accurate estimates of z̄ as R increases under data
handling scenario 1 (Figure 3a). The size distribution model re-
turns better estimates of z̄ at low levels of R (and sample size),
with z̄r = –2.37% (±32.52% standard deviation, presented as brack-
eted ±values hereon) when R = 5 (sample size ≈ 25), a pattern con-
sistent across all levels of R tested here (Figure 3). The weighted
catch-curve performed the next best with z̄r = –7.58% (±66.69%),
followed by the classic catch-curve and Chapman–Robson mod-
els [z̄r = –51.48% (±31.72%) and 55.29% (±64.09%), respectively].
The classic catch-curve method underestimated z̄ at all levels of R
tested here except the highest (R = 500), with model z̄r estimates
being more than one standard deviation away from z̄r = 0%.
All four models were robust to variability in individual z
(Figure 3b). All models returned z̄r estimates within one standard
deviation from 0%, up until σz was set at 0.05 around log10(z̄)
(equivalent to σ of ±12% around z̄). Above σz set at 0.05, bias in
estimates of z̄ started to increase.
Scenario 
Results from data handling scenario 2 were similar to scenario 1,
with all four models giving more precise and accurate estimates of
A novel approach for estimating growth and mortality of fish larvae
z̄ as R increases, and a high degree of robustness to variability in in-
dividual z (Figure 4a and b). The size distribution model returned
better estimates of z̄ at low levels of R (and sample size), with z̄r = –
0.04% (±30.91%) and –2.42% (±18.71%) when R = 5 and 10 (sam-
ple size ≈ 25 and 50), respectively. The weighted catch-curve per-
formed the next best with z̄r = –7.63% (±65.63%) at R = 5 and z̄r
= –11.52% (±26.96%) at R = 10. The classic catch-curve method,
again, underestimated z̄ at all but the highest levels of R tested, with
z̄r estimates being more than one standard deviation away from
0%. All models returned z̄r estimates with low variability that were
within one standard deviation from 0% when variability in individ-
ual z was low, up to σz set at 0.05 (equivalent to σ of ±12% of z̄).
Variability in individual s0 was problematic for all models, even
at low levels of σs0 (Figure 4c). With σs0 around log10(s0 ) set at
0.005 (equivalent to σ of just ±1% of s0 ), all models underestimated
z̄r by between 2.3 [size distribution model -11.49% (±4.93%)]
and 13.6 [Chapman–Robson –19.1% (±1.4%)] standard deviations
away from 0%. The bias from z̄r = 0% increased further for all
models as σs0 increased. The use of modal subsetting function im-
proved z̄r across all models and all levels of σs0 (Figure 4d), with
every model returning a z̄r within one standard deviation from 0%
up to σs0 = 0.03, equivalent to σ of ±7% of s0 [weighted catch-
curve z̄r = 0.04% (±3.37%), size distribution z̄r = 0.33% (±5.93%),
catch-curve z̄r = 0.7% (±4.56%), Chapman–Robson z̄r = 1.22%
(±2.77%)]. At σs0 = 0.05 (equivalent to σ of ±12% of s0 ), the classic
catch-curve, weighted catch-curve, and the size distribution mod-
els had mean z̄r within one standard deviation from 0% [z̄r = –
2.62% (±4.3%), –2.48% (±4.04%) and –4.83% (±7.01%), respec-
tively) while the Chapman–Robson methods did not (z̄r = –5.75%
(±3.9%)].
When the difference between the literature g rate applied in sce-
nario 2 and ḡ used to generate the population increased, a fast de-
cline in the ability of all models to return accurate estimates of z̄
was observed (Figure 4e). At literature g set at 5% above ḡ (i.e. lit-
erature g = 0.2205), all z̄r estimates were more than one standard
deviation from 0% [catch-curve z̄r = –5.07% (±3.91%), weighted
catch-curve z̄r = –3.64% (±3.2%), Chapman–Robson z̄r = –3.56%
(±2.09%), size distribution z̄r = –5.43% (±4.32%)]. When litera-
ture g is set 50% above ḡ, z̄r decreased by more than 30%.
Scenario 
Data handling scenario 3 results also showed all four models giv-
ing more precise and accurate estimates of z̄ as R increases, and a
high degree of robustness to variability in individual z (Figure 5a
and b). The size distribution model returned better estimates of z̄
at low levels of R (and sample size) than other models, with z̄r =
1.08% (±29.04%) and –3.32% (±19.45%) when R = 5 and 10 (sam-
ple size ≈ 25 and 50), respectively. The weighted catch-curve per-
formed the next best with z̄r = –5.38% (±71.43%) at R = 5 and
z̄r = 14.42% (±26.87%) at R = 10. The classic catch-curve method
again under predicted z̄ at all levels of R tested here except the high-
est (R = 500), with the mean z̄r estimates being more than one stan-
dard deviation away from 0%. All models returned z̄r estimates with
low variability that were within one standard deviation from 0%
when variability in individual z was low, up to and above σz around
log10(z̄) set at 0.03 (equivalent to σ of ±7% of z̄).
Individual variability in s0 caused z̄r estimates to deviate from 0%
for all models as σs0 increased, though scenario 3 methods appear
to be more robust than scenario 2 methods (Figure 5c). All mean
model z̄r estimates were within one standard deviation from 0% up

to the level of σs0 = 0.02 (as opposed to 0.005 in scenario 2). The
catch-curve and weighted catch-curve returned mean z̄r estimates
at the highest level of σs0 = 0.1 within one standard deviation of 0%
(z̄r = 3.31% (±8.29%) and –5.31% (±7.43%), respectively), while
the Chapman–Robson and size distribution model estimates were
more than one standard deviation away from 0% when σs0 = 0.03
(z̄r = –7.58% (±3.1%) and –9.2% (±5.73%), respectively). The use
of a modal subsetting function (see the "Methods" section) im-
proved z̄ estimates across all models and all levels of σs0 (Figure 5d),
with all models at all levels of σs0 returning mean z̄r estimates within
one standard deviation from 0% except the catch-curve where z̄r =
10.46% (±10.17%) when σs0 = 0.1.
All models were relatively robust to individual variability in g,
Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022
with all mean z̄r estimates within one standard deviation from 0%
(Figure 5e) and all ḡr estimates within one standard deviation of 0%
(Figure 6a) up to level σg = 0.03. As σg around log10(ḡ) increases
above 0.03, mean z̄r estimates begin to deviate above 0% increas-
ing to 5.59% (±8.62%), 19.96% (±9.98%), 22.3% (±9.72%), and
20.59% (±7.61%) at σg = 0.1 for the catch-curve, weighted catch-
curve, Chapman–Robson, and size distribution models, respec-
tively. Model ḡr estimates across the same σg range demonstrated
a similar pattern, increasing above 0% when σg is greater than 0.03,
with variability in ḡr estimates from the linear growth model used
in the catch-curve, weighted catch-curve, and Chapman–Robson
methods (i.e. length-at-age regression) being greater than the size
distribution model ḡr estimates. The ḡr estimate from the linear
growth model was equal to 7.37% (±5.9%) at σ = 0.05 and 25.11%
(±9.72%) at σ = 0.1, while size distribution model ḡr = 6.18%
(±3.47%) and 22.62% (±6.91%) at the same levels of σ .
As the number of individuals used in the estimation ḡ increased,
the variability in z̄ estimates from all models decreased as expected
(Figure 5f). The size distribution model had the least variable z̄r
estimate at lower levels of Ngrowth selected from each rough size bin,
with z̄r = 4.26% (±18.3%), 2.02% (±11.51%), 2.05% (±9.58%), and
2.24% (±7.13%) at levels Ngrowth = 1, 3, 5 and 10, respectively. The
Chapman–Robson model had the next least variable estimates of z̄r
= 0.62% (±18.3%), –0.19% (±18.74%), –0.19% (±14.67%), and –
1.29% (±10.16%) across the same levels. Estimates of ḡ from the
classic linear growth model and size distribution model had the
same trend of decreasing variability with increasing Ngrowth . The size
distribution model returned less variable estimates of ḡ than classic
growth models, with size distribution model ḡr = 5.12% (±17.78%),
2.26% (±10.66%), 2.13% (±8.4%), and 2.44 (±5.58%) at levels
Ngrowth = 1, 3, 5, and 10, respectively. The linear growth models re-
turned ḡr = –1.2 (±34.28%), –1.7% (±18.98%), –1.55 (±14.74%),
and –2.67% (±10.18%) across the same levels of Ngrowth .
Discussion
Our results highlight the value of the novel statistical techniques
and model structure we present for estimating rates of growth
and mortality in snapshot samples of fish larvae. In all three data
handling scenarios, the size-based modelling approaches we assess
here were more accurate at low sample size than the three com-
mon methods we compared them with. This highlights the ad-
vantage of removing the need to bin data and modelling abun-
dance as continuous with respect to age or size. As species-specific
larval abundances often will not exceed more than a few fish
per 100 m3 or double digits for a single tow (Hinchliffe et al.,
2021), any improvements made in our ability to estimate growth
 C. Hinchliffe et al.

(a)

(b)

Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022

(c)

(d)

(e)

Figure 4. Distribution of z̄r estimates from scenario 2. Horizontal red lines at z̄r = % represent the “true” . z̄ used to generate populations. In
each cell from left to right, violins represent z̄r estimates from the catch-curve, weighted catch-curve, Chapman–Robson and size distribution
models, respectively. Horizontal lines within violins represent , , and % quantiles. (a) Larval hatch rate R per day. (b) Values show σ of
individual z around log(z̄). (c) Values show σ of individual s around log(s ). (d) Values show σ of individual s around log(s ) of
generate populations which have been subsetted to remove individuals smaller than modal size. (e) Values show percentage increase between
the literature applied g and ḡ used to generate populations.

and mortality rates at low sample size will be beneficial. This is
particularly critical if our goal is to resolve the effects of envi-
ronmental drivers of growth and mortality at meaningfully fine
scales (Pepin 2004), such that we could predict cohort success for
oceanographic scales that characterize a range of spawning events.
With this in mind, these results suggest that use of the traditional
catch-curve should likely be avoided in favour of another estima-
tor when sample sizes are limited, as it underestimated z̄ across all
three data handling scenarios in populations with less than ∼400
individuals.
A novel approach for estimating growth and mortality of fish larvae 

(a)

(b)

Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022

(c)

(d)

(e)

(f)

Figure 5. Distribution of z̄r estimates from scenario 3. Horizontal red lines at z̄r = % represent the “true” . z used to generate populations. In
each cell from left to right, violins represent z̄r estimates from the catch-curve, weighted catch-curve, Chapman–Robson and size distribution
models, respectively. Horizontal lines within violins represent , , and % quantiles. (a) Larval hatch rate R per day. (b) Values show σ of
individual z around log(z̄). (c) Values show σ of individual s around log(s̄0 ). (d) Values show σ of individual s around log(s̄0 ) of
generating populations that have been subset to remove individuals smaller than model size. (e) Values show σ of individual g around log(ḡ).
(f) Values show number of randomly selected individuals per . mm bin-width (Ngrowth ) used in the ḡ model.
 C. Hinchliffe et al.

(a)

Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022

(b)

Figure 6. Distribution of ḡr estimate from scenario 3. Horizontal red lines at ḡr = % represent the “true” . ḡ used to generate populations. In
each cell, the violins on the left represent the ḡr estimates from the length-at-age regression used in the catch-curve, weighted catch-curve, and
Chapman–Robson methods. The violins on the right-hand side of each cell represent the size distribution model ḡr estimates. Horizontal lines
within violins represent , , and % quantiles. (a) Values show σ of individual g around log(ḡ). (b) Values show number of randomly
selected individuals per . mm bin-width (Ngrowth ) used in the ḡ model.

Scenario  While increasing variability in individual probability of mortal-

In a scenario where the ages of every fish in a sample have been de-
termined, modelling abundance as a continuous density function
(as per (1) or (8) using the statistical techniques we have presented
here, should provide the most reliable estimate of mean cohort mor-
tality. As all models perform adequately at large samples sizes (e.g.
∼2000 fish), but at lower sample sizes, the continuous model per-
forms markedly better (up to ∼200 fish), it is appropriate to rec-
ommend its use over the other models we tested, provided the as-
sumptions regarding the underlying biology used to generate popu-
lations in this study reflect the system being analysed. For instance,
the model we suggest had improved mean relative mortality esti-
mates around 5, 9, and 2% compared to the next best model (and
52, 41, and 30% compared to the worst performing model) when
samples sizes were relatively small (i.e. 20, 40, and 80, respectively).
As these sample sizes are within the typical range of a single plank-
ton tow, these improvements in accuracy would likely make a sig-
nificant impact on our effort to link environmental drivers of mor-
tality at fine scales by helping to reduce noise in a highly stochastic
system.
ity reduced the accuracy of mortality estimates, as a result of bias
caused by the persistence of an increased number of individuals
with very low z, the level of bias appears to be equal across the four
models tested here. Although previous studies have utilised size-
or growth-selective losses to provide a measure of relative individ-
ual mortality based on variability in growth (Takasuka et al., 2004,
2017; Fontes et al., 2011), it is difficult, or impossible, to transform
those inferences into true estimates of individual mortality risk in
a natural system. This implies that while we can infer rough mea-
sures of differential survival from growth rates (i.e. fast growers
have higher survival), this does not precisely inform us about the
variability of the individual probabilities of survival within groups
of larvae experiencing the same environmental conditions. Fur-
thermore, this information cannot be discerned from variability in
mean mortality rates among cohorts. If σ in individual growth rates
of a recently spawned cohort accurately reflect the variability in in-
dividual mortality risk (Takasuka et al., 2004), it may be unlikely
that the σ in individual mortality risk would exceed the >10% of the
cohort mean z̄ which is necessary to make the model estimates un-
A novel approach for estimating growth and mortality of fish larvae
reliable (Figure 3b). Researchers using mortality estimators should
be aware of the substantial effect that high variance in individual
mortality risk could have on reliability of their estimates, while we
remain limited in our ability to estimate this parameter in natural
populations.
Scenario 
Observing the influence of variable R (and sample size) and individ-
ual z on modelling z̄ from a sample where the size of every fish is
known and a literature growth rate is applied demonstrated compa-
rable advantages of our modelling approach to scenario 1, highlight-
ing the robustness of the size distribution method to sample size. At
samples sizes of around 20, 40, and 80 individuals, the size distri-
bution yielded more accurate mean relative mortality estimates of
around 8, 9, and 3%, respectively, compared to the next best model
(and 56, 41, and 30% compared to the worst performing model).
Our findings emphasize the importance of understanding two
aspects of a population before relying on model estimates of z̄ if this
approach is used. First, variability in s0 can heavily and negatively
bias estimates of z̄ even at levels of σ of just ±1% of s0 (Figure 4c),
which is well below what might be expected in a natural cohort.
This is likely because variability in s0 will manifest as bias and un-
certainty in both growth (i.e. the intercept of length-at-age regres-
sion) and mortality models by either incorrectly aging larvae (i.e.
error in growth model affecting catch-curve, weighted catch-curve,
or Chapman–Robson estimates) or shifting the distribution of sizes
so that smallest size interval in a sample is no longer the most abun-
dant (i.e. the size distribution model). The bias caused by variability
in s0 is largely driven by shifts in the intercept of the growth model
and the smallest sizes of the size distribution model because small
differences in s0 correspond to greater relative difference in ages for
younger individuals than older individuals. The bias caused by vari-
ability in s0 highlights a potentially under considered aspect of the
biology of larvae in previous studies attempting to resolve mortality
rates using the common methods available. Larvae hatched under
laboratory conditions commonly show levels of σ in individual s0 in
the range of ±3–10% of s0 (Bengtson et al., 1987; Llanos-Rivera and
Castro 2004; Jordaan et al., 2006; Garrido et al., 2015), which is well
above the level of variability in s0 needed to bias mortality estimates
in scenario 2. Bias caused by variability in s0 can be largely corrected
by removing all individuals smaller than the modal size class for all
models (Figure 4d) such that reasonable estimates of z̄ are returned
within a range of σ in s0 that might be expected of a natural pop-
ulation (i.e. less than ±10% of s0 ). Subsetting data in this way is
already a common approach for dealing with biases in the sampled
size and age distribution of larvae caused by the low catchability of
small young larvae (i.e. extrusion) (Morse 1989; Sassa et al., 2014;
Raya et al., 2020), so applying this approach can be justified here
and may have likely reduced the impact of high σs0 on mortality
estimates in previous studies.
Second, bias in estimates of z̄ caused by even small deviations
in the literature growth rate from ḡ used to generate data here un-
derscore the risk of this data handling approach. This bias occurs
because the survival of larvae is linked to the mortality rate ex-
perienced over the time it takes to grow through a given length,
whereby a positively biased literature growth rate results in an esti-
mated higher proportion of older individuals than actually exist in
the population and a decreased estimate of mortality. The inverse is
true for a negatively biased growth rate, which would result in a pos-
itively biased mortality. Intraspecific mean growth rates are known

to vary between larval cohorts, both temporally and spatially, by
an order of magnitude bigger than the 5% difference (Houde 1997)
here needed to return z̄ estimates from all four models that were
more than a standard deviation away from the true z̄. For exam-
ple, Sassa et al. (2014) show that the cohort mean growth rate (mm
day–1 ) of larval jack mackerel (Trachurus japonicus) can vary over
60% between years as a result of environmental fluctuations in the
southern East China Sea. Given this, the method in scenario 2 is
likely inappropriate for resolving mortality rates at fine scales and
should not be used unless estimating a very crude mortality rate
based on a growth rate that is determined by averaging results from
multiple studies that covers the environmental range of the species
or population in focus.
Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022
Scenario 
Estimating mortality using our size distribution approach when the
ages of a subset of fish are known, along with the size of every
fish in a sample, demonstrated very similar results to scenario 2.
Our model returned the best estimates of z̄ at lower R and was ro-
bust to variation in individual g and z. We found that with sam-
ple sizes around 20, 40, and 80 individuals, the improvement in
mean relative mortality estimates compared to the next best model
is around 4, 11, and 3%, respectively (and 55, 43, and 31% com-
pared to the worst performing model). Furthermore, biases caused
by variability in s0 were of lesser magnitude than in scenario 2 with
mortality estimates remaining relatively accurate above levels of σ
of ±3% of s0 , in the range of what might be expected of some nat-
ural populations (Bengtson et al., 1987; Chambers et al., 1988; Jor-
daan et al., 2006). Use of subsetting to trim data at the modal size
largely corrected remaining bias caused by variability in s0 across all
levels of σ .
In addition to improving z̄ estimates with fewer fish, we found
that our approach has utility in estimating ḡ more effectively than a
standard linear model. We found that not only was the size distribu-
tion model more robust to variability in individual g, the standard
deviation of ḡr estimates was between 43 and 48% less for the size
distribution model than the standard linear model used to estimate
ages for the other mortality estimators. This trend occurred across
all levels of N per size class used to select the subset of individuals
with age and size data available in the growth models (Figure 6).
This finding highlights the applicability of our approach not just
to studies interested in mortality or recruitment indices but also
to those solely concerned with estimating growth rates. As mod-
els exploring environmental effects on growth will likely have high
variability in their residuals as a result of environmental stochas-
ticity, reducing uncertainty in growth estimates as response vari-
ables in these models will improve our confidence in their final
estimates.
Limitations
In the present study, we systematically observe the influence of bias
caused by variability in parameters of population dynamics and
found that variability in individual traits affect model estimates rel-
atively equally across the four models tested here. However, due to
the number of possible populations produced from combinations
of parameters with different variability levels (here, we have four
parameters and tested seven levels of variability, 74 is 2401 possible
population settings), we have not considered interactions between
variability in different parameters (i.e. interactions between varying

levels of σs0 , σg , and σz ). While this approach is common (Saltelli
et al., 2002; Smith et al., 2019), it is possible that we have missed
potential susceptibilities or strengths of the models. For example,
it may be that as σs0 and σg increase, the biases they both cause on
model estimates cancel each other out (or are additive) and this ef-
fect could be non-linear.
This study also omits the use of age-length keys, a common
approach to aging a population from a subsample. This is largely
because they require a large, representative, simultaneously sam-
pled, aged “parental” group collected to avoid bias (Westrheim and
Ricker 1978; Coggins Jr et al., 2013; Ailloud and Hoenig 2019),
which is often unattainable at the tow or sample level, and as such
has limited use in resolving rates at fine scales of interest. Future
developments of the size distributions models could be adapted to
use age-length keys but given the results from scenario 1 where all
ages are known, the continuous model we present (1) would again
offer the best alternative.
There are several limitations which we have not considered
which are related to the underlying biology of the systems being
modelled, and it should be noted that these are of concern for all
the models being tested here. In need of particular attention are the
common assumptions of constant flux of individuals into the pop-
ulation being sampled, and the limited loss of individuals owing
to the advection. As we have alluded to in the introduction, non-
random directional shifts in larval supply can propagate as bias in
z̄ estimates (Ricker 1975; Houde 2002). In attempting to apply the
models presented to resolve larval ḡ and z̄ at finer scales, a good un-
derstanding of specific–specific spawning biology is required. Lim-
iting the age and size range of individuals that mean mortality is
integrated over may alleviate bias introduced by shifts in spawning
(e.g. only include larvae up to 14 days), while understanding bias
driven by advection requires a strong estimation of current fields
in the sampling area (Helbig and Pepin 1998). We have established
that the size-based modelling approach is as appropriate as cur-
rent methods for estimating mortality in circumstances where other
common methods are already applied (i.e. for survey/multiple sur-
vey level estimates) but further empirical field study is needed to
establish the feasibility of applying the models to finer-scale data
(see the "Future directions" section).
Other biological limitations relate to situations where growth
and mortality rates are not constant. For example, mortality rates
are likely to be non-constant through development resulting from
aspects of the growth–survival paradigm (Takasuka et al., 2017),
while some species may exhibit non-constant growth through their
development as a consequence of changes in feeding ability and
success (Pepin et al., 2015; Vasbinder and Ainsworth 2020). Addi-
tionally, problems may arise through the omission of density (or
frequency) dependence in the models, whereby increased popu-
lation sizes reduce resource availability, thereby increasing intra-
specific competition, and reducing growth and survival of larvae
(Stige et al., 2019). This ultimately leads to non-constant popula-
tion rates through time. Density-dependent effects on the early-life
stages of fish have long been thought to impact recruitment (Cush-
ing 1974; Shepherd and Cushing 1980; Stige et al., 2019) and failure
to account for this may cause bias across all the models presented
when tested on real populations. Again, these non-constant rates
will bias estimates from all the models here. However, the easily
modifiable size distribution model that we describe here presents
a new opportunity to determine how rates of growth and mortal-
ity change throughout development and model them accordingly
within a single framework.
C. Hinchliffe et al.
Future directions
A major advantage of the approach we suggest is that it allows for
models to be easily adjusted to assess non-linear growth and mor-
tality scenarios. Muller-Landau et al., (2006) demonstrated how
growth and mortality rates that vary as power functions of size can
be incorporated to predict corresponding size distributions. For ex-
ample, by deriving size-specific growth from non-linear size-at-age
equations such as a Gompertz (Gompertz 1825) or von Bertalanffy
growth equation (von Bertalanffy 1938), we can fit models to pop-
ulations shaped from a wider range of biological conditions. A next
logical step in this research would therefore be to develop a pack-
age wherein multiple growth and mortality models could be fit to
data, and compared, with the aim of retaining the best model based
Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022
on relevant model selection criteria (Ward 2008). Achieving this
would allow widespread application of the size-based modelling
approaches presented here beyond larvae populations into adult
stocks, where growth is very unlikely to ever be linear (Mommsen
2001).
As well as improving estimates of ḡ and z̄, these models may add
to our understanding of the fine scale variability in cohort success
by relating cohort dynamics at the tow or sample level directly to
in situ environmental parameters. The structure of (1) and (8) al-
lows for environmental effects to directly influence estimates, by
including additional submodels in a hierarchical framework (Wikle
2003; Gelman et al., 2015) that specify how ḡ and z̄ vary as a func-
tion of commonly sampled parameters such as temperature, salin-
ity, chlorophyll a, or zooplankton biomass. This will be a valuable
next step in maximising the utility of these models.
An important step in verifying the applicability and utility of the
size distribution models we present here requires their application
to field data. In approaching this, future studies should first assess
variability in accuracy and precision of z̄ and ḡ estimates taken at
the single tow, station (i.e. repeated tows deployed at the same lo-
cation) and entire survey level. In doing so, they ought to evaluate
how reasonable it may be to quantify vital rates at the finest scales
available for a given dataset. Appropriate scales likely vary between
species based on their biology (e.g. short or protracted spawning
times, abundances) and among seascapes (e.g. levels of retention or
aberrant drift, convergence-divergence eddy structure). The neces-
sary precision of these estimates may also vary between projects and
study goals. Where studies have lots of tows available, they may be
less affected by higher error in estimates. For example, a study may
wish to relate variability in z̄ and ḡ with environmental drivers using
the hierarchical framework mentioned above. If error in tow level
estimates (i.e. noise) is not biased in any particular direction, and
many tow level replicates are available, the bias may be averaged
out and the direction and size of effects (i.e. signal) could still be
estimated. One advantage of a hierarchical size distribution mod-
elling approach is that it allows for easy indexation of the models
such that a tow, station (an area within a survey where multiple
tows are taken) and entire survey level estimate of z̄ and ḡ can be
gained from a single modelling exercise. Estimating vital rates fol-
lowing a hierarchy of scales in such a way to address issues of bias
would greatly benefit from the inclusion of a framework, like that
suggested by Helbig and Pepin (1998), incorporating theoretical ex-
pressions evaluating the quality of spatial sampling based on physi-
cal oceanographic processes. Already existing databases containing
size data comprised of extensive sampling across a seascape (e.g. the
California Cooperative Oceanic Fisheries Investigations (CalCOFI)
sampling of the California current since 1951; Bograd et al., 2003),
may provide the best avenue for this exploration.
A novel approach for estimating growth and mortality of fish larvae
Conclusion
This study demonstrates the potential for available techniques that
remain novel in fisheries science to improve upon our ability to
empirically determine rates of population dynamics. Achieving ac-
curate measurements of vital rates that are fundamental to under-
standing population dynamics in highly variable ecosystems is es-
sential if we hope to someday accurately predict success of the lar-
val stages from seascape conditions, and thereby reduce a great in-
hibitor to predicting cohort success in fish. By adopting an approach
that models abundance as a continuous measure with respect to age
or size, and removes the need to bin data, we have shown how the
accuracy and precision of estimates can be enhanced. Furthermore,
we have shown that substituting the underlying age distribution of
catch-curves for a size distribution can result in models that not
only have the advantage of treating growth and mortality within a
single framework, thereby conserving uncertainty between the two
rates, but also produces more accurate and precise estimates. While
the necessary future work mentioned above will improve our con-
fidence in, and applicability of, these models, we encourage fish-
eries scientists to consider these methods as another tool to improve
upon our collective understanding of larval success.
Data availability
The data underlying this article will be shared on reasonable request
to the corresponding author.
Author contributions
CH and DSF designed the analysis, CH performed the analysis and
led the writing of the manuscript. All authors helped conceive ideas,
contributed critically to the drafts, and gave final approval for pub-
lication.
Supplementary Data
Supplementary material is available at the ICESJMS online version
of the manuscript.
Acknowledgements
CH is funded by an Australian Government Research Training
Program Scholarship. DSF is funded by ARC Future fellowship
(FT160100113). We thank Jian Yen for useful discussions, and two
anonymous reviewers for their helpful comments.
References
Ailloud, L. E., and Hoenig, J. M. 2019. A general theory of age-length
keys: combining the forward and inverse keys to estimate age com-
position from incomplete data. ICES Journal of Marine Science 76:
1515–1523.
Anderson, J. T. 1988. A review of size dependent survival during pre-
recruit stages of fishes in relation to recruitment. Journal of North-
west Atlantic Fishery Science 8: 55–66.
Bailey, K. M., Brodeur, R. D., and Hollowed, A. B. 1996. Cohort sur-
vival patterns of walleye pollock, Theragra chalcogramma, in She-
likof Strait, Alaska: a critical factor analysis. Fisheries Oceanogra-
phy, 5: 179–188.
Bailey, K. M., and Houde, E. D. 1989. Predation on eggs and larvae of
marine fishes and the recruitment problem. Advances in marine bi-
ology 25: 1–83.

Bannister, R. C. A., Harding, D., and Lockwood, S. J. 1974. Larval mor-
tality and subsequent year-class strength in the plaice (Pleuronectes
platessa L.). In: The Early Life History of Fish, pp. 21–37. Ed. by
Blaxter, J. H. S. Springer, Berlin, Heidelberg.
Bengtson, D. A., Barkman, R. C., and Berry, W. J. 1987. Relationships
between maternal size, egg diameter, time of spawning season, tem-
perature, and length at hatch of Atlantic silverside, Menidia menidia.
Journal of Fish Biology 31: 697–704.
Beverton, R. J. H., and Holt, S. J. 1957. On the Dynamics of Exploited
Fish Populations. Ministry of Agriculture and Fisheries, London.
Beyer, J. E. 1989. Recruitment stability and survival: simple size-specific
theory with examples from the early life dynamics of marine fish.
Dana 7: 45–147.
Blanchard, J. L., Heneghan, R. F., Everett, J. D., Trebilco, R., and Richard-
son, A. J. 2017. From bacteria to whales: using functional size spec-
Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022
tra to model marine ecosystems. Trends in Ecology & Evolution 32:
174–186.
Bograd, S. J., Checkley, D. A., and Wooster, W. S. 2003. CalCOFI: a half
century of physical, chemical, and biological research in the Cali-
fornia Current System. Deep Sea Research Part II: Topical Studies
in Oceanography 50: 2349–2353.
Chambers, R. C., Leggett, W. C., and Brown, J. A. 1988. Variation in and
among early life history traits of laboratory-reared winter flounder
Pseudopleuronectes americanus. Marine Ecology Progress Series 47:
1–15.
Chapman, D. G., and Robson, D. S. 1960. The analysis of a catch curve.
Biometrics 16: 354–368.
Coggins, L. G. Jr, Gwinn, D. C., and Allen, M. S. 2013. Evaluation of
age–length key sample sizes required to estimate fish total mortal-
ity and growth. Transactions of the American Fisheries Society 142:
832–840.
Coomes, D. A., Duncan, R. P., Allen, R. B., and Truscott, J. 2003. Dis-
turbances prevent stem size-density distributions in natural forests
from following scaling relationships. Ecology Letters 6: 980–989.
Cushing, D. H. 1974. The possible density-dependence of larval mor-
tality and adult mortality in fishes. In: The Early Life History of Fish,
pp. 103–111. Ed. by Blaxter, J. H. S. Springer, Berlin, Heidelberg.
Dannevig, H. C. 1907. On some peculiarities in our coastal winds and
their influence upon the abundance of fish in inshore waters. Journal
of the Royal Society of NSW 41: 27–15.
Datta, S., Delius, G. W., Law, R., and Plank, M. J. 2011. A stability anal-
ysis of the power-law steady state of marine size spectra. Journal of
Mathematical Biology 63: 779–799.
de Roos, A. M. 1997. A gentle introduction to physiologically struc-
tured population models. In: Structured-Population Models in Ma-
rine, Terrestrial, and Freshwater systems. pp. 119–204, Ed. by Tul-
japurkar, S. and Caswell, H. Springer, Boston, MA.
Ebert, T. A., Schroeter, S. C., and Dixon, J. D. 1993. Inferring demo-
graphic processes from size-frequency distributions: effect of pulsed
recruitment on simple models. Fishery Bulletin 91: 237–243.
Fontes, J., Santos, R. S., Afonso, P., and Caselle, J. E. 2011. Larval growth,
size, stage duration and recruitment success of a temperate reef fish.
Journal of Sea Research 65: 1–7.
Fry, F. E. J. 1971. The effect of environmental factors on the physiology
of fish. Fish Physiology 1–98.
Garrido, S., Ben-Hamadou, R., Santos, A.M.P., Ferreira, S., Teodósio,
M.A., Cotano, U., Irigoien, X. et al. 2015. Born small, die young:
intrinsic, size-selective mortality in marine larval fish. Scientific re-
ports 5: 1–10.
Gelman, A., Lee, D., and Guo, J. 2015. Stan: a probabilistic program-
ming language for Bayesian inference and optimization. Journal of
Educational and Behavioral Statistics 40: 530–543.
Gompertz, B. 1825. XXIV. On the nature of the function expressive of
the law of human mortality, and on a new mode of determining
the value of life contingencies. In a letter to Francis Baily, Esq. F. R.
S. andc. Philosophical Transactions of the Royal Society of London
115: 513–583.
Govoni, J. J. 2005. Fisheries oceanography and the ecology of early life
histories of fishes: a perspective over fifty years. Scientia Marina 69:
125–137.

Hare, J. A. 2014. The future of fisheries oceanography lies in the pursuit
of multiple hypotheses. ICES Journal of Marine Science 71: 2343–
2356.
Helbig, J. A., and Pepin, P. 1998. Partitioning the influence of physi-
cal processes on the estimation of ichthyoplankton mortality rates.
I. Theory. Canadian Journal of Fisheries and Aquatic Sciences 55:
2189–2205.
Heneghan, R. F., Everett, J. D., Blanchard, J. L., and Richardson, A. J.
2016. Zooplankton are not fish: improving zooplankton realism in
size-spectrum models mediates energy transfer in food webs. Fron-
tiers in Marine Science 3: 201.
Hinchliffe, C., Smith, J. A., Everett, J. D., Falster, D. S., Lara-Lopez,
A., Miskiewicz, A. G., Richardson, A. J. et al. 2021. Modelling the
distribution of larval fish in a western boundary current using a
multi-voyage database. Reviews in Fish Biology and Fisheries 31:
399–415.
Hjort, J. 1914. Fluctuations in the great fisheries of Northern Eu-
rope viewed in the light of biological research. Rapports et Procès-
Verbaux des Réunions, Conseil International pour l’Exploration de
la Mer 20: 1–13.
Houde, E. D. 1997. Patterns and trends in larval-stage growth and mor-
tality of teleost fish. Journal of Fish Biology 51: 52–83.
Houde, E. D. 2002. Mortality. In: Fishery Science: The Unique Contri-
butions of Early Life Stages, pp. 64–87. Ed. by Fuiman, L. A. and
Werner, R. G. John Wiley & Sons, New York City, NY.
Houde, ED. 1987. Fish early life dynamics and recruitment variability.
American Fisheries Society Symposium Series 2: 17–29.
Jordaan, A., Hayhurst, S. E., and Kling, L. J. 2006. The influence of tem-
perature on the stage at hatch of laboratory reared Gadus morhua
and implications for comparisons of length and morphology. Jour-
nal of Fish Biology 68: 7–24.
Kohyama, T., Suzuki, E., Partomihardjo, T., Yamada, T., and Kubo, T.
2003. Tree species differentiation in growth, recruitment and allom-
etry in relation to maximum height in a Bornean mixed dipterocarp
forest. Journal of Ecology 91: 797–806.
Law, R., and Plank, M. J. 2018. Balanced harvesting could reduce
fisheries-induced evolution. Fish and Fisheries 19: 1078–1091.
Law, R., Plank, M. J., James, A., and Blanchard, J. L. 2009. Size-spectra
dynamics from stochastic predation and growth of individuals.
Ecology 90: 802–811.
Llanos-Rivera, A., and Castro, L. R. 2004. Latitudinal and seasonal egg-
size variation of the anchoveta (Engraulis ringens) off the Chilean
coast. Fishery Bulletin 102: 207–212.
Maceina, M. J. 1997. Simple application of using residuals from catch-
curve regressions to assess year-class strength in fish. Fisheries Re-
search 32: 115–121.
Maceina, M. J., and Bettoli, P. W. 1998. Variation in largemouth bass
recruitment in four mainstream impoundments of the Tennessee
River. North American Journal of Fisheries Management 18: 998–
1003.
Mommsen, T. P. 2001. Paradigms of growth in fish. Comparative Bio-
chemistry and Physiology Part B: Biochemistry and Molecular Bi-
ology 129: 207–219.
Morse, W. W. 1989. Catchability, growth, and mortality of larval fishes.
Fishery Bulletin 87: 417–446.
Mullaney, T. J., and Suthers, I. M. 2013. Entrainment and reten-
tion of the coastal larval fish assemblage by a short-lived, subme-
soscale, frontal eddy of the East Australian Current. Limnology and
Oceanography 58: 1546–1556.
Muller-Landau, H.C., Condit, R.S., Harms, K.E., Marks, C.O., Thomas,
S.C., Bunyavejchewin, S., Chuyong, G. et al. 2006. Comparing trop-
ical forest tree size distributions with the predictions of metabolic
ecology and equilibrium models. Ecology Letters 9: 589–602.
Neill, W. H., Miller, J. M., Van Der Veer, H. W., and Winemiller, K.
O. 1994. Ecophysiology of marine fish recruitment: a conceptual
framework for understanding interannual variability. Netherlands
Journal of Sea Research 32: 135–152.
Nelson, G. A. 2019. Bias in common catch-curve methods applied to age
frequency data from fish surveys. ICES Journal of Marine Science
76: 2090–2101.
C. Hinchliffe et al.
Nelson, G. A. 2019b. fishmethods: Fishery science methods and models.
R package version 1.11.
Odum, H. T., and Odum, E. P. 1955. Trophic structure and productivity
of a windward coral reef community on Eniwetok Atoll. Ecological
Monographs 25: 291–320.
Pepin, P. 1991. Effect of temperature and size on development, mortal-
ity, and survival rates of the pelagic early life history stages of marine
fish. Canadian Journal of Fisheries and Aquatic Sciences 48: 503–
518.
Pepin, P. 2004. Early life history studies of prey-predator interactions:
quantifying the stochastic individual responses to environmental
variability. Canadian Journal of Fisheries and Aquatic Sciences 61:
659–671.
Pepin, P. 2016. Death from near and far: alternate perspectives on size-
dependent mortality in larval fish. ICES Journal of Marine Science:
Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022
Journal du Conseil 73: 196–203.
Pepin, P. 2016. Reconsidering the impossible — linking environmen-
tal drivers to growth, mortality, and recruitment of fish. Canadian
Journal of Fisheries and Aquatic Sciences 73: 205–215.
Pepin, P., Robert, D., Bouchard, C., Dower, J.F., Falardeau, M., Fortier,
L., Jenkins, G.P. et al. 2014. Once upon a larva: revisiting the rela-
tionship between feeding success and growth in fish larvae. ICES
Journal of Marine Science 72: 359–373.
Polovina, J. J. 1984. Model of a coral reef ecosystem. Coral reefs 3: 1–11.
Quiñonez-Velázquez, C., Nevarez-Martı´nez, M. O., and Gluyas-
Millán, M. G. 2000. Growth and hatching dates of juvenile pacific
sardine Sardinops caeruleus in the Gulf of California. Fisheries Re-
search 48: 99–106.
R Core Team 2019. R: A Language and Environment for Statistical
Computing. R Foundation for Statistical Computing, Vienna.
Raya, V., Salat, J., and Sabatés, A. 2020. The box-balance model: a new
tool to assess fish larval survival, applied to field data on two small
pelagic fish. Marine Ecology Progress Series 650: 289–308.
Ricker, W. E. 1975. Computation and interpretation of biological statis-
tics of fish populations. Bulletin of the Fisheries Research Board of
Canada 191: 1–382.
Rose, G. A., and Rowe, S. 2020. Evidence of near year-around spawning
in Atlantic cod off southern Newfoundland: implications for man-
agement. Canadian Journal of Fisheries and Aquatic Sciences 77:
1969–1976.
Rutherford, E. S., Houde, E. D., and Nyman, R. M. 1997. Relationship
of larval-stage growth and mortality to recruitment of striped bass,
Morone saxatilis, in Chesapeake Bay. Estuaries 20: 174–198.
Saltelli, A., Tarantola, S., Campolongo, F., and Ratto, M. 2002. Sensitivity
analysis in Practice: A Guide to Assessing Scientific Models. John
Wiley & Sons, New York City, NY.
Sassa, C., and Takahashi, M. 2018. Comparative larval growth and mor-
tality of mesopelagic fishes and their predatory impact on zooplank-
ton in the Kuroshio region. Deep Sea Research Part I: Oceano-
graphic Research Papers 131: 121–132.
Sassa, C., Takahashi, M., Nishiuchi, K., and Tsukamoto, Y. 2014. Dis-
tribution, growth and mortality of larval jack mackerel Trachurus
japonicus in the southern East China Sea in relation to oceano-
graphic conditions. Journal of Plankton Research 36: 542–556.
Secor, D. H., and Houde, E. D. 1995. Temperature effects on the tim-
ing of striped bass egg production, larval viability, and recruitment
potential in the Patuxent River (Chesapeake Bay). Estuaries 18: 527–
544.
Sexton, S. C., Ward, T. M., Stewart, J., Swadling, K. M., and Huveneers,
C. 2019. Spawning patterns provide further evidence for multiple
stocks of sardine (Sardinops sagax) off eastern Australia. Fisheries
Oceanography 28: 18–32.
Shepherd, J. G., and Cushing, D. H. 1980. A mechanism for
density-dependent survival of larval fish as the basis of a stock-
recruitment relationship. ICES Journal of Marine Science 39:
160–167.
Sinko, J. W., and Streifer, W. 1967. A new model for age-size structure
of a population. Ecology 48: 910–918.
Smith, B. D., Botsford, L. W., and Wing, S. R. 1998. Estimation of growth
and mortality parameters from size frequency distributions lacking
A novel approach for estimating growth and mortality of fish larvae
age patterns: the red sea urchin (Strongylocentrotus franciscanus) as
an example. Canadian Journal of Fisheries and Aquatic Sciences 55:
1236–1247.
Smith, J. A., Eyre, B. D., Rosentreter, J. A., and Taylor, M. D.
2019. Modelling estuarine stocking density for crustaceans us-
ing net ecosystem metabolism. Bulletin of Marine Science 95:
217–238.
Stan Development Team 2019. RStan: the R interface to Stan. R package
version 2.19.1.
Stevenson, D. K., and Campana, S. E. 1992. Otolith Microstructure Ex-
amination and Analysis. Department of Fisheries and Oceans. Ot-
tawa, Canada.
Stige, L.C., Rogers, L.A., Neuheime, A.B., Hunsicker, M.E., Yaragina,
N.A., Ottersen, G., Ciannelli, L. et al. 2019. Density- and size-
dependent mortality in fish early life stages. Fish and Fisheries 20:
962–976.
Takasuka, A., Aoki, I., and Mitani, I. 2003. Evidence of growth-selective
predation on larval Japanese anchovy Engraulis japonicus in Sagami
Bay. Marine Ecology Progress Series 252: 223–238.
Takasuka, A., Aoki, I., and Mitani, I. 2004. Three synergistic growth-
related mechanisms in the short-term survival of larval Japanese an-
chovy Engraulis japonicus in Sagami Bay. Marine Ecology Progress
Series 270: 217–228.
Takasuka, A., Sakai, A., and Aoki, I. 2017. Dynamics of growth-based
survival mechanisms in Japanese anchovy (Engraulis japonicus) lar-
vae. Canadian Journal of Fisheries and Aquatic Sciences 74: 812–
823.

Tian, T., Fiksen, Ø., and Folkvord, A. 2007. Estimating larval fish growth
under size-dependent mortality: a numerical analysis of bias. Cana-
dian Journal of Fisheries and Aquatic Sciences 64: 554–562.
Vanalderweireldt, L., Winkler, G., Mingelbier, M., and Sirois, P. 2019.
Early growth, mortality, and partial migration of striped bass (Mo-
rone saxatilis) larvae and juveniles in the St. Lawrence estuary,
Canada. ICES Journal of Marine Science 76: 2235–2246.
Vasbinder, K., and Ainsworth, C. 2020. Early life history growth in fish
reflects consumption-mortality tradeoffs. Fisheries Research 227:
105538.
von Bertalanffy, L. 1938. A quantitative theory of organic growth (in-
quiries on growth laws. II). Human biology 10: 181–213.
Von Foerster, H. 1959. Some remarks on changing populations. In: The
Kinetics of Cellular Proliferation, pp. 382–407. Ed. by Stohlman, F.
Grune and Stratton, New York, NY.
Downloaded from https://academic.oup.com/icesjms/article/78/8/2684/6364353 by guest on 03 March 2022
Ward, E. J. 2008. A review and comparison of four commonly used
Bayesian and maximum likelihood model selection tools. Ecolog-
ical Modelling 211: 1–10.
Watanabe, Y., Oozeki, Y., and Kitagawa, D. 1997. Larval parameters de-
termining preschooling juvenile production of Pacific saury (Colo-
labis saira) in the northwestern Pacific. Canadian Journal of Fish-
eries and Aquatic Sciences 54: 1067–1076,
Westrheim, S. J., and Ricker, W. E. 1978. Bias in using an age–length
key to estimate age-frequency distributions. Journal of the Fisheries
Research Board of Canada 35: 184–189.
Wikle, C. K. 2003. Hierarchical Bayesian models for predicting the
spread of ecological processes. Ecology 84: 1382–1394.
Handling Editor: David Secor