BULLETIN OF MARINE SCIENCE. 60(3): 1129-1157.
1997
SIZE-SELECTIVE MORTALITY IN THE JUVENILE
STAGE OF TELEOST FISHES: A REVIEW
Susan M. Sogard
ABSTRACT
Individual variability in body size provides a template for selective mortality processes
during early life history stages of teleost fishes. This size variability has generated the logically intuitive hypothesis that larger or faster growing members of a cohort gain a survival
advantage over smaller conspecifics via enhanced resistance to starvation, decreased vulnerability to predators, and better tolerance of environmental extremes. This review evaluates
field and laboratory studies that have examined size-based differences in survival, with emphasis on the juvenile stage of teleost fishes. The results in general support the "bigger is
better" hypothesis, although a number of examples indicate non-selective mortality with no
obvious size advantages. The reverse pattern, with enhanced survival of smaller individuals,
is rare with the notable exception of bird predation. Major size-selective processes during
the juvenile stage include overwinter mortality for temperate species, associated with either
starvation or intolerance of physical extremes by smaller members of the young-of-the-year
cohort, and predation, with smaller fish more susceptible to successful capture by predators.
Most studies examining these processes have used indirect methods to evaluate size-selective
mortality, with interpretation of results dependent on several critical assumptions. For methods that track size distributions over time, unbiased samples collected from the same population are critical, and changes in size distributions associated with mortality must be distinguished from changes due to individual growth. The latter requirement can be met with the
direct, "characteristics of survivors" method, but few studies have used this approach. Experimental methods isolating specific mechanisms of size-specific mortality must appropriately represent the natural context of environmental factors. Specific predator/prey combinations, for example, can elucidate size-based prey preferences but may be irrelevant compared to the natural, multi-species predator field. The composition of the predator field and
its correspondence to size-spectrum theory is crucial to the probability of size-selective predation as a cohort progresses through the juvenile stage. Distinction of selection on body
size vs. selection on growth rate has received little attention. However, a number of physiological constraints and ecological trade-offs can place restrictions on growth rates and apparently override the advantages of large body size. Identifying the major sources of mortality
and how they operate in the juvenile stage has valuable applications in understanding population dynamics and recruitment variability.
High mortality rates during the early life stages of most teleost fishes ensure
that the likelihood of survival to adulthood for any particular individual is extremely low. There is currently considerable interest in determining which members of a cohort or year class survive and why. The basic question is whether
mortality acts indiscriminately, with all individuals having the same chance of
being removed from the population; randomly, with inconsistent or unpredictable
probability of mortality; or non-randomly, with particular traits reducing the relative risk of mortality. If mortality is either indiscriminate or random, careful consideration of individual variability in phenotypic traits will be of little utility in
tracking the dynamics of a fish population. In contrast, if particular behavioral,
morphological or physiological traits enhance the survival probability of certain
individuals in the same local population, we may be able to use an assessment of
such traits to predict the future of a particular cohort (Crowder et al., 1992).
A current paradigm is that body size (and associated growth rate) during the
larval and juvenile stages is a major determinant of survival. Anderson (1988)
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1997
succinctly outlines the basic framework of size-selective theory and the growthmortality hypothesis. Because mortality rates generally decrease with increasing
body size (Peterson and Wroblewski, 1984; Houde, 1987; Miller et al., 1988),
individuals that grow more rapidly should spend less time in the more vulnerable
size classes. The assumption that rapid growth enhances survival has become
pervasive in the literature and forms the underlying basis for studies examining
growth processes and variability (Sogard, 1992; 1994). Modeling studies examining recruitment variability often include the higher survival of faster growing!
larger individuals as a crucial but untested assumption (Gutreuter and Anderson,
1985). The logical appeal of larger individuals being better able to escape from
predators, resist starvation, and tolerate physiological extremes compared to
smaller conspecifics has presumably increased the acceptance of the 'bigger is
better' hypothesis without careful evaluation of the evidence.
In this review I consider body size to be the trait on which selective mortality
operates. Obviously body size is intimately integrated with growth rate, and a
number of factors correlated with growth rate or body size can potentially influence mortality. For example, slowly growing individuals are likely to be in poorer
condition and to take greater behavioral risks compared to faster growing fish;
vulnerability to predators may differ for two individuals of the same length but
different condition. For juvenile stages, the effects of these correlates of body
size on probability of mortality have received little attention. Hare and Cowen
(in press), however, found a close correlation of growth rate with size-at-age for
larval and juvenile bluefish (Pomatomus sa/tatrix), suggesting that the two traits
cannot be distinguished in their effects on selective mortality. The studies examined in this review have generally used body size as the metric of comparison
and did not test for selection directly on growth rate.
The review focuses on the juvenile stage of teleost fishes. Evaluations of
size-based processes in the larval stage have been conducted by Miller et al.
(1988), Bailey and Houde (1989), Pepin (1993) and others, and will not be further
elaborated here. I pose a number of questions related to the general topic of sizeselective mortality and attempt to address the major factors that generate and
interact with size-based processes to configure a year class during its passage
through the juvenile stage. My goal is not only to evaluate the validity of the
'bigger is better' hypothesis, but also point out the conditions that temper or
reverse any advantages of large size.
Assessment of selective mortality is typically based on a cohort (individuals of
a single year class) of young-of-the-year juveniles occurring in the same location.
A cohort may be comprised of several sub-cohorts arising from different spawning
pulses. Obviously mortality operates at the scale of the individual, but any sizebased probability of mortality is a function of both the fish's absolute size and its
relative size compared to other members of the young-of-the-year population.
Absolute size is particularly influential in threshold effects, where fish attaining
a particular size are no longer vulnerable to certain mortality agents. Rapid growth
in this situation allows an individual to quickly reach a size refuge (the stage
duration hypothesis, Houde, 1987). Relative size is important for factors like
intracohort cannibalism and for predators making a choice among potential prey.
Rapid growth in this situation allows an individual to alter its position in the size
hierarchy, with the risk of mortality potentially shifted to smaller sized conspecifics. This review will focus on the individual's risk of mortality under different
conditions. The cumulative effects of individual mortalities are reflected in the
success of a sub-cohort and of the year class.
SOGARD: SIZE-SELECTIVE MORTALITY IN JUVENILE FISHES
1131
Why is the Juvenile Stage Important?
Within-cohort size-selective mortality can occur as early as the egg stage (Rijnsdorp and Jaworski, 1990), and much prior research has focused on the larval
stage, with conflicting evidence both supporting and refuting size-based processes
(Bailey and Houde, 1989; Laidig et al., 1991; Litvak and Leggett, 1992; Cowan
and Houde, 1992; Pepin et al., 1992; Brown and Bailey, 1992). Non-random
mortality based on size is potentially more evident and more likely in the juvenile
stage than in the larval stage for a number of reasons. 1) For post-metamorphic
juveniles, development is generally complete, in contrast to the larval stage, when
changes in morphology, pigmentation, and behavior can increase encounter rates
with predators and modify vulnerability curves (Fuiman, 1989). Juanes and Conover (1994a) provide convincing evidence that, as juvenile size increases, encounter rates vary little and are insignificant compared to decreasing capture success by predators; thus, size can be examined independently of development for
its role in susceptibility to predators. 2) Indiscriminate mortality processes that
are independent of fish size and density are more likely to impact larval survival
than juvenile survival. Advection and transport of larvae away from suitable nursery areas presumably affects all size classes. Physical extremes such as cold temperatures can eradicate early-spawned sub-cohorts of larvae (Rutherford and Houde,
1995), obviously outweighing any size advantages relative to later sub-cohorts.
The negative impact of storms, evident for larval stages (Peterman and Bradford,
1987; Maillet and Checkley, 1991; Bailey and Macklin, 1994), may be tempered
for juveniles. 3) Size variation, providing a template for size-selective processes,
typically increases during the juvenile stage relative to the larval stage. Initial
larval size is constrained by egg size, with subsequent growth variability resulting
in an increase in size variance as the mean size increases.
In addition to the greater likelihood of detectable size-dependent mortality in
the juvenile stage than in the larval stage, a number of recent studies suggest that
the early juvenile period plays a greater role in population regulation and determination of year class strength than previously thought (Sissenwine, 1984; Peterman et aI., 1988; Hixon, 1991; Bailey and Spring, 1992; Bradford, 1992; Bailey, 1994; Bailey et al., 1996; Campana, 1996). Survivors to the juvenile stage
have greater reproductive value (R.,) than larvae but still experience sufficient
mortality to significantly modify population size. Thus, understanding the operation of size-dependent mortality processes during the juvenile stage has valuable
applications in broader questions concerning recruitment variability, the occurrence of exceptional year classes, and population growth rate.
What Conditions and Mechanisms Induce
Size-selective Mortality?
The occurrence of size-selective mortality requires three conditions: 1) size
variation in the population, 2) non-random mortality, and 3) relatively high mortality. Variation in size could arise from different spawning dates, genetic differences in growth capacity, or individual differences in food consumption. YOY
cohorts of teleost fishes typically develop substantial size variation by the juvenile
stage. Non-random mortality based on size is the critical component needing
thorough testing before size-selective theory can be applied to understanding population dynamics or recruitment variability. Finally, sufficient mortality must occur to allow selection. Non-random but low mortality may not detectably modify
the size distribution of survivors.
Selective mortality acting on a size distribution of prey can be directional,
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BULLETIN OF MARINE SCIENCE, VOL. 60, NO.3,
1997
primarily removing one tail of the distribution; stabilizing, with both tails removed; or disruptive, with large and small individuals favored and intermediate
sizes removed. As individuals grow and environmental conditions change over
time, the form and direction of selective mortality can vary. Thus, patterns of
size-selective mortality are not static, and the relative vulnerability of an individual fish can vary as it grows, Miller (in press) provides further detail on modes
of selection, potential shifts in selection over time, and the detectability of different types of selection. The studies examined in this review primarily focused
on directional selection; the extent to which other types of selection occur is
unknown and possibly difficult to detect (Miller, in press).
Assessment of selection has used a number of techniques aimed at both elucidating potential mechanisms of size-based mortality and documenting differences in pre- and post-selection size distributions. The former approach examines
specific components of the mortality process, such as the vulnerability of a particular size class of prey to particular predators, whereas the latter approach attempts to verify a change in the population over time. Different conclusions may
arise from the two approaches if a cohort is subject to multiple sources of mortality during a specific time interval.
Given that mortality rates vary by fish size, other factors may further influence
the susceptibility of a particular individual. One is the maintenance of relative
size differences among the individuals in a population. If, for example, mortality
is continually biased toward smaller members of a cohort and size differences are
maintained over time, smaller fish have a distinctly lower probability of survival
than larger fish throughout the juvenile stage. In contrast, if growth trajectories
of individuals are not parallel, an individual may experience varying degrees of
vulnerability to size-selective mortality as it moves through the juvenile stage.
The studies that have directly addressed this question have generally found that
relative size positions are maintained, at least within the juvenile stage (Hager
and Noble, 1976; West and Larkin, 1987; Tsukamoto et aI., 1989; Johnson ,md
Margenau, 1993; Thpper and Boutilier, 1995a). Contrasting results, with crossings
of individual growth trajectories, have been reported by Otten} (1992) and Sabo
and Orth (1995).
Compensatory growth can disrupt the maintenance of size differences and result
in decreased variability in size over time. Many species are able to increase their
growth rate following a period of poor growth (Dobson and Holmes, 1984; Bertram et aI., 1993; Jobling et al., 1994) or low dissolved oxygen (Bejda et aI.,
1992), allowing them to catch up in size to individuals that have been growing
at a steady rate.
Size-selective mortality can in itself reduce the degree of size variation in a
population, decreasing the likelihood of further selection. Examples are evident
from laboratory studies documenting the cessation of intracohort cannibalism
when all small fish have been removed from the population (van Darnme et aI.,
1989). Thus, selective mortality may operate only during an interim period during
the growth of the cohort.
In contrast to the narrowing of size ranges by processes of size-selective mortality and growth compensation, growth depensation produces a broader size distribution, allowing intracohort cannibalism for piscivores and increasing the likelihood of other size-dependent losses from the population. For example, during
their initial marine residence, larger juvenile chum salmon (Oncorhynchus keta)
differed in length from smaller fish by only about 5% and their relative survival
was higher by a factor of 2.8. Later, when mean lengths differed by 19% due to
variable growth rates, the survival of larger fish was greater by a factor of 36.6
SOGARD: SIZE-SELECTIVE MORTALITY IN JUVENILE ASHES
1133
(Healey, 1982). The onset of piscivory by some individuals can elicit a dramatic
increase in size variability, with piscivores rapidly outgrowing non-piscivorous
conspecifics (Buijse and Houthuijzen, 1992; Juanes and Conover, 1994b, Fitzhugh
and Rice, 1995). Growth depensation is often induced through behavioral interactions, with dominant individuals excluding subordinate individuals from food
resources (Magnuson, 1962; Koebele, 1985).
A number of mechanisms can induce size-selective patterns of mortality. Much
prior research has focused on predators as the agent of mortality. Size-biased
consumption can be attributed to gape limitation, behavioral selection by the predator, or variation in escape capability with prey size. Under size-spectrum theory
(Sheldon et al., 1977; Platt and Denman, 1978), the abundance of predators should
progressively decrease as predator size increases; thus, smaller prey will continually have a larger suite of potential predators compared to larger prey (Houde,
in press). In addition, despite the predictions of optimal foraging theory, piscivores
typically continue to include small prey in their diet, simply expanding the range
of prey sizes as they grow (Juanes and Conover, 1995; Ellis and Gibson, 1995).
This aspect was clearly elucidated by Juanes (1994), who analyzed 32 studies of
piscivorous fishes and found that predators consistently consumed prey smaller
than the optimal size predicted by theory. For gape-limited predators, the opposing
effect of inclusion of prey larger than the mouth size is not physically possible.
Thus, size refuges attained through growth should be more reliable for prey fish
than refuges dependent on behavioral preferences of predators.
Overwinter mortality in temperate species can be size-selective, with low energy reserves of small fish more likely to result in starvation (Oliver et al., 1979;
Henderson et al., 1988). Extremes in physical factors such as temperature, dissolved oxygen, or salinity potentially also cause size-selective mortality, by means
of varying physiological tolerance (Wedemeyer et al., 1980; Johnson and Evans,
1996). Finally, different size classes may vary in their susceptibility to disease.
West and Larkin (1987) suggested that higher parasite infestation in smaller sockeye salmon (Oncorhynchus nerka) juveniles is potentially responsible for their
higher mortality rates relative to larger sockeye.
What Methods and Evidence Exist for Evaluating
Size-selective Mortality?
A number of methods have been used to examine size-selective processes. In
the following sections I examine the evidence for non-random mortality in juvenile fishes, based on the results of pertinent studies in each method category.
Table 1 summarizes these studies, with size-selective mortality classified as absent, negative (higher mortality of smaller individuals in the population), or positive (higher mortality of larger individuals in the population).
Interannual Correlative Comparisons.-Correlations of mean YOY size with subsequent population abundance can address the relation of size to survival on an
interannual basis. Positive correlations of mean juvenile size with abundance at a
later date have been found across an extended time series for brook trout (Salvelinus fontinalis, Hunt, 1969), yellow perch (Perea jlavescens, Nielsen, 1980),
pikeperch (Stizostedion lucioperca, Buijse and Houthuijzen, 1992), Atlantic cod
(Gadus morhua, Campana, 1996), and sockeye salmon (Foerster, 1954). No relation, however, was found for sockeye populations examined by Hyatt and Stockner (1985) or Henderson and Cass (1991).
Use of the correlative method is severely limited by the difficulty of separating
size-selective components of mortality from other factors that cause interannual
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BULLETIN OF MARINE SCIENCE, VOL. 60, NO.3.
1997
variability in survivorship. Size-biased mortality could occur within a year class
regardless of interannual correlations between size and year class strength. Confounding factors across years could either falsely support size-selective mortality
or mask selective processes within a year. For example, Hunt's (1969) analysis
of brook trout indicated that survival was positively correlated with winter temperature. Thus, warmer temperatures could both increase mean size via faster
growth and promote higher survival of all individuals in the year class, regardless
of size. To address this argument, Hunt used fin clips to mark large and small
size classes in one year class; collections in the spring indicated a 60% survival
rate for the larger fish and only 52% survival of the smaller fish. This 8% difference in survival was statistically significant (X2 test). Similarly, when size distributions within a year class were examined in sockeye salmon, Henderson and
Cass (1991) did find a correspondence of smolt size with survival. Analysis of
survival within a year class can provide valuable support for size-selective mortality suggested by correlative relationships across years.
Experimental Comparisons of Predation Rates.-Direct
tests of predator behavior
provide a valuable means of verifying non-random selectivity of prey. For example, gape limitation appears to be the primary factor causing coho salmon
(Oncorhynchus kisutch) to forage selectively on small size classes of pink (Oncorhynchus gorbuscha, Parker, 1971) and chum salmon (Hargreaves and LeBrasseur, 1986) in mesocosm cages. Juvenile pink salmon grow at a faster rate
(1.4% d-I) than their coho predators (0.7% d-1), allowing them to attain a size
refuge (Parker, 1971). Intracohort cannibalism is particularly sensitive to gape
limitation effects. Due to allometric growth of body depth and mouth height, there
is a limited window in which size differences are sufficient to allow cannibalism
in yay carp (Cyprinus carpio, van Damme et al., 1989), Atlantic cod (attera
and Folkvord, 1993), and walleye pollock (Theragra chalcogramma. Sogard and
Olla, 1994). Larger fish must grow at a faster rate to continue being able to
cannibalize smaller members of their cohort (Fig. 1).
In yellow perch, behavioral preferences appeared to be more important than
gape limitation in causing selective mortality on small prey fish (Post and Evans,
1989a, Paszkowski and Tonn, 1994). Large prey were consumed, but apparently
only if all smaller prey had already been eaten or if only large prey were offered.
In contrast, Juanes and Conover (1994a) found that juvenile bluefish attacked all
prey sizes encountered, but capture success was strongly size-dependent, resulting
in clear survival advantages for large prey.
For juvenile flatfish, the development of effective escape tactics allows large
individuals to avoid predation by crangonid shrimp. Following metamorphosis
and settlement to benthic habitats, yay flatfish are highly vulnerable to shrimp
predators. Laboratory experiments with juvenile plaice (Pleuronectes platessa,
van del' Veer and Bergman, 1987), Japanese flounder (Paralichthys olivaceus,
Seikai et al., 1993), and winter flounder (Pleuronectes americanus, Witting and
Able, 1993) demonstrate a clear size refuge attained with growth; for winter
flounder the probability of consumption by Crangon septemspinosa declines from
60% to 0% as flounder length increases from 9 to 20 mm (Witting and Able,
1993).
In manipulative field experiments, Carr and Hixon (1995) set up populations
of juvenile reef fish on patch reefs, then removed piscivorous fishes from half of
the reefs. Initial size distributions of prey were similar for control and predator
removal treatments. At the end of the 27-d experiment, densities of blue chromis
(Chromis cyanea) were significantly reduced in the presence of predators, and
SOGARD: SIZE-SELECfIVE
MORTALITY IN JUVENILE FISHES
1135
2.5
s
E
2
E
..•..•.•
Q)
.•...
~ 1.5
.c
~
0,
~
1
o
.•...
ro
"0
~ 0.5
0...
o
0.0
0.5
1.0
1.5
2.0
Prey growth rate (mm/d)
2.5
Figure 1. Relationship
between predator growth rate and prey growth rate that demarcates gapelimited cannibalism in juvenile walleye pollock (shaded area). Values outside this area will not allow
future consumption
of a prey initially 20 mm in total length by a predator initially 40 mm in total
length (values based on data in Sogard and Olla (1994)). The resultant slope suggests that unless
larger fish grow 1.5X faster, smaller fish can outgrow their vulnerability to potential cannibals. Dashed
line indicates a 1: 1 correspondence
in absolute growth rates.
their average size was significantly larger than that of fish on predator-removal
reefs. This result was consistent with an interpretation of size-selective predation
but, alternatively, could have been a consequence of density-dependent growth
on the reefs lacking predators. Size distributions of two other prey fish, bluehead
wrasse (Thalassoma bifasciatum) and rainbow wrasse (Halichoeres pictus) did
not differ between treatments, suggesting no size-selection occurred.
In contrast to the fish and crustacean predators noted above, bird predators
generally appear to be positively size selective on YOY fishes; birds allowed free
access to fish in mesocosm and field studies appear to preferentially select relatively large size classes of juveniles (Britton and Moser, 1982; Power et al., 1989;
Trexler et al., 1994). The relative importance of bird predation as a mortality
agent likely varies across ecosystems. In some pelagic habitats, bird predation is
considerably lower than fish predation, particularly for age-O juveniles (Livingston, 1993).
With the exception of bird predation, experimental studies generally demonstrate that predation risk decreases as size of prey fish increases. However, experimental methods may not provide realistic encounter rates of predators with
different sizes of prey and experiments typically are restricted to a greatly simplified predator/prey community that does not reflect the natural complex of interacting species. The importance of testing relevant combinations of prey and
predator sizes is clearly evident in the results of Rice et al. (1993); with small
predators (southern flounder, Paralichthys lethostigma), mortality is biased toward
small spot (Leiostomus xanthurus), but the outcome of predation is reversed in
the presence of large predators (Fig. 2).
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BULLETIN OF MARINE SCIENCE, VOL. 60, NO.3, 1997
100
c
o
Prey
••
size class
Small
~
Large
75
en
o
Q.
E
50
o
u
lo...
o
>
25
>
lo...
:::::l
(f)
o
NONE
SMALL
Predator
LARGE
MIXED
field
Figure 2. Results of pond experiments in which two size classes of spot (Leiostomus xanthurus)
were exposed to varying predator conditions of no predators (control), small southern flounder (Paralichthys lethostigma), large flounder, or mixed sizes of flounder. Bars indicate the size composition
of spot at the conclusion of the 20-d experiments; initial size distributions were 50:50 in all treatments.
Data from Rice et al. (1993).
Field Studies of Predator Size-Selectivity.-A
more direct means of testing for
size-dependent predation is examination of actual predator diet compared to the
available size range of prey under natural field conditions. For example, concurrent collections of predators and prey provided consistent evidence of negative
size selection in YOY walleye (Stizostedion vitreum) cannibalized by adults
(Chevalier, 1973), and Atlantic silversides (Menidia menidia) and bay anchovies
(Anchoa mitchilli) consumed by juvenile bluefish (Juanes and Conover, 1995).
In a thorough analysis of size distributions of YOY flatfish and their predators,
Ellis and Gibson (1995) observed clear size-dependent effects in accordance with
size spectrum theory. Small flatfish (Pleuronectes platessa, P. flesus, and Limanda
limanda) were preyed upon by a greater diversity and greater size range of predators; consequently, they comprised a greater proportion of the gut contents of
the predator field compared to large prey on each sampling date. However, large
predators able to consume flatfish as they grew were absent from the study site,
demonstrating a break in the size spectrum. Thus, flatfish that reached a size of
about 45 mm attained a size refuge releasing them from co-occurring predators.
Ellis and Gibson (1995) emphasized the importance of this disruption in the predator size spectrum in establishing the beach habitat as a nursery ground. As juvenile flatfish approached the size refuge, they were subject to a narrowing number and abundance of predators. After reaching a sufficient size, they had virtually
escaped predation until leaving the nursery ground.
In a different nursery system in the Wadden Sea, van der Veer et al. (in press)
also compared size distributions of flatfish (several species) with concurrently
SOGARD: SIZE-SELECTIVE
MORTALITY IN JUVENILE FISHES
1137
sampled gut contents of their major predators, extending the analysis back to
larval stages and forward to late YOY stages. Their results document the dynamic
nature of selective processes as an individual passes through successive life stages.
The larval stage is subject to high predation rates by coelenterates, which are
largely non-size selective. Newly metamorphosed individuals, in contrast, are subject to strong size-selective predation by crangonid shrimp, which primarily consume fish < 30 mm in length. During the subsequent juvenile period, fish predators are also size-selective, but the direction of this selection is dependent on
predator size. Young-of-the-year Atlantic cod select smaller flatfish juveniles «
30 mm), but age-l cod prefer larger flatfish (> 50 mm). Bird predators (cormorants) typically select large members of the age-O cohort. Thus, an individual
flatfish on the Wadden Sea progresses through a series of both size-selective and
non-selective predators as it grows through the first year. The cumulative outcome
of this predator field on survival to age 1 depends on the mortality rate at each
step.
The direction of size-selective predation also appears to vary with life history
stage for juvenile Atlantic salmon (Salmo salar). Red-breasted mergansers consume a broad size range of juvenile Atlantic salmon (30-130 mm), but appear to
be positively size-selective for parr stages and negatively size-selective for smolts
(Feltham, 1990). These results are consistent with a generalized dome-shaped
vulnerability curve.
Experimental Tests of Overwinter Survival.-For temperate species, experimental
studies have concluded that larger members of a cohort are more likely to survive
extended periods of cold temperatures compared to smaller conspecifics of smallmouth bass (Micropterus dolomieu), Atlantic silverside, sand smelt (Atherina boyeri), Colorado squawfish (Ptychocheilus lucius), rainbow trout (Oncorhynchus
mykiss), smallmouth flounder (Etropus microstomus), and walleye pollock (Table
1). The mechanism of size-biased mortality has been attributed to starvation
(caused by higher metabolic rates and lower energy stores of small fish compared
to large fish), continued size-dependent predation through the winter, or physiological intolerance
of cold temperatures.
A series of laboratory and field studies documented size-dependent effects of
cold temperatures on white perch (Morone americana) and yellow perch (Post
and Evans, 1989b, Johnson and Evans, 1990; Johnson and Evans, 1991). Overwinter mortality was significantly influenced by species (white perch more susceptible than yellow perch), feeding level (starved fish more susceptible than fed
fish), temperature (higher survival at 4° than 2.5°), and fish size (higher survival
for large fish than for small fish). The interacting effects of winter severity and
fish size on survival of white perch resulted in size-dependent mortality being
most evident under intermediate winter conditions; at 4°, 90% of the deaths were
individuals smaller than average at the start of the experiment, whereas at 2.5°C,
the increased mortality of large fish resulted in only 64% of the deaths being
attributable to small fish (Johnson and Evans, 1990). Severe winters, then, should
result in high mortality of all size classes, eliminating any advantages for large
fishes, whereas mild winters should promote high survival of all size classes.
Thus, size-dependency of mortality is most likely under intermediate winter conditions.
Release and Tracking of Marked lndividuals.- Tracking of hatchery-reared individuals marked and released into natural systems has generally provided strong
support for the 'bigger is better' hypothesis (Wahl and Stein, 1989; Svasand and
Kristiansen, 1990; Johnson and Margenau, 1993; Willis et al., 1995). For example,
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BULLETIN OF MARINE SCIENCE, VOL. 60, NO.3, 1997
Table 1. Summary of studies that have reported size-selective mortality in juvenile stages of teleost
fishes, categorized by method of assessment. Negative size-selectivity indicates higher mortality of
smaller size classes, positive size-selectivity indicates higher mortality of larger size classes, stabilizing
selectivity indicates higher survival of intermediate size classes, and disruptive selectivity indicates
higher mortality of intermediate size classes.
Direction of
Species
Interannual correlative comparisons
Salvelinus fontinalis
Perca jfavescens
Stizostedion lucioperca
Oncorhynchus nerka
Predation experiments
Oncorhynchus gorbuscha
Oncorhynchus keta
Perca jfavescens
Pomatomus saltatrix
Pleuronectes platessa
Paralichthys olivaceus
Pleuronectes americanus
Chromis cyanea
Halichoeres pictus
Thalassoma bifasciatum
Gambusia affinis
Rineloricaria uracantha
Ancistrus spinosus
Poecilia latipinna
Leiostomus xanthurus
(large predators)
(smaIl predators)
Field studies of predator preference
Stizastedian v. vitreum
Menidia menidia
Anchoa mitchilli
Limanda limanda
Pleuronectes jfesus
Pleuronectes platessa
(larval)
(early juvenile)
(late juvenile)
Salmo salar (parr)
(smoll)
Overwinter survival experiments
Micropterus dalomieu
Menidia menidia
Atherina boyeri
Perca jfavescens
Morone americana
Prychocheilus lucius
Oncorhynchus mykiss
Centropristis striata
Etropus microstomus
Theragra chalcagramma
size-selective
mortality
Reference
negative
negative
negative
negative
none
none
Hunt, 1969
Nielsen, 1980
Buijse and Houthuijzen, 1992
Foerster, 1954
Hyatt and Stockner, 1985
Henderson and Cass, 1991
negative
negative
negative
negative
negative
negative
negative
negative
negative
none
none
positive
none
positive
positive
Parker, 1971
Hargreaves and LeBrasseur, 1986
Post and Evans, 1989a
Paszkowski and Tonn, 1994
Juanes and Conover, 1994a
van der Veer and Bergman, 1987
Seikai et aI., 1993
Witting and Able, 1993
Carr and Hixon, 1995
Carr and Hixon, 1995
Carr and Hixon, 1995
Britton and Moser, 1982
Power et aI., 1989
Power et aI., 1989
Trexler et aI., 1994
positive
negative
Rice et aI., 1993
Rice et aI., 1993
negative
negative
negative
negative
negative
negative
none
negative
positive
positive
negative
Chevalier, 1973
Juanes and Conover, 1995
Juanes and Conover, 1995
Ellis and Gibson, 1995
Ellis and Gibson, 1995
Ellis and Gibson, 1995
van der Veer et aI., in press
van der Veer et aI., in press
van der Veer et aI., in press
Feltham, 1990
Feltham, 1990
negative
negative
negative
negative
negative
negative
negative
negative
disruptive
negative
negative
Oliver et aI., 1979
Conover, 1984
Henderson et aI., 1988
Post and Evans, 1989b
Johnson and Evans, 1991
Johnson and Evans, 1990, 1991
Thompson et aI., 1991
Smith and Griffith, 1994
Hales and Able, in press
Hales and Able, in press
Sogard, unpubl. data
SOGARD: SIZE-SELECTIVE
1139
MORTALITY IN JUVENILE FISHES
Table I. Continued.
Direcrion
Species
Tracking marked individuals
Micropterus salmoides
Gadus morhua
(larvae)
(juveniles-low food)
(juveniles-high food)
Esox masquinongy
Sciaenops ocellatus
Pagrus major
MugU cephalus (halchery)
(wild)
Tracking length-frequency distributions
Menidia menidia
Stizostedion v. vitreum
Lepomis macrochirus
Micropterus salmoides
of
size-selective
mOl1ality
negative
negative
none
negative
negative
negative
negative
negative
negative
negative
negative
negative
negative
negative
negative
negative
negative
negative
none
none
none
negative
(strong)
(weak)
(strong)
(weak)
Perca fiavescens
Pimephales promelas
Lepomis cyanellus
Pomoxis annularis
Stizostedion lucioperca
Salmo trutta
(low density)
negative
(high density)
stabilizing
Centropristis striata
negative
Tautoga onitis
negative
Tautogolabrus adspersus
negative
Etropus microstomus
negative
Monitoring characteristics of survivors in natural populations
Oncorhynchus keta
negative
Oncorhynchus kisutch
none
negative
(low food)
negative
(high food)
none
Oncorhynchus nerka
negative
negative
(early season)
positive
(late season)
negative
Oncorhynchus mykiss
negative
Perca fiavescens
(low food)
negative
(high food)
none
Reference
Wahl and Stein, 1989
Svasand and Kristiansen, 1990
Blom et aI., 1994
Blom et aI., 1994
Blom et aI., 1994
Johnson and Margenau, 1993
Willis et aI., 1995
Tsukamoto et aI., 1989
Leber, 1995, Leber et aI., 1995
Leber et aI., 1995
Conover and Ross, 1982
Conover, 1984
Chevalier, 1973
Forney, 1976
Toneys and Coble, 1979
Toneys and Coble, 1979
Adams et aI., 1982
Post and Evans, 1989b
Toneys and Coble, 1979
Toneys and Coble, 1979
Toneys and Coble, 1979
Buijse and Houthuijzen, 1992
Elliott, 1990a, 1990b
Elliott, I990a, 1990b
Hales and Able, in press
Hales and Able, in press
Hales and Able, in press
Hales and Able, in press
Healey, 1982
Fisher and Pearcy, 1988
Hager and Noble, 1976
Holtby et aI., 1990
Holtby et aI., 1990
Henderson and Cass, 199I
West and Larkin, 1987
Bilton et aI., 1982
Bilton et aI., 1982
Ward et aI., 1989
Post and Prankevicius, 1987
Post and Prankevicius, 1987
Tsukamoto et al. (1989) used fluorescent otolith marks to code two size groups
(mean length = 20 and 40 mm) of cultured red sea bream (Pagrus major) released
into a natural population. Subsequent recaptures provided two lines of evidence
of size-dependent mortality: survival of fish in the 40-mm size group was 49%
higher than that of the 20-mm group, and survival was positively related to size
within this group, based on dimensions of otolith marks.
1140
BULLETIN OF MARINE SCIENCE, VOL. 60, NO.3,
1997
The stocking method, however, has several potential drawbacks that can produce equivocal results concerning the importance of size-based processes. 1) Mark
and release methods allow the creation of atypical size distributions, potentially
increasing variability and thus artificially inducing size-selective processes. 2)
Patterns of size-selective mortality can differ for hatchery-reared and wild fish.
Hatchery-reared juvenile striped mullet (Mugil cephalus) released into known
nursery habitats in Hawaii exhibited clear negative size-selection, with small size
classes eventually disappearing from the study sites, but for wild juveniles that
were similarly tagged and released, the influence of size on survival was less
pronounced, and small size classes persisted throughout the 7-month recapture
period (Leber, 1995; Leber et al., 1995). 3) Fish are often stocked at a relatively
large size, potentially missing a critical early period of high mortality in either
the larval or early juvenile stages.
The difficulty of tagging early stages was resolved by Blom et al. (1994) by
using genetic markers in Atlantic cod to track survival from the egg stage. This
study revealed valuable insights regarding the timing of selective processes and
their variable intensity. Eggs and newly hatched larvae from two parental phenotypes were stocked in ponds, with survival monitored through the summer
growing season, encompassing both the larval and early juvenile stages. Mortality
rates during the larval stage did not differ between the two strains and did not
suggest size-selective mortality in either year of the study. However, after metamorphosis there were substantial differences in mortality between the two strains,
and the contrast was size-related. In 1990, strain A was consistently smaller than
strain B; although stocked at a proportion of 80%, strain A fish declined to only
about 45% of the population at the end of the experiment. In contrast, in 1991
strain A fish were larger than strain B and increased in proportion from 44% at
stocking to 60% at the end of the experiment. Size-selective mortality was more
intense in 1990 than in 1991 and appeared to be correlated with food availability;
macrozooplankton densities were consistently lower in 1990, and overall survival
during the juvenile stage was lower (estimated at 7.7% for 1990 and 25% for
1991). The mechanism of mortality was presumed to be cannibalism. During the
post-metamorphic stage, growth depensation was evident, creating sufficient size
variability to allow high levels of cannibalism. Blom et al. (1994) suggested that
lower food availability in 1990 exacerbated density-dependent competition for
food, increasing the incidence of cannibalism compared to 1991. Because water
inflow to the ponds screened out potential heterospecific predators, the study did
not adequately assess size-dependent losses in a natural community with a full
predator complement. Alternative explanations for the differential survival of the
two strains include genetic effects on mortality, but this effect would have to
switch between years to be applicable. Survival of the faster growing strain could
have occurred each year without any differences in mortality based on relative
size within a strain. However, the lack of any difference in mortality between the
two strains during the larval stage and the clear correspondence of high mortality
of the slow-growing strain with the period of maximal cannibalistic potential
(based on size ranges) provide support for Blom et al.'s (1994) conclusion of sizedependent mortality.
Tracking of Length-frequency Distributions in Natural Populations.-Comparison
of the size distribution of a natural, unmanipulated YOY cohort at different times
can test for size-selective mortality, provided some critical assumptions are met.
It is vital to obtain unbiased estimates of the size distribution and to verify that
successive samples are derived from the same population. Because size-selective
SOGARD: SIZE-SELECTIVE
MORTALITY IN JUVENILE FISHES
1141
processes can vary over time, appropriate scales of sampling are also necessary.
This aspect is clearly documented by Elliott (1990a) for stream populations of
YOY brown trout (Salmo trutta); size-dependent mortality occurs during a critical
period following juvenile emergence from gravel nests, but not before or after
this period. Finally, changes in the size distribution due to mortality must be
distinguished from changes due to ongoing growth (Miller, in press). Ideally,
comparisons of size distributions before and after a time interval of suspected
size selection employ longitudinal sampling, in which repeated measurements of
the same individuals are available, allowing direct assessment of individual
growth (Chambers and Miller, 1995). Longitudinal sampling provides the additional benefit of allowing distinction of selection on body size vs. selection on
growth rate (Lynch and Arnold, 1988), although this approach has rarely been
incorporated by fish ecologists. Prior sizes are typically estimated using otolith
or scale increments; appropriate assumptions associated with back-calculation
(Campana and Neilson, 1985; Campana, 1990) are critical for accurate data interpretation. If sampling is limited to separate groups of individuals (cross-sectional sampling), variability in individual growth is unknown and can only be
indirectly estimated. Miller (in press) and Post and Evans (1989b) outline statistical procedures that can be used to assess selective mortality from subsequent
size-frequency distributions when only cross-sectional samples are available.
However, these techniques cannot uniquely identify the underlying selective processes, and only intense selection produces statistically significant effects. Thus,
with cross-sectional sampling, detectability of size-selective mortality is problematic (Miller, in press).
The tracking method, using cross-sectional sampling, has been effective in examining overwinter mortality. The growth problem is addressed by assuming that
cold winter temperatures prohibit measurable growth; this assumption is typically
supported by the lack of any increase in maximum size in spring samples. Growth
rates of four Northwest Atlantic estuarine species held in the laboratory under
ambient winter temperatures and provided with ad libitum food also suggest minimal length increases (Hales and Able, in press). Disappearance of small size
classes between fall and spring sampling, presumed to indicate high winter mortality for small fish, has been reported for Atlantic silversides, walleye, bluegill
(Lepomis macrochirus), largemouth bass (Micropterus salmoides), yellow perch,
black sea bass (Centropristis striata), tautog (Tautoga onitis, cunner (Tautogolabrus adspersus), and smallmouth flounder (Table 1). However, Toneys and Coble (1979) found no size relation in overwinter mortality for fathead minnows
(Pimephales promelas), green sunfish (Lepomis cyanellus), or white crappie (Pomoxis annularis). The opposing pattern of an advantage to small size over the
winter has not been reported.
Buijse and Houthuijzen (1992) tracked length-frequency distributions of YOY
pikeperch across the growing season for three year classes, and attributed a decline
in abundance of small size modes to selective mortality. The alternative explanation of accelerated growth by small pikeperch was ruled out by analysis of
condition; smaller fish had proportionately lower fat and energy content than
larger fish, and those levels decreased over the summer.
Based on length-frequency sampling of YOY brown trout, Elliott (1990a,
1990b) concluded that the intensity and direction of size-selective mortality are
dependent on initial egg density. When egg densities are low, survival is high,
the range of individual sizes is high, and mortality appears to be selective only
against the smallest size classes. In contrast, in years with high initial egg density,
survival rates are low, the variation of size narrows, and both small and large
1142
BULLETIN OF MARINE SCIENCE. VOL. 60. NO.3. [997
size modes disappeared from the population. Thus, Elliott (1990b) provides one
of the few studies suggesting the occurrence of stabilizing selection for intermediate sizes. Although direct support for the hypothesized survival advantage of
intermediate size classes was not possible, indirect support was based on the
absence of large and small size modes in years of high density and by the greater
proportion of large and small fish among those migrating away from the study
site; migrating fish were in poorer physiological condition and presumed to have
higher mortality rates than fish remaining in the nursery habitat. Small fish presumably were excluded from adequate foraging sites, whereas large fish were
potentially eliminated because of the energetic costs of defending relatively large
territories under high density conditions (Elliott, 1990b).
Comparison of size distributions is a relatively simple means of estimating sizedependent mortality, but violation of assumptions, particularly regarding growth,
allows a high potential for misinterpretation. Note that while growth variability
can bias estimation of size-selective mortality, the reverse situation is also likely,
with size-selective mortality producing a bias in estimation of growth rates. Disproportionate removal of small fish causes overestimation of growth rates if the
latter is based only on survivors. This problem is succinctly illustrated by Ottera
(1992): specific growth rates of juvenile Atlantic cod are consistently overestimated if the higher mortality of smaller fish compared to larger fish is not considered in growth analyses.
Characteristics of Survivors in Natural Populations.- The most concrete test of
size-dependent mortality employs longitudinal sampling to evaluate characteristics
of survivors and non-survivors in natural populations (Miller, in press). With this
approach, comparisons are based on natural densities and size compositions that
are not altered by adding individuals, and the population is subjected to natural
mortality sources. This method typically involves determining the initial size distribution of a cohort. After the time interval in question, a second sample of
survivors is collected and the size distribution of this group is back-calculated to
the initial sampling time, typically using otolith or scale increments. The initial
sizes of survivors are compared with initial sizes of the total population, and any
deviations are presumed to indicate non-random mortality. As with all of the field
methods, the assumptions regarding unbiased sampling of the same population
apply.
The method has primarily been applied to salmonid populations. For example,
scale circuli of juvenile chum salmon were analyzed by Healey (1982) to examine
mortality patterns just after migration into marine habitats. The proportion of the
population comprised of individuals with wide circuli spacing increased over a
20-d period, indicating significant selection against small fish. The effect was
particularly dramatic for slightly older fish, suggesting that the intensity of sizeselective mortality increased over time, peaking at a size range of 45-55 mm. In
contrast, Fisher and Pearcy (1988) concluded that there was little evidence for
size-selective mortality during the first summer of ocean residence in coho salmon. Monthly sampling from May through September, with back-calculation of
May lengths based on scale circuli, suggested that large size in May was consistently advantageous in only 1 out of 5 years.
On a broader time scale, a number of studies have compared the size of salmon
as outmigrating smolts with the back-calculated smolt size of adults returning to
freshwater on spawning migrations. Higher mortality for smaller smolts than larger smolts within a cohort has been reported for sockeye (Henderson and Cass,
1991), coho (Hager and Noble, 1976), and steelhead (Oncorhynchus mykiss, Ward
SOGARD: SIZE-SELECTIVE
MORTALITY IN JUVENILE FISHES
1143
et al., 1989). Bilton et al. (1982) found seasonal differences in the direction of
size-selective mortality; among sockeye smolts released early in the season, smaller individuals were more likely to return as adults, whereas for smolts released
later, larger individuals had higher adult returns. Because smolts released on later
dates had higher total survival compared to early releases, the results in general
supported a survival advantage of large juvenile size.
With broad scale sampling, early periods of selective mortality can be obscured
or missed due to later periods of non-random mortality. For many of the salmonid
studies, adults were sampled after returning to their natal stream, following the
imposition of substantial fishing mortality. In populations where size differences
are maintained and juvenile size is a good predictor of adult size, selective fishing
mortality on relatively large individuals could accentuate positive size-based juvenile mortality and obscure negative size-based mortality.
More detailed analysis of progressive stages in the life history was conducted
by West and Larkin (1987), who tracked the survival of sockeye salmon from
emergence through the first year of life. Otolith radii measurements were used to
back-calculate the initial fry length of surviving individuals at successive stages.
Because size differences were maintained, disappearance of fish that were small
as fry could be attributed to their relatively small size throughout the juvenile
period. Strong negative size-selection was apparent; individuals in the lower half
of the initial size distribution at emergence had only 8.9% survival to the smolt
stage, whereas those in the upper half survived at a rate of 63.6%. Based on
interim sampling periods, West and Larkin (1987) concluded that size-selective
mortality was not important during the early part of the summer (following emergence in May-June), but intensified late in the summer, presumably after the
period of highest mortality. However, this conclusion, which seems counterintuitive to the logic that size-selection should be most intense when mortality rates
are high and fish are small, is not evident from their size-frequency distributions.
The first post-emergence sampling indicated a high abundance of fish that were
small at emergence, suggesting that mortality immediately following emergence
was strongly selective against large fish. Subsequent samples demonstrated a consistent shift toward survival of relatively
large individuals,
supporting
the conclu-
sion of negative size-selective mortality. An alternative explanation for this pattern
is that initial fry collections severely underestimated the abundance of small sockeye. The contrast in interpretation of size distributions under these two alternatives
is striking. If sample collections were representative, an initial period of intense
positive size-selective mortality must be invoked. If the collection at emergence
inadequately sampled small fry, initial mortality could have been indiscriminate
or negatively size-selective, but an even greater contrast in initial size distributions
of survivors to the smolt size would have to be accepted. These problems are
analyzed in detail by Anderson (1995), who derived size-based survival functions
from spline curve analysis of West and Larkin's (1987) data and discerned probable sampling biases.
Size-selective mortality varied between populations of yellow perch in two
Wisconsin lakes, based on otolith analysis of survivors (Post and Prankevicius,
1987). The contrasting results were attributed to two interacting ecological factors
differing between the lakes. In the lake where strong negative size-selectivity
occurred, growth rates were reduced due to lower Daphnia densities; thus, the
young perch spent more time in vulnerable size classes compared to the lake with
faster perch growth and no apparent size-selective mortality. However, the importance of food availability was potentially confounded by different predator
fields in the two lakes. The lake with poorer survival of small perch was domi-
1144
BULLETIN OF MARINE SCIENCE, VOL. 60. NO.3. 1997
nated by small, gape-limited predators, whereas the lake with no apparent sizeselective mortality contained large northern pike, presumably capable of consuming all sizes of YOY perch.
In one of the few long term assessments of size-dependent juvenile survival,
data on the size distribution of outmigrating coho salmon smolts and subsequent
adult population size were compared by Holtby et al. (1990). Size-selective mortality occurred in years with poor overall survival, but not in years with high
ocean survival. Data on the correspondence of size with marine survival were
available for 14 years, which fell naturally into two groups with low and high
survival. Significant regressions of smolt size with survival to adulthood (based
on back-calculation from scale radii) occurred in 5 of the 7 low survival years
and none of the high survival years. Because survival was positively correlated
with early juvenile growth after smolts entered oceanic waters, slow overall
growth appeared to enhance size-selective mortality, with gape-limited predators
a potential mortality agent. Interestingly, there was little indication of densitydependence; early growth and marine survival were unrelated to the total production of srnolts in the region. The absence of size-selection in years of high
survival could potentially be attributed to a reduced intensity of predation or a
more narrow size distribution of smolts. The latter effect was unlikely, because
the range of smolt lengths did not differ between years of high and low survival.
Modeling.-Modeling methods have been used extensively in analyzing the potential outcomes of size-selective mortality in juvenile fishes. They have been
valuable in deriving predictions of conditions likely to induce size selection and
in providing means of detecting the occurrence of size-selection. Modeling enables extension beyond the restricted conditions necessary for interpretable experiments. Increasing sophistication in modeling techniques demonstrates a clear progression from correlating mean size with survival to developing testable predictions of the consequences of variable timing and intensity of size-biased mortality.
Miller (in press) used individual-based models to generate survivorship patterns
under varying growth and mortality schedules for larval and juvenile Atlantic
cod. Predicted shifts in size-frequency relationships resulting from each model
were then compared with cross-sectional field data on larvae collected off Nova
Scotia. Although model predictions were not all unique, a pattern of size-selective
mortality occurring late in the tested time interval could be rejected. In general,
however, Miller (in press) concluded that the statistical techniques applicable to
cross-sectional sampling can reveal only intense size-selective mortality. The
probability of detecting more subtle selective processes was greatly improved with
longitudinal sampling, when simulated prior sizes were included in the model.
Shuter et al. (1980) developed a simple physiological model to describe sizeselective overwinter mortality of smallmouth bass. Extensive field and laboratory
data on temperature responses were used to relate probability of survival to size
at the onset of winter and duration of the cold period. They found a reasonably
close correspondence of year class strength (derived from virtual population analysis) with overwinter survival as predicted from their model.
Modeling has been particularly effective in describing the likely mortality scenarios for dynamic predator-prey interactions in which both prey and predators
are growing, resulting in continually changing relative size relationships. For seasonal habitats, Pope et al. (1994) suggested that successful prey species must
adequately exploit peaks in productivity while avoiding developing waves of prospective predators. A more explicit examination of the wave model of growing
predators and growing prey was presented by Rice et al. (in press). Based on a
1145
SOGARD: SIZE-SELECTIVE MORTALITY IN JUVENILE FISHES
.,~
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Figure 3. Predicted daily mortality rates of growing prey (spot, LeiostomltS xanthltrlts) in the presence
of growing predators (souIhern flounder. Paralichthys lethostigma), derived from an individual-based
simulation model. Dotted lines indicate size trajectories of spot with different growth rates (increasing
from a to d) occurring with flounder growing at a constant rate; percentages denote spot survival at
the end of 60 d. For a 45 mm spot, fast growth in the presence of small flounder allows prey to
outgrow their vulnerability, but fast growth with large predators moves prey up the mortality curve
to peak vulnerability. Figure from Rice et al. (in press), with permission from Chapman and Hall
publishers.
series of studies that have elucidated size-dependent components of the predator-prey interaction between southern flounder and spot (Rice et aI., 1993; Wright
et al., 1993; Crowder et al., 1994), empirically-derived growth rates and gapelimited predation rates were incorporated into a more complex model. The resulting simulations clearly elucidated the importance of timing to any advantages
gained by large or small size, with different optimal growth rates depending on
the position of the prey relative to the size distribution of the predators (Fig. 3).
Early-spawned individuals would increase their survival probability by growing
rapidly and remaining ahead of the high mortality ridge of the predator wave. In
contrast, late-spawned individuals would benefit from slow growth rates that allowed the predator wave to move away from them. Thus, the model predicted
that the influence of flounder predation on a spot cohort will depend on key
1146
BULLETIN OF MARINE SCIENCE. VOL. 60. NO.3.
1997
environmental variables shaping the size distribution of flounder, the timing of
spawning by spot, and subsequent growth rates of both populations.
What Factors Modify or Mask the Effects of
Size-selective Mortality?
If bigger is generally better, we should expect continual directional selection
toward large body size and fast growth rates. Obviously, there must be constraints
or trade-offs that place boundaries on such selection. An initial constraint is phylogenetic; interspecific differences in the mechanics of muscle fiber recruitment
limit the potential for rapid growth in species with small adult size (Weatherley
et al., 1988). Within a species, trade-offs begin at spawning. Although larger eggs
generally result in larger larvae (Blaxter and Hempel, 1963), which may enjoy a
persistent size advantage relative to individuals from smaller eggs, females producing large eggs entail a potential fitness cost of lowered fecundity. The pervasive small size of teleost eggs, particularly for marine species, suggests that
fitness advantages of egg quantity outweigh advantages of large egg size (Duarte
and Alcaraz, 1989; Elgar, 1990; Winemiller and Rose, 1993).
For temperate species with seasonal growth cycles, the timing of spawning has
a major influence on body size; early-spawned individuals should have a substantial size advantage compared to late-spawned fish (Tanaka et al., 1989; Folkvord et al., 1994; Cargnelli and Gross, 1996). However, early-spawned sub-cohorts may experience higher mortality rates than late-spawned fish due to unfavorable temperatures (Rutherford and Houde, 1995), mismatch with plankton production (Cushing, 1990), or reduced growth rates and extended stage duration
due to colder temperatures (Rice et al., 1987). Schultz (1993) concluded that high
predation rates on dwarf perch (Micrometrus minimus) born early in the season
and high overwinter mortality of individuals born late results in stabilizing selection for intermediate birthdates.
Another potential trade-off deals with habitat selection. Numerous studies have
documented habitat-dependent differences in growth rates (reviewed in Sogard,
1994) and predation rates (Werner et al., 1983; Kneib, 1987; McIvor and Odum,
1988; Rozas and Odum, 1988). Habitats that provide faster growth often have a
higher predation risk than habitats supporting slower growth, requiring fish to
make a behavioral trade-off between rapid growth and protection from predators
(Mittelbach, 1981; Werner and Gilliam, 1984; Lima and Dill, 1990; Milinski,
1993). Thus, for a population distributed across a mosaic of habitats, bigger may
be better within a habitat but not across the population if fast growing individuals
reside in risky habitats. A broad variety of species are found in greater density
in protective habitats despite lower growth rates compared to alternative habitats
(Fig. 4, Sogard, 1992, 1994; Tupper and Boutilier, 1995b).
Social interactions can also influence growth rates. Juvenile damselfish (Dascyllus albisella) reside in groups structured by dominance hierarchies (Booth,
1995). Fish in large groups tend to have higher survival rates but slower growth
rates than fish in small groups, resulting in delayed time to maturity. Post-larvae
Figure 4. Upper graph-mean growth rate and mean density of Gobiosoma bose in different habitats
(seagrass, sand adjacent to seagrass, sand adjacent to Viva, and Viva beds) of New Jersey estuaries.
Lower graph-mean growth rate, percentage of successful captures by predators, and percentage survival of juvenile Gadus morhua occupying different habitats in Nova Scotia. Data on Gobiosoma bose
from Sogard (1992); data on Gadus morhua from Tupper and Boutilier (l995b).
1147
SOGARD: SIZE-SELECTIVE MORTALITY IN JUVENILE FISHES
0.6
"'C
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::::J
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Ha bitat
REEF
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GRASS
1148
BULLETIN OF MARINE SCIENCE, VOL. 60, NO.3, 1997
prefer to settle in large groups of conspecifics, again suggesting that growth is
sacrificed in favor of an improved probability of survival. Likewise, schooling
behavior can provide protection from predators, but at a potential cost of reduced
growth due to competition (Eggers, 1976). Behavioral responses to predators and
competitors can also reduce individual growth (Metcalfe, 1986).
Further trade-offs involve balancing the advantages of fast growth with associated physiological costs. Conover and Schultz (in press) provide a compelling
argument suggesting that physiological constraints prevent southern populations
of Atlantic silverside from attaining their maximum growth potential, despite demonstrated advantages of large size for avoiding predation and surviving over the
winter. Northern populations have a higher genetic capacity for rapid growth,
allowing fish to reach the same body size in the fall as their southern counterparts,
despite a shorter growing season (Conover and Present, 1990), Why, if large body
size is beneficial, do southern individuals not attain the growth rates displayed by
northern populations? Conover and Schultz (in press) suggest that physiological
costs select for more moderate growth rates. High metabolic rates induced during
processing of ingested food (specific dynamic action) may encompass the full
available metabolic scope, particularly for fish of small body size, which have a
limited capacity for anaerobic functioning. Thus, maximal ingestion and growth
rates severely restrict the scope for other energy demands, such as active predator
avoidance. In northern populations, intense size-dependent overwinter mortality
requires the silversides to sacrifice other energetic needs and allocate more resources to growth. Southern populations, with their extended growing season, can
readily attain sufficient overwinter size with a moderate growth rate and maintain
an energy reservoir for other activities. Although their energy budgeting hypothesis has not been tested, Conover and Schultz (1997) provide one of the few
studies distinguishing selection on growth rate from selection on body size and
suggesting conflicting benefits for the two factors.
Additional trade-offs between rapid growth and other ecological requirements
are succinctly reviewed across a wide range of taxa by Arendt (in press). Although
convincing evidence is limited, some factors that might select for less than maximal growth rates include energetic costs of tissue and organ development, maintenance and repair costs, and costs of defense against predators. The allocation
of resources to these competing requirements has only recently been addressed
by ecologists, but should prove to be a fruitful area of study for understanding
both intra- and interspecific variability in growth rates.
Does Size-selective Mortality Influence Population
Dynamics or Recruitment Variability?
Identifying the mechanisms that generate non-random mortality allows estimation of which members of a cohort will survive, but does not necessarily clarify
the role of size-based processes in structuring the population or determining year
class strength. As noted by Rice et al. (in press) the impact of size-selective
mortality on survival can be substantial, but will not affect variability in recruitment unless the factors governing size-based processes vary themselves on an
interannual basis. Few empirical studies have examined the linkages between sizeselective mortality and population dynamics. Further examination of such relationships is needed to determine the utility of focusing on individual, size-based
processes as a means of understanding overall population regulation.
The potential impact of size-selective predators on both density and size distributions of their prey was demonstrated by Tonn and Paszkowski (1986), using
SOGARD: SIZE-SELECTIVE MORTALITY IN JUVENILE FISHES
1149
long-term tracking of size distributions in central mudminnows (Umbra limi).
Wisconsin lakes lacking adult yellow perch had high densities of mudminnows,
with a smaller mean size than in lakes with perch. After a severe winter that
removed most of the adult perch population in Jude lake, mudminnows reached
high densities, dominated by small individuals. As the perch population recovered
and juvenile perch grew into predatory size classes, the size distribution of mudminnows displayed a distinct shift toward larger sizes. Laboratory experiments
confirmed that small perch had a limited capacity for mudminnow consumption
and large perch selected small prey; a clear size refuge was attained for minnows
at about 76 mm. Thus, following the removal of large perch, small mudminnows
had a temporary refuge from predation; the increased survival of small fish resulted in a dramatic shift in the size distribution. One year later, after perch
attained sizes capable of consuming mudminnows, the mudrninnows had an intermediate size distribution. After 2 years, the prey size distribution had reverted
back to that exhibited before the predator die-off, and recruitment was severely
restricted, with only a few mudminnows escaping predation and attaining large
sizes. Thus, size-dependent predation appeared to be highly influential in structuring this population.
Theoretically, size-selective mortality should play a crucial role in densitydependent population regulation, assuming that density directly modifies growth
rates. Negative size selection should moderate variability in abundance, whereas
positive size selection should increase variability in population size. van der Veer
et al. (in press) compared the interannual variability in year class strength among
different life stages to evaluate the influence of size-selective predation on population abundance in plaice. As expected, the non-selective predation by ctenophores during the larval stage resulted in no change in the C.V. (coefficient of
variation) of year class strength between stages of larval immigration and peak
settlement. During the early juvenile stage, with predators dominated by negatively size-selective shrimp, the predicted dampening of recruitment variability
occurred in one of three nursery areas. In the other two areas, however, temperature-induced fluctuations in shrimp abundance appeared to override any moderating effect of size-dependent mortality. Later in the juvenile stage, with predators dominated by positively size-selective fish and birds, the predicted increase
in C.V. of year class strength did not occur, suggesting that these predators did
not modify interannual variability in recruitment. Thus, van der Veer et al. (in
press) concluded that on an overall basis size-selective predation did not affect
recruitment variability in plaice.
Straightforward effects of size-dependent mortality on population dynamics and
recruitment variability are presumably more likely in low diversity, closed systems
like the lakes examined by Tonn and Paszkowski (1986). In more complex systems, detecting the impact of size-dependent processes is more difficult. Direct
feedback linkages between predator and prey abundances are less apparent in open
marine systems and the moderating effects of size-selective processes are more
likely to be masked by indiscriminate or random mortality factors.
CONCLUSIONS
Field and laboratory studies on juvenile stages of teleost fishes generally support the bigger is better hypothesis, within certain limitations. The evidence is
straightforward for overwinter mortality; larger members of a cohort can better
tolerate physical extremes and endure longer periods without food compared to
smaller conspecifics. With regard to predation, size-selective mortality depends
1150
BULLETIN OF MARINE SCIENCE. VOL. 60. NO.3. 1997
on the predator field, but smaller fish are typically susceptible to a broader spectrum of predators and experience higher mortality rates than larger fish. When
size-selective mortality has been detected in natural populations, it has generally
been biased against small members of the population (Table 1).
The validity of the conclusion that negative size-selective mortality is a common feature for juvenile fishes depends on the assumptions and limitations associated with each of the methods used to evaluate selectivity. The context of
experimental and modeling methods (e.g. predator-prey combinations in predation
experiments, temperature conditions in overwinter experiments, initial size distributions in mark-recapture experiments) must appropriately match the environment
naturally encountered by a juvenile fish. The contrasting outcome of predation
experiments depending on the initial combinations of predators and prey (Rice et
aI., 1993) highlights the relevance of this concern. Likewise, for methods that
evaluate population structure before and after a particular time interval, unbiased
samples from the same population are crucial for accurate interpretation of
changes in size distributions. West and Larkin (1987) provide one of the few
studies using the characteristics of survivors method with multiple, longitudinal
samples. However, the direction of selective mortality derived from their first two
samples is fully dependent upon the accurate estimation of the population's initial
size distribution. For methods that track length-frequency patterns with crosssectional sampling, the separation of growth-induced from mortality-induced
changes in size distributions further complicates the evaluation of selection.
All of the methods described in this review can provide insight into size-selective processes, but the longitudinal monitoring of natural populations is best
suited for evaluating the characteristics of survivors and demonstrating the occurrence of non-random mortality within a cohort. Assumptions of representative
samples and accurate back-calculation of prior sizes are critical to successful
application of this method, but if these assumptions are met the technique can
provide an unequivocal test of selective mortality. Remarkably few studies, however, have incorporated longitudinal sampling, despite the availability of otolith
techniques that can estimate both prior sizes and growth rates, assuming increment
widths accurately estimate somatic growth.
Few attempts have been made to distinguish selection on body size from selection on growth rate. Hare and Cowen (in press) provide a notable exception,
using otoliths to compare both body size and growth rate as factors enhancing
survival. Further investigation of the effects of correlates of body size (age, condition, growth rate) on mortality is necessary to separate the relative roles of these
different factors.
Despite clear advantages of large body size, maximal growth rates may not
always be beneficial; a number of physiological constraints and ecological
trade-offs can limit growth on both ecological and evolutionary time scales. Genetic differences in growth capacity and physiological costs of resource allocation
place physical limits on individual growth (Conover and Schultz, in press). Behavioral selection of habitats or social conditions (i.e., conspecific aggregations)
that improve the probability of survival may result in a sacrifice of rapid growth,
and behavioral responses to potential predators and competitors can entail energetic or foraging costs that reduce growth. Under these conditions, the advantages
of large size are outweighed by the advantages of better protection from predators
and balanced physiological functioning. Such trade-offs can mask the occurrence
of directional selection within a particular habitat or promote stabilizing selection
for moderate growth rates. Conover and Schultz's (in press) results suggest conflicting attributes of large size and rapid growth; over the long term large size is
SOGARD: SIZE-SELECTIVE
MORTALITY IN JUVENILE FISHES
1151
beneficial in both escaping predators and overwinter survival, but over the short
term the energetic demands of rapid growth can threaten physiological functionmg.
There are a ·number of conditions under which size-selective mortality cannot
be detected or will not occur. By the end of a particularly harsh winter, for example, initial mortality on small fish will not be discernable due to subsequent
high mortality on all size classes. In contrast, during mild winters, survival of all
size classes will be high, with no selective mortality. Physical mortality factors
that are non-selective, such as oxygen depletion or temperature extremes, can
override selective mortality factors such as predation. If the direction of selective
mortality switches across time periods or life history stages, a single analysis of
survivors at the end of this progression may imply only random mortality. Predators that do not conform to size-spectrum theory may exert equivalent predation
pressure on all sizes of a cohort.
The composition of the predator field during the yay stage is a critical determinant of size-selective predation. If the size distribution and abundances of predators follow size-spectrum theory, then the number of potential predators will
always decline as prey size increase. An individual continues to encounter new
predators but fewer of them as it grows through the predation gauntlet. A break
in the predator distribution at the upper end of the prey's size range can effect a
size refuge beyond which prey vulnerability sharply declines (Ellis and Gibson,
1995). In this case an apex predator size can be identified, with negative sizeselective mortality up to but not beyond the peak size of vulnerability to this
predator size. For juvenile fishes, this scenario may largely define the 'nursery'
status of different habitats. An earlier break in the predator field, in contrast, can
shift the majority of predation to large size classes and change the direction of
size-selective mortality. There is currently little evidence either validating the
theoretical size-spectrum of predators or identifying factors that disrupt it.
A particularly intriguing result common to several studies (Post and Prankevicius, 1987; Holtby et al., 1990; Blom et al., 1994) is the apparent relation of
size-selective mortality with food availability. Under food-limited conditions, average growth rates are low, overall mortality rates are high, and size-selective
mortality is evident. These results are consistent with the stage duration hypothesis
(Houde, 1987): when growth is poor, fish remain in vulnerable size classes for
longer periods of time. Increased competition for limited food may also lead to
growth depensation, providing greater size variation and allowing intracohort cannibalism in some piscivores. The consequent high mortality rates increase the
likelihood of detecting the occurrence of size-selective processes. Under favorable
conditions with rapid growth and high survival, size-selective mortality may be
too subtle to be detected. Alternatively, this relationship could arise from a threshold effect, with rapid growth allowing most individuals to quickly attain some
minimum size, beyond which mortality is non-selective. Under poor growth conditions, individuals below the threshold size would experience high mortality.
Threshold effects may be particularly likely in overwinter mortality, with little
additional size advantages beyond some minimum that allows survival in most
winters. Further investigation of the intensity of size-selective mortality under
different environmental conditions will be valuable in elucidating the hypothesized correspondence with foraging success.
Better understanding of the extent of size-selective mortality during the juvenile
stage and the conditions under which it occurs has valuable applications in understanding recruitment variability. The processes that induce recruitment variability are likely to vary in influence between random and non-random mortality
1152
BULLETIN OF MARINE SCIENCE. VOL. 60, NO.3. 1997
scenarios, and attempts to discern environmental correlates with recruitment may
require different research approaches. If size is an important determinant of survival, research efforts should focus on factors that moderate growth. If, in contrast,
survivors are randomly derived from the initial population, research efforts should
focus on factors that moderate mortality. Because predation is a major source of
mortality under either scenario, assessment of the predator field is crucial to predictions of mortality rates. Potentially fundamental differences in the operation of
mortality factors for larvae and juveniles emphasize the need for separate evaluation of these two stages.
ACKNOWLEDGMENTS
This paper is dedicaled to C. Richard Robins, my M.S. advisor at the University of Miami. His
enthusiasm and sense of wonder at the amazing diversity of life histories in the fishes continue to
inspire me. I am grateful to S. Berkeley, M. Hixon, T. Miller, J. Rice, and two anonymous reviewers
for providing thorough critiques of the manuscript and valuable suggestions for improvements. I thank
W. J. Richards for inviting me to contribute to this special volume and the many authors who provided
me with pre-publication copies of their papers.
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DATE ACCEPTED: July 30, 1996.
ADDRESS: Alaska Fisheries Science Center, National Marine Fisheries Service, Hatfield Marine
Science Center, Newport, Oregon 97365.