Oecologia (2006) 148: 573–582
DOI 10.1007/s00442-006-0410-7
POPULATION ECOLOGY
Rena E. Vandenbos Æ William M. Tonn
Shelly M. Boss
Cascading life-history interactions: alternative density-dependent
pathways drive recruitment dynamics in a freshwater fish
Received: 3 August 2005 / Accepted: 23 February 2006 / Published online: 17 March 2006
Springer-Verlag 2006
Abstract Although density-dependent mechanisms in
early life-history are important regulators of recruitment
in many taxa, consequences of such mechanisms on
other life-history stages are poorly understood. To
examine interacting and cascading effects of mechanisms
acting on different life-history stages, we stocked
experimental ponds with fathead minnow (Pimephales
promelas) at two different densities. We quantified
growth and survival of the stocked fish, the eggs they
produced, and the resulting offspring during their first
season of life. Per-capita production and survival of eggs
were inversely related to density of stocked fish; significant egg cannibalism by stocked minnows resulted in
initial young-of-the-year (YOY) densities that were inversely related to adult densities. Subsequent growth and
survival of YOY were then inversely related to these
initial YOY densities, and survival of YOY was selective
for larger fish. Because of these compensatory processes
in the egg and YOY stages, treatments did not differ in
YOY abundance and mean size at the end of the
growing season. Because of differences in the intensity of
size-selective mortality, however, variation in end-of
season sizes of YOY was strongly (and inversely) related
to densities of stocked fish. When mortality was severe in
the egg stage (high densities of stocked fish), final YOY
size distributions were more variable than when the
dominant mortality was size-selective in the YOY stage
(low stocked fish densities). These differences in size
variation could have subsequent recruitment consequences, as overwinter survival is typically selective for
Communicated by Libby Marschall
R. E. Vandenbos Æ W. M. Tonn (&) Æ S. M. Boss
Department of Biological Sciences, University of Alberta,
Edmonton, AB, Canada T6G 2E9
E-mail: [email protected]
Tel.: +1-780-4924162
Fax: +1-780-4929234
Present address: R. E. Vandenbos
School of Renewable Resources, Selkirk College,
Castlegar, BC, Canada V1N 3J1
YOY fish larger than a critical threshold size. Densitydependent effects on a given life stage are not independent, but will be influenced by earlier stages; alternative
recruitment pathways can result when processes at earlier stages differ in magnitude or selectivity. Appreciation of these cascading effects should enhance our
overall understanding of the dynamics of stage-structured populations.
Keywords Early life-history Æ Population regulation Æ
Size-selective mortality Æ Egg cannibalism Æ
Pimephales promelas
Introduction
Following Nicholson’s (1933) introduction of the concept and subsequent decades of debate (e.g., Andrewartha and Birch 1954; Den Boer 1968; Strong 1986),
there is now general consensus that the regulation of
animal populations operates through density-dependent
mechanisms (Sinclair 1989; Turchin 1999; Lorenzen and
Enberg 2002). Nevertheless, for most groups of animals,
we still have a poor understanding of where densitydependence occurs in the life cycle, and how different
density-dependent mechanisms might interact (Sinclair
1989; Hanski 1990).
For many organisms, population regulation is
believed to be rooted early in life history (e.g., Miller
et al. 1988; Petranka 1989). This has led in recent decades to a large increase in studies focused on these early
stages (e.g., Brockelman 1969; Semlitsch and Caldwell
1982; Moksnes 2004). As a consequence of this emphasis, however, studies are often conducted in isolation of
other stages (but see, e.g., Prout and McChesney 1985;
Altwegg 2003).
For fishes, numerous studies have also focused on
processes occurring in larval and post-larval youngof-the-year (YOY) stages (see Miller et al. 1988; Sogard
1997; Chambers and Trippel 1997). Hatch date (Cargnelli
and Gross 1996), growth rate (Rice et al. 1993), and
574
body size (Post and Prankevicius 1987) have all been
shown to be important determinants of survival and
cohort strength. As well, variability in growth, age, and
size may also affect the intensity and selectivity of
mortality in YOY fish (Crowder et al. 1992; Rice et al.
1993).
Many of these characteristics may, in turn, be affected by intra-cohort densities. Most field studies,
however, can at best only estimate initial YOY densities.
And, in common with those on other taxa, many studies
of survival and recruitment in YOY fish largely ignore
other life stages. Information on adult density is sometimes incorporated (Post and Prankevicius 1987; Tonn
et al. 1994), but effects of adult density on YOY
recruitment are rarely examined in detail (but see Dong
and DeAngelis 1998; Post et al. 1998).
In most natural situations, life stages are not isolated
from each other. For instance, YOY survival may be
influenced directly and indirectly by other age-classes,
via cannibalism (Polis 1981; Smith and Reay 1991),
competition (Hamrin and Persson 1986; Hill 1992), and
consumption of YOY predators by older conspecifics
(Rettig and Mittelbach 2002). Also, although initial intra-cohort characteristics (e.g., density, timing of hatch,
size-distribution) may influence which YOY survive,
these characteristics can be determined by processes
acting on other life-history stages (Lorenzen and Enberg
2002; Vonesh and De la Cruz 2002). Furthermore, the
relative effects of one age-class on another might affect
the stability of population dynamics (May et al. 1974;
Cushing and Li 1992).
An early life stage that has not received much
attention is the egg. Mechanisms occurring during the
egg stage will affect YOY and can often be linked to
characteristics of the adult population. Egg production
may be affected by density-dependent growth in adults,
since maturity (Andrews and Flickinger 1974) and
fecundity (Wootton 1990) are often related to adult
body size. Egg survival may also be related to adult
density due, e.g., to a reduced ability of parents to defend eggs (Polis 1981; Smith and Reay 1991; Mappes
and Kaitala 1994). However, quantifying the number
and fate of eggs is often difficult, and usually only estimates are made, often rather roughly, of either egg
production or survival (Fox 1994; Post et al. 1998), even
though egg production and egg survival are often uncorrelated (e.g., Cole and Sadovy 1995). Until the
occurrence, strength, and interactions of densitydependent mechanisms among all life-stages, including
eggs, are better understood, we cannot fully understand
what controls recruitment of young and the regulation
of populations (Rodriguez 1989; Altwegg 2003).
We manipulated densities of fathead minnow (Pimephales promelas Rafinesque) in experimental ponds and
quantified processes acting on stocked fish, the eggs that
they produced, and the resulting offspring. Our objectives were to determine: (1) if YOY survival through the
first growing season is influenced (directly or indirectly)
by density-dependent processes acting on adults; and (2)
if and how egg-stage dynamics contribute significantly
to recruitment of YOY. Our ultimate goal was to assess
whether an examination of density-dependent mechanisms acting and interacting during different, often under-appreciated life-stages enhances our understanding
of population regulation.
Methods
Natural history
The fathead minnow is a small-bodied (ca. 5–8 cm),
omnivorous fish widely distributed in North America. In
the boreal region of Alberta, fathead minnows are
common in small, shallow lakes and ponds lacking piscivores, and frequently occur allopatrically as the only
fish species (Robinson and Tonn 1989). Two to four
summers are typically required for fathead minnows to
reach maturity in Alberta (Danylchuk and Tonn 2006),
compared with 1–2 summers at lower latitudes (Held
and Peterka 1974). Many populations are subject to
periodic winterkill, but can rebound quickly (Danylchuk
and Tonn 2003), suggesting that mechanisms exist that
allow rapid recovery (Danylchuk and Tonn 2001).
Populations in less-disturbed habitats, however, can
persist at high and relatively stable densities (Danylchuk
and Tonn 2003), suggesting regulation.
Males establish small (ca. 155 cm2; Flickinger 1973),
aggregated nesting territories (inter-nest distances often
£ 50 cm; Andrews and Flickinger 1974; Unger 1983;
Jones and Paszkowski 1997) and, following spawning,
guard a nest of eggs laid on the underside of plants, logs,
or rocks (McMillan and Smith 1974). Fathead minnows
reproduce readily in small ponds when provided with
nesting substrate (e.g., floating wooden boards, Jones
and Paszkowski 1997; Danylchuk and Tonn 2006);
manipulating substrate availability can ensure that eggs
are easy to find and enumerate. Eggs take ca. 5 days to
hatch at 25C (McMillan and Smith 1974), but require
6–12 days at ambient pond temperatures in boreal Alberta (Divino 2005; R. Vandenbos, unpublished data).
Eggs have distinct developmental stages (Nagel 1976; see
below), discernible to the unaided eye, which assist in
tracking the fate of egg batches. Adults are fractional
spawners, able to spawn more than once in a breeding
season (Gale and Buynak 1982), but there is high postreproductive mortality, especially among males (Markus
1934). Because of these life-history traits, all life-stages,
including eggs, are easy to sample, observe, and use in
realistic experimental settings, facilitating a study of
interactions among life-stages.
Experiment
This study was conducted at the University of Alberta’s
Meanook Biological Research Station (54 37¢ N, 113
35¢ W). The experiment was run for a full growing
575
season in each of 2 years, from spring (May) to near iceup (September–October).
Two research ponds (360 m2 surface area, 1.3 m
maximum depth) were divided in half by polyvinyl
curtains connected to wooden stakes that were buried
into the substrate and extended well above the water
level. Abundant nesting substrate (ten floating wooden
boards, 0.14·1.8-m, tied to weights) was added to each
pond half. The nest boards covered approximately 45%
of the inshore perimeter. Prior to stocking, the ponds
were raked and cleared of any other structures suitable
for nesting.
We manipulated initial densities of fish by adding a
1:1:1 ratio of mature males, mature females, and juveniles, collected from nearby natural ponds, to each of the
four pond halves at two density levels: 1 and 4 fishÆm 2.
These represent average and high densities, respectively,
seen in nearby natural populations (Danylchuk and
Tonn 2003). In a preliminary experiment, these densities
resulted in differences in growth, but not survival, of
stocked fish. There were duplicates of each treatment in
each year, with each divided pond hosting both treatments.
Mature males (‡70 mm total length (TL)) and females (‡63 mm TL) were identified by secondary sexual
characteristics, including tubercles on males and ovipositors on females (Danylchuk and Tonn 2001). Juveniles (two size-classes: 40–49 mm and 50–56 mm TL)
were defined as smaller fish that lacked secondary sexual
characteristics. Fish were marked with a subcutaneous
injection of fluorescent elastomer (Northwest Marine
Technology Inc., Shaw Island, WA) (Year 1) or fin
clipping (Year 2) to differentiate groups throughout the
experiment.
Data collection
We monitored stocked populations throughout the season to assess growth, condition, and mortality. Monthly,
we set five minnow traps overnight in each pond half;
setting of traps 1 day after stocking showed that this level
of sampling could catch up to 90% of the stocked fish
present (R. Vandenbos and W. Tonn, unpublished data).
Captured fish were counted, identified by their mark,
measured (TL), and returned to the ponds.
Throughout the spawning season, we examined nest
boards daily to quantify the production and fate of eggs.
For every egg batch, we recorded its date of appearance,
mapped its location, and determined the number, stage
of development, and state (healthy, diseased, depredated) of all eggs. Based on previous observations, we
assigned eggs into three developmental stages (Nagel
1976). Newly laid eggs were fairly opaque, containing
primarily yolk and lacking eye development in the embryo. In the second stage, eyes were visible and eggs
were about half full of yolk. In the final stage, eggs were
strikingly gold-tinted (from retinal development) and
hatched quickly (within 24–48 h).
To quantify egg production, we identified any egg
batches with eggs in the first stage of development that
had appeared since the previous day. The total numbers
of eggs in these batches were determined daily by
counting up to 200 eggs, determining the area that this
number of eggs occupied, and extrapolating to the area
of the entire batch (similar to Forsgren et al. 1996). Any
eggs laid in a dispersed manner were counted individually. Therefore, we were able to keep track of individual
batches and could quantify the total number of eggs laid
in each pond half every day.
We monitored the fate of egg batches from the time
they were laid to the time they disappeared. Diseased
eggs became white and opaque or showed evidence of
fungal hyphae and lingered for many days before disappearing. Healthy egg batches that disappeared suddenly before the third stage of development could not
have hatched and were recorded as depredated. Eggs
that disappeared after reaching the third developmental
stage were recorded as hatching successfully.
In Year 2, we sampled the successfully hatched YOY
in five equally spaced 2.5-m horizontal net hauls, with
nets (0.4 m diameter, 1 mm mesh) pulled at a speed of
approximately 0.75 m/s, ca. 1 month after hatching began. This allowed us to determine mid-season size distributions of YOY fish in each pond half and to monitor
their densities. All YOY caught were preserved in 95%
ethanol.
In the fall of both years, ponds were drained to ca.
30 cm depth and fish were censused by removal. Adults
were removed by 3 days of minnow trapping (prior to
draining) and seining (following draining). YOY fish
were removed with shore-to-shore seine hauls. Seining
continued until two hauls in a row produced fewer than
five fish. All fish removed were preserved in 95% ethanol. These fish were later counted, weighed, and measured (TL) to determine recruitment rates, final sizes,
and conditions (mass/length3Æ100) of YOY fish. Ice-up
occurred within 2 weeks of removal of fish in both years.
Analyses
Because treatments were paired within ponds, paired t
tests were used for comparisons of average or total
measures (survival of stocked adult males, total and per
capita egg production, number and proportion of eggs
surviving to hatch, YOY final abundance, survival, final
size and condition, and coefficient of variation of final
YOY sizes). All proportion data were arcsine squareroot transformed. Mid-season length distributions of
YOY, measured only in the second year, were compared
between treatments within each pond separately (n=2)
using Kolmogorov–Smirnov two-sample tests. In Year
2, one pond flooded in early August, shortly after the
mid-season sampling, mixing fish from the two treatments. This reduced the number of pond-year replicates
to three for YOY survival, final length, mass and condition, but not egg production, hatching or mid-season
576
growth (n=4). Statistical analyses used are outlined in
Sokal and Rohlf (1981).
70
LDS HDS
Pond 1-94
Pond 2-94
Pond 1-95
Pond 2-95
Results
60
Density differences of stocked fish were maintained between treatments throughout the experiment in both
years. Although there were the expected declines in catch
rates due to post-spawning mortality, catches were always at least three times higher in the pond halves with
the high stocked fish density treatment (HDS) versus the
low stocked fish density treatment (LDS) during the
monthly trappings. Adult male survival at the end of the
season was, in fact, higher in the HDS (17±11%,
mean ± SE) than in the LDS treatment (6±6%; paired
t test t=2.52, df=2, P=0.04).
There were too few mature males and females
remaining at the end of the season, likely due to high
post-spawning mortality, to assess adult growth. The
two stocked juvenile size-classes, however, grew consistently better in the LDS treatment than in the HDS
treatment (Fig. 1). As a result, final lengths of juveniles
were longer in LDS pond halves than in the HDS pond
halves for both large (65.2±0.5 vs. 59.4±1.0 mm,
respectively) and small size classes (64.6±2.1 vs.
57.7±1.0 mm, respectively).
Egg production and hatching success
Males were observed guarding territories under nest
boards within 2 days of stocking and the first egg batches appeared within 1 week in both years. Egg laying
and hatching tapered off mid to late July, with the last
eggs seen on 4 August. The number of egg batches
present at any one time peaked during the first 2 week of
the reproductive season, yet there were always empty
nest sites. The maximum number of batches observed
per board simultaneously was 13, but 5–6 batches on a
board was more usual. Surprisingly, empty nest sites
were especially common in the HDS treatment, where
there were usually less than 3–4 egg batches per board,
especially after the first week. Consistent with this, fewer
eggs were produced in HDS pond halves (26323±4634,
mean ± SE) than in LDS halves (32108±4991). As a
result, there was a strong density-dependent difference in
per capita egg production (mean difference (within
ponds)=212±33 SE; paired t test t=6.5, df=3,
P=0.004), with eggs laid per stocked fish in the HDS
treatment being less than 1/4 of the amount in the LDS
treatment (Fig. 2a).
In addition to density-dependent egg production,
there were dramatic differences between treatments in
the fate of eggs (diseased, predated, hatched). Only
1–5% became diseased, with no obvious difference
between treatments. Instead, most losses involved the
Total length (mm)
Stocked fish
a. Large juveniles
50
0
70
60
50
b. Small juveniles
0
INITIAL
JUN
JUL
AUG
SEPT
Fig. 1 Summer growth (mean total length ± SE) of a large and b
small juvenile fathead minnows (Pimephales promelas) stocked into
two experimental ponds in 1994 and 1995 at low (LDS) and high
(HDS) densities, 1 and 4 fish m 2, respectively. Data for pond 1–95
are absent for August and September due to mid-season flooding.
Initial measurements were taken on May 26–28
sudden disappearance of entire batches, beginning
within 3 days of laying and well before development
could be completed. These events were clearly the result
of predation. In the HDS treatment, schools of stocked
fish were frequently observed mobbing nest-guarding
males and chasing males off their territories. After such
encounters, we always observed signs of egg predation,
with partially eaten eggs and other debris being all that
remained of egg batches. Consequently, survival of eggs
to hatch was lower in the HDS treatment than in the
LDS treatment (mean difference (within ponds) =
0.58±0.1 SE; paired t test t=5.04, df=3, P=0.007;
Fig. 2b). As a result, the number of eggs that successfully hatched in HDS averaged <20% of the number in
the LDS pond halves (HDS mean ± SE=4677±2143,
LDS=25161±5097).
Young-of-the-year growth and survival
Mid-season net hauls of YOY yielded dramatic differences between treatments in Year 2. Not surprisingly,
given the differences in the number of eggs that were
hatching, many more YOY were netted in the LDS than
in the HDS treatment (Fig. 3). These samples also
Egg production (no. per stocked fish)
577
a
300
200
100
0
Proportion of eggs that hatched
1.0
b
0.8
0.6
0.4
0.2
pond halves in the fall (paired t test, t=2.23, df=2,
P=0.15).
Overall, survival of YOY from hatching to ice-up was
higher in the HDS treatment (mean difference (within
ponds) = 0.44±0.07 SE; paired t test t=7.14, df=2,
P=0.019; Fig. 2c). As a result, numbers of YOY in the
fall converged between treatments; five of the six pond
halves had 1,850–5,000 YOY regardless of treatment
and no treatment effects were detected (number of YOY
at ice-up: HDS mean ± SE=2991±1119, LDS=2050
±960; paired t test, t=0.69; df=2; P=0.56). The
exception was the LDS treatment in Pond 2–95, which
had very few YOY (n=200) in the fall. Interestingly, this
pond half had the highest initial number of fry. Indeed,
when we compared mortality of YOY between treatments using initial number of hatched YOY as a covariate, the latter explained the majority of the
variability in mortality (ANCOVA: F=41.74; df=1, 3;
P=0.008), relegating the effect of stocked fish density
(HDS vs. LDS) to a marginal role (F=9.3; df=1, 3;
P=0.06). The relationship between the number of surviving YOY versus initial number of YOY was unimodal, best fit by a quadratic equation that explained 89%
of the variation in YOY survivors, indicating that total
survivors decreased as initial numbers increased beyond
ca. 15,000 (Fig. 4a).
0.0
Proportion of YOY survivors
0.8
c
35
Pond 1-95
LDS n=107
HDS n= 11
30
0.6
25
20
0.4
15
0.2
10
LDS
HDS
Fig. 2 Reproductive success of fathead minnows in two experimental ponds in 1994 and 1995 with low (LDS) and high (HDS)
densities: a per capita egg production, b proportion of eggs laid that
hatched and c proportion of young-of-the-year (YOY) that
survived from hatching until fall. See Fig. 1 for explanation of
symbols
YOY (no.)
5
0.0
0
25
Pond 2-95
LDS n=50
HDS n=10
20
15
10
5
revealed an intracohort density effect on YOY growth.
In both ponds, length-frequency distributions differed
between treatments (Kolmogorov–Smirnov two-sample
tests Pond 1: D=0.629, P=0.001; Pond 2: D=0.68,
P<0.001), with lengths of HDS YOY generally greater
than lengths of LDS YOY (Fig. 3). Although we could
not assess if there was a comparable mid-season density
effect on condition of YOY (mass was not measured),
there was a trend for condition to be greater in HDS
0
6
8
10
12
14
16
18
20
22
24
26
Total length (mm)
Fig. 3 Mid-season (July 15) length-frequency distributions of
young-of-the-year (YOY) fathead minnows in Ponds 1 and 2 with
low (LDS, shaded bars) and high (HDS, open bars) densities of
stocked fish in 1995. Sampling effort was equal in all pond halves,
therefore, sample sizes should reflect relative densities of YOY
578
Despite strong mid-season differences in growth, sizes
of YOY that survived to the fall had converged between
HDS and LDS populations (HDS mean ± SE=21.9±1.8 mm, LDS=22.1±2.2 mm; paired t test,
n=3: t=0.29, P=0.79). Similarly, there was no relationship between final mean size and initial number of
YOY (Regression F=0.30; df=1, 4; P=0.61). Likely as
a consequence of differences in intra-cohort densitydependent selective mortality, however, the coefficient of
variation of the final mean size (TL) of YOY was
strongly related to initial number of YOY (Fig. 4b).
Final sizes were less variable in cohorts with higher
initial densities and higher post-hatch mortality.
Discussion
The populations of fathead minnows in this study
exhibited very strong density-dependent processes at a
6000
a
YOY survivors (no.)
5000
4000
3000
2000
1000
number of different life-history stages. We documented
density-dependent growth of stocked fish and observed
strong density-dependent effects on per capita egg production, egg survival to hatch, mid-season size structure
of YOY minnows, and YOY survival. Despite initial
stocking densities that differed by fourfold, interactions
and interdependencies of stage-specific processes in each
treatment ultimately resulted in a convergence of
abundance and average length of YOY by the end of the
season. Although similar, these recruitment outcomes
were achieved via alternative pathways, with densitydependent processes acting most strongly on the egg
stage in HDS populations and on the larval stage at low
stocking densities. Because the dominant densitydependent processes differed, however, in their (size)
selectivity, the two treatments produced cohorts of
young that differed in body size variation.
The loss to flooding of one pond (1–95) eliminated
our replicate for that pond and year for end-of-season
measurements and introduced the possibility that endof-year (but not earlier) results were being driven by
either the remaining pond or the 1994 data. However,
examination of the end-of season results from individual
pond-years showed that treatment effects, when present,
were strong and consistent, not driven by a single year or
pond. Furthermore, fathead minnows stocked at nearly
the same density as the LDS treatment in a subsequent
year (and in different pond halves; Grant and Tonn
2002) produced mean values for number of eggs laid per
stocked fish (441), proportion of eggs that hatched
(0.81), and proportion of YOY surviving to ice-up (0.04)
that are consistent with our LDS results and inconsistent
with our HDS results.
0
CV (final YOY length)
35
b
30
25
20
0
0
5
10
15
20
25
30
35
Initial number of YOY (thousands)
Fig. 4 a Number of young-of-the-year (YOY) fathead minnows
from a given pond-year that survived over the summer as a
function of initial number of YOY that hatched. The quadratic
regression equation is: Number of survivors=330.52+0.57(initial
no. YOY) 1.89E-05(initial no. YOY)2; R2=0.89 (F=12.4, df=5,
P=0.04). b Coefficient of variation (CV) of final (fall) lengths of
young-of-the-year (YOY) fish from a given pond-year as a function
of the initial number of YOY. The regression equation is:
CV=35.8 5E-4 (initial no. YOY); R2=0.92 (F=56.3, df=5,
P=0.001). See Fig. 1 for explanation of symbols
Density-dependent effects on the stocked fish
Density-dependent mortality is common in early lifestages of fish, whereas growth and reproduction are
the density-dependent traits more often observed later
in life (Charnov 1986; Lorenzen and Enberg 2002);
this was also the case in our experiment. Overall, per
capita mortality of stocked fish was similar for HDS
and LDS populations, therefore, the treatment (high
and low stocked fish density) was maintained
throughout the experiment. The slightly higher survival of adult males in the HDS than in the LDS
treatment could well have been due to reduced
reproductive investment, and therefore reduced postreproduction mortality, in the HDS treatment (Andrews and Flickinger 1974). Growth of stocked fish
was, however, strongly reduced in the HDS treatment,
most likely related to exploitation competition among
the stocked fish (Tonn et al. 1994). Adult fathead
minnows tend to take bigger prey than juveniles (Price
et al. 1991) but otherwise feed on a similar prey base
(chironomids, copepods, cladocerans, and detritus),
with moderate to high overlap in diets (Schoener’s
(1974) diet overlap index=0.55–0.81; Janowicz 1999),
579
suggesting the possibility for strong competitive effects
among the stocked fish cohorts.
Density-dependent effects on other life-history stages
Our results indicated that the density of stocked fish also
interacted, directly or indirectly, with other life-history
stages to affect the recruitment pattern of YOY fish. The
strong density-dependent effect on per capita egg production, for example, was likely due to greater interference at establishing and maintaining nesting
territories in HDS (Danylchuk and Tonn 2001), rather
than to differences in fecundity between HDS and LDS;
there were no initial differences in adult sizes and condition between treatments that would influence fecundity and adults began reproducing within a week of
being stocked. Interference is also consistent with the
higher survival of adult males that we observed in the
HDS treatment (Andrews and Flickinger 1974). We also
noted that a number of egg batches in the HDS treatment only had 5–10 eggs in them (versus an average of
ca. 300 for both treatments), suggesting that spawning
attempts were aborted. Finally, the greater growth of
stocked juveniles in LDS pond halves likely allowed
some to mature and reproduce, especially later in the
protracted spawning season (Danylchuk and Tonn
2006), and thus contribute to the greater per capita
production of eggs in LDS.
In contrast, the availability of nesting sites was unlikely to have limited egg production in HDS pond
halves. Nest territory size is very compressible in fathead
minnows and many males will communally guard
adjacent egg batches at good sites where nests are clustered (Andrews and Flickinger 1974). In terms of surface
area, we provided more nesting substrate than the
amount required by males (Flickinger 1973), even
assuming that every stocked male in HDS established a
nest; indeed, we observed empty nest sites every day.
Greater per capita egg production in the LDS treatment, in fact, slightly overcompensated for differences in
the density of stocked fish. Although the once-a-day
sampling regime might have missed some batches of eggs
produced and eaten in the same day, it was relatively
rare to observe signs of a depredated nest (e.g., partially
eaten eggs, egg debris) where we had not observed an
egg batch the day before.
There was also a strong interaction between stocked
fish density and egg survival. Most, if not all, of the
difference in egg survival was likely due to cannibalism
by stocked fish. There were no other vertebrate predators in the ponds, and daily observations and monthly
minnow trapping revealed no obvious differences in the
numbers of potential invertebrate predators, e.g., dytiscid beetles and odonate larvae (R. Vandenbos and
W. Tonn, personal observation). Instead, the large
numbers of conspecific egg predators in high-density
ponds appeared to frequently overwhelm guarding
males (Hyatt and Ringler 1989; R. Vandenbos and
W. Tonn, personal observation). Although males defended
their nests more actively in the high-density treatment
(R. Vandenbos, personal observation), reductions in
male condition due to the increased (and continual)
defence activities could have limited the ability to
successfully sustain nest defence (Unger 1983). Finally,
because food was likely more limiting in the HDS
treatment, eggs likely became a valued food item
(Polis 1981).
Initial post-hatch differences in density of YOY fish
were still present during the mid-season sampling,
which also had indicated intra-cohort density-dependent early growth of YOY. By the end of the season,
however, both mean size and density of YOY had
converged between treatments. Clearly, YOY in LDS
treatments experienced higher mortality after mid-season and this density-dependent mortality was selective
based on size (Post and Prankevicius 1987) or growth
rate (Rice et al. 1993). Not only had final mean sizes
converged, but variability of the final size distributions
was inversely related to mortality rate of YOY during
this life-history stage.
Adult fathead minnows can cannibalize YOY in a
size-limited manner in the laboratory (Vandenbos 1996);
the intra-cohort density-dependent growth of YOY at
mid-season meant that the slower growing YOY in LDS
would have been more vulnerable to this source of
mortality than the HDS YOY. Starvation was also a
likely source of size-selective mortality (Frank and
Leggett 1994); the density-dependent growth that YOY
fish were experiencing is often an indication of poor food
availability (e.g., Fox et al. 1989). Indeed, nutrient
enrichment (leading to increased food availability) increased the number of YOY fathead minnows surviving
to the end of the season by more than fivefold in another
study (Grant and Tonn 2002). Clearly, the two mechanisms are not mutually exclusive, as small fish in poor
condition are more susceptible to predation, as well as to
starvation (Sogard 1997). Either way, intra-cohort density-dependent competition appeared to be ultimately
behind the large difference in YOY mortality between
treatments.
The convergence of final average lengths of the
YOY, despite the mid-season differences, was, in turn,
a consequence of the density-dependent, size-selective
mortality of YOY in LDS, which also produced the
strong intra-cohort density-dependent variability in the
final size distributions (see also Elliott 1990). This difference in size variation at ice-up could have significant
recruitment consequences. An important source of
mortality for YOY fish is the overwinter period, especially for populations like fathead minnows in Alberta,
near the northern limit of the species’ range (Shuter
and Post 1990; Munch et al. 2003). Overwinter mortality can result from depletion of energy reserves (Post
and Evans 1989) and lowered osmoregulatory ability
(Johnson and Evans 1996), both of which are influenced by body size and condition (with smaller individuals faring worse), and by the length and severity of
580
the winter (Sogard 1997). Indeed, strong size-selective
mortality was displayed by YOY allowed to overwinter
in these same experimental ponds in another experiment (Grant and Tonn 2002). Although YOY around
20 mm in length comprised a substantial proportion of
the cohort in the fall (similar to our study, where mean
length was ca. 22 mm), most survivors in the spring
were >29 mm, and none were <20 mm. Thus, sizeselective overwinter survival should have different
consequences for populations with the same mean size
but different variation in size; similar consequences of
variation have been suggested with size-dependent
predation (Rice et al. 1993).
The specific minimum threshold size needed to survive the winter period will differ from 1 year to the next,
reflecting differences in the length or severity of the
winters (see also Danylchuk and Tonn 2003). Whether
cohorts with broad or narrow size distributions would
display greater recruitment would thus depend on the
mean size that the cohort achieved in the fall, and the
threshold size required for overwinter survival.
Conclusions
Although it is commonly accepted that processes acting
during the first year of life are of critical importance to
recruitment in fish (or other stage-structured) populations (Sinclair 1989), there are actually several life-stages
during the first year, e.g., eggs, larvae, post-larval YOY,
each of which can have stage-specific processes that may
be important directly or through interactions with other
stages and cohorts. Therefore, it should be rewarding to
understand what those stage-specific processes are and
how density-dependent processes can interact among
stages to drive recruitment patterns.
In our experiment, variability in end-of-summer
YOY size distribution was ultimately related to the lifehistory stage at which the dominant density-dependent
processes occurred, and whether or not those processes
were size-selective. In the HDS treatment, the dominant
density-dependent processes occurred during the egg
stage, with little or no size-selectivity; this led indirectly
to a final YOY size distribution that was more variable.
In the LDS treatment, the dominant process(es) occurred during the YOY stage, resulting in strong sizeselective mortality; this, in turn, produced a YOY cohort
that was less variable with respect to size.
Although the processes acting on different life stages
can be distinct, the stages themselves are not independent. Outcomes of processes that act, or fail to act,
during one stage will ‘cascade’ to subsequent stages, in a
manner analogous to interactions among trophic levels
in a food chain (Carpenter et al. 1985), by contributing
to the traits of subsequent stages and to the biotic
environment in which these later stages must operate
(Fig. 5). Such cascading processes can continue to shape
populations for years (Hamrin and Persson 1986; Sanderson et al. 1999).
a. Low density
Adult
b. High density
Reproductive
inhibition or
interference
Egg
Adult
Egg
Cannibalism
Larval
Larval
Starvation
Predation
FYOY
J2
FYOY
Overwinter
mortality
J2
Fig. 5 Flow diagram illustrating the alternative outcomes of
cascading density-dependent processes important to different lifehistory stages of fathead minnows, which interact to affect YOY
recruitment in populations with: a low density, and b high density
of older age-classes. Sizes of boxes represent relative densities at a
given stage; width of horizontal (no fill) arrows reflects the
importance of processes that influence the transition of individuals
from one stage to the next. Width of vertical (black fill) arrows
reflects the magnitude of the per capita rates represented by the
arrows. Processes highlighted in bold are size-selective. Dashed lines
indicate uncertain outcomes. FYOY=YOY in the fall; J2 = juveniles at the beginning of the second growing season
The relative strengths of processes that act and
interact during this cascade of life-stages, and the different outcomes that these processes can produce, indicate that a focus on a single life-history stage can restrict
our understanding of recruitment and population
dynamics. To better understand population regulation
in species with stage-structured life histories, we need to
consider not only the mechanisms that act during individual life-history stages, but how stages interact.
Acknowledgements We gratefully acknowledge M. Janowicz,
S. Grant, K. Vladicka, and L. Rempel for field assistance, and
S. Boutin, M. Mangel, E. Marschall, C. Osenberg, C. Paszkowski,
J. Post, J. Roland, B. Wilson, and an anonymous reviewer for
constructive comments and advice. This research was generously
supported by grants to REV from the Electric Power Research
Institute, Canadian Circumpolar Institute, and Alberta Conservation Association (Biodiversity Challenge Grant), a capital equipment grant to Meanook Biological Research Station, and by a
Research Grant from the Natural Sciences and Engineering Research Council of Canada (NSERC) to WMT. REV was supported
by an NSERC Post-Graduate Fellowship, assistantships from the
Department of Biological Sciences, and professional development
funding from Selkirk College. The research was conducted under
an animal care permit issued by the Biosciences Animal Policy and
Welfare Committee, University of Alberta, and collection and
research permits issued by Alberta Fish and Wildlife.
581
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