Download Body size distributions in North American freshwater fish: smallscale

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Ecology of Freshwater Fish 2013: 22: 257–267
ECOLOGY OF
FRESHWATER FISH
Body size distributions in North American
freshwater fish: small-scale factors and synthesis
David Griffiths
School of Environmental Sciences, University of Ulster, Coleraine BT52 1SA, UK
Accepted for publication November 26, 2012
Abstract – The ecosystem size/trophic structure hypothesis predicts that the shape of body size distributions will
change with ecosystem size because of increases in the relative importance of large, predatory, species. I test the
hypothesis by examining the statistical moments, as measures of shape, of species body size distributions of North
American freshwater fish assemblages in lakes. Species lists, coupled with dietary and body size information, are
used to document the patterns. Body size distributions in small lakes are unimodal and right-skewed, but
distributions become more symmetrical and bimodal in large ecosystems. In small lakes, body sizes are generally
small and fish trophic levels low, but size and trophic level increase up to lake volumes of about 0.001 km3, and
change little in larger lakes. Adding trophic level to the analysis greatly improves the variance explained by the
body size–lake size relation. The conclusions of Griffiths (2012, Global Ecology & Biogeography 21: 383-392),
that postglacial recolonisation and evolutionary change are important determinants of body size distributions at
regional and larger scales, are combined with those of this study. Mean body size in local assemblages of lakedwelling species is larger than in regional and continental ones. Overall, body size distributions are affected by
processes operating at a variety of spatial and temporal scales, with the type, size and duration of the ecosystem
probably playing a central role by influencing the proportions of vagile and predatory species, the species which
dominate the large size mode.
Key words: ecosystem size; trophic structure; skewness; kurtosis; bimodality
Introduction
A variety of energetic, evolutionary, biogeographic
and ecosystem processes have been suggested to
influence the shape of species body size distributions
(Allen et al. 2006). Both physical constraints and
biotic interactions affect the body size distributions of
the species assemblages that occur in aquatic, and
other, ecosystems. Large species require large home
ranges (Minns 1995; Woolnough et al. 2008) and
tend to be predatory (Brose et al. 2006; Cohen 2007;
Romanuk et al. 2010). Physically larger ecosystems
support more (the species-area relation; Rosenzweig
1995) and larger species, for both energetic and population dynamic reasons, while food chain length
(FCL) has been suggested to increase with ecosystem
size and/or ecosystem productivity (Schoener 1989;
Cohen & Newman 1991; Holt 1993; Vander Zanden
et al. 1999). Tests, mainly in lakes and streams, but
also in experimental microcosms, pitcher plants and
islands, have found support for the ecosystem size
hypothesis (Spencer & Warren 1996; Vander Zanden
et al. 1999; Post et al. 2000; Thompson & Townsend
2005; Takimoto et al. 2008; Doi et al. 2009;
McHugh et al. 2010; Baiser et al. 2012).
I extend this hypothesis by predicting a correlation
between the shape of body size distributions and ecosystem size. The moments of size frequency distributions, i.e., mean, standard deviation, skewness and
kurtosis, can be used to describe distribution shape.
The greater range of trophic levels, and consequently
higher mean trophic levels, in large ecosystems
should, because of the link between body size and
trophic level, be accompanied by a greater body size
range. The smallest ecosystems will support few,
probably small, species, low population sizes of large
species increasing the risk of stochastic extinction
(Gaston 1994). As ecosystem size increases larger
Correspondence: David Griffiths, School of Environmental Sciences, University of Ulster, Coleraine BT52 1SA, UK. E-mail: [email protected]
doi: 10.1111/eff.12023
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David Griffiths
species can persist, so the mean and standard deviation of assemblage body size will increase. As some
of these larger species will be predatory, they will
tend to reduce the abundance and/or occurrence of
smaller species (Rahel 1984; Robinson & Tonn
1989; Chapleau et al. 1997; Magnuson et al. 1998;
Pace et al. 1999), thereby reducing skewness and
kurtosis if the modal sizes are more likely to be
eaten. Griffiths (1986) and Marquet et al. (2008) have
suggested that this process (termed species stacking
and hitch-hiking, respectively) can generate bimodal
distributions. Hence, species stacking occurs because
most predators consume prey that are distinctly smaller than themselves (Vezina 1985; Cohen et al.
1993), so that a basal mode of small abundant prey
can support distinctly larger size modes at higher trophic levels. Marquet et al. (2008) simulated this process: initially uniform and overlapping predator and
prey size distributions diverged over time to generate
a bimodal distribution (their fig. 4.5). Hence, the
inclusion of trophic structure in the ecosystem size
model suggests that once predators can be maintained
(above an ecosystem size-dependent threshold), there
will be a change in body size distribution shape and
number of modes.
Here, I consider the role of ecological (ecosystem
scale) processes in determining species assemblage
body size distributions of North American freshwater
fish (NAFF). I document how fish size distributions
vary with ecosystem size in lakes and evaluate the
ecosystem size hypothesis as a predictor of those patterns. To test the model, fish body size distributions
and trophic structure are examined across a wide range
of lake sizes. Griffiths (2012) concluded that postglacial recolonisation by large, habitat generalist, migratory species was the main determinant of latitudinal
size distribution trends while new, small, species were
most likely to evolve in small streams. A final section
examines the contributions of those regional and continental scale factors and the more local processes
examined here in determining fish size distributions.
Methods
Data
This article follows the procedures described in Griffiths (2012). Size distributions were determined from
published species lists from 387 lakes (Supporting
information Table S1). Page & Burr (1991) was the
primary source of information on maximum fish (total)
lengths. Species with log length 1.5 (31.6 cm), the
position of the trough between modes (Griffiths
2012), were identified as large mode species.
To test the ecosystem size/trophic structure hypothesis, I determined how the moments of species size
258
frequency distributions and diet changed with ecosystem size. Fish can show considerable intraspecific
size variation across ecosystems, but because of the
scarcity of system-specific body size measures, I used
species values. In one test, maximum lengths for fish
caught in multipanel gill nets in Lough Neagh, Northern Ireland (Griffiths, unpublished) were correlated
with the Europe-wide values recorded by Maitland
(2000)(r = 0.86, n = 11, P < 0.001), suggesting that
continental values are adequate. Maximum, rather
than mean, species length is preferred as, because
prey size increases with body size, it is more likely to
reflect the maximum trophic level attained by the species. These two size measures are linked: from data
in Maitland (2000) for European fish, ‘typical’ species length is strongly correlated with maximum
length (r = 0.96, n = 203, P < 0.001). Although size
distributions can be examined at a variety of taxonomic levels, I used the species level for pragmatic
reasons (more data are available). Species stacking
depends on the abundances of different-sized species.
There is an extensive literature on size–abundance
relations, with larger aquatic species (Strayer 1994;
Cyr 2000; Schmid et al. 2002; Jonsson et al. 2005)
and individuals (Kerr & Dickie 2001; de Eyto &
Irvine 2007) being rarer, so species size also contains,
admittedly crude, abundance information.
As Post et al. (2007) make clear, defining ecosystem
size is not straightforward. In all but the smallest lakes,
water depth has a significant structuring influence
(Moss 1998). When testing the hypothesis, volume,
estimated as the product of lake area and the most
widely available depth measure, maximum depth, was
used: maximum depth is strongly correlated with mean
depth (r = 0.86, n = 184, P < 0.001).
The ecosystem size hypothesis argues that longer
food chains occur in larger ecosystems. FCL, i.e., the
number of times energy is transferred from the bottom to the top of the food web, has usually been calculated from stable isotope analyses although
Thompson & Townsend (2005) calculated it from
food web structure. I used broad dietary categories to
identify trophic levels and the range of trophic levels
within a system to estimate FCL. From information
in Scott & Crossman (1973), Coker et al. (2001) and
FishBase (FishBase 2004) adult fish were scored as
plant feeders (1), invertebrate feeders (2) or piscivores (3): species consuming more than one of these
categories as adults were given median scores. This
is a crude measure of diet as, for example, a species
consuming all three food categories would receive
the same score as one specialising on zooplankton or
on benthic invertebrates, and it ignores size-linked
shifts in diet: nevertheless, it gives an indication of
the species trophic position. As a check on the validity of this procedure, I regressed these diet scores
Body size distributions in freshwater fish
against the trophic levels estimated from the more
detailed diet composition in FishBase (FishBase
2004, p181). Scores and trophic levels are correlated
(r = 0.79, n = 137, P < 0.001), but I used the score
data because they included a greater range of species.
Lake assemblage trophic level scores were calculated
as means of species diet scores.
Analyses
In line with previous studies, body sizes were log10transformed, for practical and theoretical reasons
(Griffiths 2012). The shapes of body size distributions are described by their moments [mean, variance
(SD2), skewness (g1) and kurtosis (g2)]: for practical
reasons, I used the standard deviation (SD) as a measure of the second moment. Positive values of skewness indicate right-skewed distributions. Positive
kurtosis (leptokurtosis) indicates distributions, which
are more peaked than a normal distribution while
negative values (platykurtosis) occur when frequencies around the mean are less than expected for a normal distribution: negative kurtosis might indicate
bimodality in the data. It is more difficult to detect
significant kurtosis than significant skewness as the
standard error of g2 is twice that of g1 for a given
sample size. Statistical tests for deviations from
unimodality, e.g., Hartigans’ dip test tend to be conservative, sensitive to nonnormality and spatial separation of the modal groups, and to sample size
(Jackson et al. 1989; Cheng & Hall 1998)(Supporting
information Fig. S1). Analysis of dip statistic values
for large lakes (which are expected and tend to exhibit bimodal size distributions) shows that they vary
with kurtosis and sample size, but are very conservative (Supporting information Table S2). Consequently, I report only values of kurtosis and note that
platykurtic distributions are not necessarily bimodal.
To test whether trends in body size moments were
simply due to changes in species richness, 100 samples for lakes with 2–128 species, a richness range
which covers the range of lake sizes in the data, were
taken at random from the observed lake continental
species pool and the means of moments calculated
for each richness class. I also tested whether the
moments could be generated by randomly sampling
from different body size ranges (log size ranges from
0.2–2.2, in steps of 0.2) of the size distributions for
NAFF species found in lakes.
All lengths are in cm, logarithmic transformations
are to the base 10, all interval estimates are standard
errors, all correlations are parametric (r) and all nonlinear trend lines in the figures are fitted by locally
weighted scatterplot smoothing (LOWESS). To test
for nonlinearity, the fits of piecewise (Toms &
Lesperance 2003) and linear regression models were
compared using the small sample Akaike Information
Criterion (AICc).
Results
There are clear relationships between the moments of
the size distributions in lakes (Fig. 1, left). Broadly
similar, although less extreme, relationships are produced by random sampling from different size ranges
of lacustrine species (Fig. 1, right), i.e., the observed
trends are, at least in part, a consequence of the shape
of the source species size distributions. Kurtosis is
strongly correlated with skewness, but note that platykurtic assemblages tend to be of average size (Fig 1c)
and symmetrical in size (Fig 1d): inspection of histograms confirmed these assemblages to be bimodal
(see Supporting information Fig. S2 for examples).
Mean body size rises with lake volumes up to
about 0.001 km3, but it and the other moments show
little change in larger lakes (Fig. 2). Species richness
(Fig. 3a) and maximum body size in assemblages
increase rapidly with lake volume, whereas minimum
size shows a less-marked, but significant, decline
(Fig. 3b; r = 0.61,
0.31, n = 261, P < 0.001,
respectively). As with the moments, these trends are
not linear, but change in slope at lake volumes of
about 0.001–0.01 km3: for all these variables, twoline piecewise models show better fits than one-line
models (DAICc 7.8–86.0).
There is considerable variability in the mean fish
size–lake volume relationship, particularly in small
lakes. The hypothesis predicts that this relationship is
a consequence of changes in trophic level rather than
species richness. In both small and large lakes, mean
size increases with lake size and mean trophic level
(proportion of predatory species), as predicted by the
hypothesis (Table 1). Trophic level has about three
times the effect of lake size and addition of mean trophic level to the model increases the variance
explained considerably, whereas richness has no
effect (DAICc small and large lakes 208.3, 105.7,
respectively). Kurtosis shows a U-shaped relation
with mean body size (Fig. 1c) with the majority of
leptokurtic assemblages dominated either by small or
large mode fishes. Assemblages in the smallest lakes
are dominated by small mode fishes (Fig. 2a; log
means around 1.1–1.2), but in large lakes, fish size
distributions are platykurtic (Fig 2d) and bimodal
(Fig. 4). Across North American lake-dwelling species, diet score increases with body size (r = 0.49,
n = 183, P < 0.001). The mean trophic level of fish
assemblages varies with lake volume (Fig. 3c) in a
similar way to mean size, with a piecewise model
showing a better fit than a linear one (DAICc 32.0).
This is unsurprising given the strong relationship
between mean assemblage trophic level and mean
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David Griffiths
Observed
0.6
(a)
0.5
Predicted
0.6
0.5
0.4
SD
0.4
0.3
0.3
0.2
0.2
0.1
0.0
0.1
1.0
1.2
1.4
1.6
1.8
2.0
1.0
1.2
Mean length
(b)
3
1.6
1.8
2.0
1.8
2.0
1.8
2.0
3
2
Skewness
2
Skewness
1.4
Mean length
1
0
1
0
–1
–1
–2
–2
1.0
1.2
1.4
1.6
1.8
2.0
1.0
1.2
Mean length
1.4
1.6
Mean length
(c)
5
5
4
3
3
1
Kurtosis
Kurtosis
2
0
–1
1
–1
–2
–3
–3
–4
–5
–5
1.0
1.2
1.4
1.6
1.8
2.0
1.0
1.2
Mean length
1.4
1.6
Mean length
(d)
5
5
4
3
3
1
Kurtosis
Kurtosis
2
0
–1
1
–1
–2
–3
–3
–4
–5
–5
–2
–1
0
1
Skewness
260
2
3
–2
–1
0
1
Skewness
2
3
Fig. 1. Observed (left) and modelled (right)
relationships between the mean and (a)
standard deviation (SD), (b) skewness, (c)
kurtosis and (d) between skewness and
kurtosis, for body lengths of fish found in
lakes. Lowess smoothers (tension 0.5) have
been fitted to the data points.
Body size distributions in freshwater fish
2.0
0.6
(a)
(b)
0.4
1.5
SD
Mean length
0.5
0.3
0.2
1.0
0.1
0.0
0.5
–5 –4 –3 –2 –1
0
1
2
3
4
3
–5 –4 –3 –2 –1
5
0
1
2
3
4
5
(c)
5
(d)
4
2
3
Kurtosis
Skewness
2
1
0
1
0
–1
–2
–1
–3
–4
Fig. 2. The moments of fish size distributions
vary with lake size in 387 N. American
lakes. Lowess smoothers (tension 0.5) have
been fitted to the data points.
–2
–5
–5 –4 –3 –2 –1
0
1
2
3
4
5
–5 –4 –3 –2 –1
0
1
2
3
4
3
1.5
Log body length (cm)
Log (number of species + 1)
2.0
1.0
0.5
2
1
(a)
(b)
0.0
0
–5 –4 –3 –2 –1
0
1
2
3
4
5
–5 –4 –3 –2 –1
Trophic level range
Trophic level
0
1
2
3
4
5
3
3
Fig. 3. (a) Fish species richness, (b) mean
body size, (c) mean trophic level of species
assemblages and (d) the range in trophic
levels within an assemblage, as functions
of lake volume. Lowess smoothed
minimum and maximum values for body
size and trophic level are also shown in (b)
and (c), but the data points are omitted for
clarity.
5
Log lake volume (km3)
2
2
1
(c)
(d)
0
1
–5 –4 –3 –2 –1
fish size (r = 0.86, n = 260, P < 0.001), although
there is also a small, negative, contribution of lake
volume (standardized coefficients 0.89,
0.10,
0
1
2
3
4
5
–5 –4 –3 –2 –1
0
1
2
3
4
5
Log lake volume (km3)
respectively). Minimum assemblage trophic level
declines with increasing lake size (Fig. 3c);
r = 0.50, n = 262, P < 0.001), i.e., a greater
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David Griffiths
Table 1. Summary of multiple linear regression statistics of mean body size for lakes below (n = 174) and above (n = 90) log lake volumes of 2.42
(0.006 km3, identified by piecewise regression of the data in Fig. 2a). The last three columns show R2 and AICc values for regressions with lake volume and
mean trophic level or species richness as predictors.
Standardised
coefficient SE
t
P
Predictor variables
Vol
Log volume 2.42
Log volume (Vol)
Log species (Spp)
Trophic level (TL)
R2
AICc
0.060 0.012
0.011 0.012
0.198 0.010
Log volume > 2.42
Log volume (Vol)
Log species (Spp)
Trophic level (TL)
R2
AICc
0.027 0.009
0.011 0.009
0.096 0.007
4.85
0.89
19.88
2.91
1.28
14.06
% Species (arcsine transformed)
40
30
20
10
0
0
1
2
3
Log length (cm)
Fig. 4. Percentages (open circles) of species constituting the various size classes for the 18 lakes analysed in Table S2: mean values (filled circles) (1 s.e.) are also shown. Over all lakes, there
are significantly fewer species in the intermediate size classes.
The histogram shows the distribution of mean body sizes across
the lakes. If the bimodality in species contributions was a consequence of lumping together lakes with large or small modal sizes,
the distribution of means should mirror that of the species contributions rather than occur between the modes.
proportion of herbivorous fish occur in large lakes.
Small lakes tend to have assemblages that feed at a
single, low, trophic level, but trophic level range
increases, nonlinearly, with lake size (Fig. 3d).
Discussion
Data and analysis limitations
The extended ecosystem size hypothesis is best tested
using location-specific measures of body size and tro262
Vol, Spp
Vol, TL
0.27
23.5
0.29
26.8
0.79
235.1
0.03
144.1
0.03
141.9
0.70
247.7
<0.001
0.38
<0.001
<0.01
0.20
<0.001
phic level for each species. Intraspecifically, body
size and trophic level can vary appreciably with latitude, climate, productivity and ecosystem size. Individuals growing in warmer environments are often
smaller than those in colder ones, i.e., Bergmann’s
Rule (Atkinson 1994; Huston & Wolverton 2011).
However, latitudinal variation in maximum body size
is uncommon in freshwater fish (3/28 species examined: Belk & Houston 2002; Blanck & Lamouroux
2007) despite a strong temperature trend with latitude,
and consequently is unlikely to alter the patterns discussed here. More productive ecosystems can support
higher trophic levels (Oksanen et al. 1981; Vander
Zanden et al. 1999) and ontogenetic dietary shifts in
more productive ecosystems would also be expected
from the ecosystem size hypothesis. Similarly, at least
some individual species tend to be larger in large
lakes (Alm 1946; Griffiths 1994; Ylikarjula et al.
1999; Purchase et al. 2005) and to feed at higher trophic levels (perch (Perca fluviatilis) (Alm 1946), arctic charr (Salvelinus alpinus) (Griffiths, unpublished),
lake trout (Salvelinus namaycush) (Martin & Olver
1980)), consistent with the ecosystem size hypothesis.
In the absence of location-specific measures, continental scale measures, i.e., species sizes permit a preliminary, though weaker, test of the hypothesis. Data
for one lake showed a strong correlation between the
location-specific and continental species sizes.
Blanchet et al. (2010) have shown that introduced
species tend to be larger than their native counterparts
(medians 33 vs. 12 cm respectively). These values
roughly correspond to the modal sizes observed in
assemblages (e.g., Fig. 4) and raise the possibility
that the bimodality is simply a consequence of introductions. However, the great majority of assemblages
analysed here consist only of, or are dominated by,
native species.
Body size distributions in freshwater fish
The observed and modelled relations between the
moments of the fish size distributions are of similar
shapes: a closer fit should not be expected given the
very crude model employed and the use of a continental species pool rather than regional pools.
Finally, many factors vary with lake size (see below)
and potentially confound the analysis: the conclusions presented here must be regarded as preliminary
until more comprehensive data become available.
Local factors
NAFF body size distributions change with lake size.
Fishes in small water bodies are small and unimodal
while the size range is greater in larger ecosystems,
with distributions tending to bimodality.
The ecosystem size hypothesis, that FCL increases
in larger ecosystems, has found support in both lentic
and lotic environments (see references in the Introduction) and in my lake data. The evidence presented
here for species stacking, while indirect (nonlinear
increases in assemblage mean, SD and mean trophic
level, declines in skewness and kurtosis), is consistent
with expectation. The Marquet et al. (2008) model
generates bimodal species distributions while Kerr &
Dickie (2001) present what is, in essence, a sizebased stacking model, where the production of a
predator mode depends on the production of its prey
and the relative sizes of predator and prey. Studies of
particular systems have shown that fish growth rates
and body size distributions depend on the availability
of different-sized prey. For example, Popova (1978)
describes a model by Menshutkin (1964) of a lake
population where perch is the only fish present.
Cyclical changes occur between uni- and bimodal age
(size) structures. These result from cannibalism by
large fish on small, the increasing numbers of large
perch eventually reducing the abundance of small
planktivorous perch, with a subsequent reduction in
the numbers of predators. Persson et al. (2003)
describe and model a similar situation, also involving
perch. Kerr (1979) noted that differences in growth
efficiencies of lake trout feeding on large (fish) and
small prey (plankton) could generate a bimodal size
distribution while Kerr & Dickie (2001) outline other
examples where species stacking is probable.
The degree of isolation and duration of the ecosystem, its short-term environmental variability and the
threats experienced (both abiotic and biotic), habitat
heterogeneity, species richness, assemblage composition and population sizes all vary with lake size
(Cohen & Johnston 1987; Wellborn et al. 1996;
Søndergaard et al. 2005). For example, larger ecosystems probably contain more habitats than small ones.
Small lakes, which are generally shallow, are likely
to be dominated by littoral habitat, but with increas-
ing lake size, profundal and pelagic habitats will also
occur and in the deepest lakes, some fish species
occupy a midwater zone. Consequently, larger ecosystems can potentially support more species (Kerr
et al. 2001; Triantis et al. 2003; Fløjgaard et al.
2011) and possibly a greater body size diversity.
There is little information on habitat-specific species
size distributions, but I can think of no obvious reason why profundal and pelagic zones in large lakes
should, on average, support larger species than littoral habitats. On the contrary, profundal habitats
usually (Hindar & Jonsson 1982; L’Abee-Lund et al.
1993), although not always (Power et al. 2009), support smaller morphotypes (of Salvelinus alpinus and
Coregonus lavaretus) than littoral habitats, i.e., habitat heterogeneity per se does not appear likely to generate the observed size trends. Small species are
probably less prone to extinction in small ecosystems
than large species, simply because they potentially
have larger population sizes (Gaston & Blackburn
2000; Rosenfield 2002).
In NAFF species, maximum and mean species
sizes increase with lake size (Fig. 3b). Predation
affects size structure in lakes (for example, Chapleau
et al. 1997). In NAFF, changes in body size moments
and trophic structure (Figs 2 and 3) occur at lake volumes of 10 3 to 10 2 km3 (area about 0.1–1 km2,
maximum depth 5–10 m, mean depths about onethird of these values): the species richness–lake area
relationship also changes slope at about this lake size
(Fig. 3a; Griffiths 1997). The smallest, species poor,
lakes are dominated by low trophic level species,
with right-skewed and unimodal size distributions.
Larger lakes support more species, including some
piscivorous ones: hence mean size, mean trophic
level and trophic level range increase with lake size
(Fig. 3). However, piscivores can exclude or reduce
the abundance of smaller, prey, species, generating
less right-skewed (or even left-skewed) and more
platykurtic distributions (Fig. 2c, d). Prey species
might persist in lakes with piscivores because of
defensive spines and/or large adult size or spatial refuges, although the latter are less likely to occur in
small lakes. In the Wisconsin assemblages studied by
Magnuson et al. (1998), only 29% (n = 31) of species were small (<1.5 log length) in lakes with pike
(Esox lucius)/largemouth bass (Micropterus salmoides) compared with 67% (n = 15) in piscivore-free
lakes (z = 2.46, P < 0.05). All trophic levels occur in
the largest lakes and, possibly as a consequence of
greater habitat heterogeneity, fish assemblages are
more symmetrical and platykurtic in size. Spencer
et al. (1999) suggested an ecosystem size threshold
above which the proportion of predatory species is
more or less constant, consistent with the data presented here.
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David Griffiths
A number of authors (Schoener 1989; Holt 1993;
Vander Zanden et al. 1999; Post et al. 2000; Takimoto et al. 2008; Doi et al. 2009) have produced evidence for the ecosystem size hypothesis, where food
chain length, and hence the importance of large predators, increases with ecosystem size. Both Vander
Zanden et al. (1999) and Post et al. (2000) demonstrated increases in FCL with lake size, although the
relationship levelled off for the two largest lakes in
the Vander Zanden et al. (1999) data, consistent with
the fish trophic level pattern in Fig. 3d: these studies
cover similar lake size ranges to that analysed here.
Thompson & Townsend (2005) and McHugh et al.
(2010) found an ecosystem size effect on food chain
length in streams, suggesting that there will also be
an effect on body size structure.
Synthesis
This article and Griffiths (2012) have found evidence
for biogeographic, evolutionary and biotic influences
on fish size distributions. The size, long-term stability, persistence and connectivity of ecosystems affect
species characteristics, particularly vagility (Griffiths
2010). Ecosystem size and persistence, which are
generally regarded as correlated (Russell-Hunter
1978; Cohen & Johnston 1987; Wellborn et al.
1996), have an important influence on size distributions by determining the range of body sizes, and
consequently of trophic interactions, found. Speciation and extinction rates also vary with ecosystem
size. Olden et al. (2007) showed that threatened
freshwater species are generally small (unlike most
taxa: Gaston & Blackburn 2000; Purvis et al. 2000)
while Griffiths (2010) concluded that small NAFF
species tend to occupy headwaters and have geographically restricted distributions, making them
potentially more vulnerable to extinction, but also,
because of reduced gene flow, to greater speciation.
Latitudinal trends in the moments of the size distributions reflect the greater postglacial recolonisation
abilities of vagile, generally large, species (Knouft
2004; Griffiths 2012). Knouft & Page (2003) and
Griffiths (2010) concluded that species diversification
was most likely to occur in small channels and, consequently, in small species. Endemics are smaller
than more widespread species (Griffiths 2012) and
their numbers decline rapidly with increasing latitude
(Griffiths 2010), and this could also contribute to latitudinal shifts in mean size.
The shape of NAFF body size distributions varies
with spatial scale, mean body size increasing, SD
decreasing and kurtosis increasing to zero (Table 2),
mainly because there are fewer small species at the
local scale. Others have produced evidence for
(Brown & Nicoletto 1991) and against (Gaston &
Blackburn 2000) this conclusion. These scale-dependent effects could be due to biotic interactions, resulting in the loss of smaller species because they are
competitively inferior, more vulnerable to predation
or have higher extinction rates, and/or to small species showing greater turnover (beta) diversity because
they are more specialised (Brown & Nicoletto 1991)
or have smaller ranges (Griffiths 2010). Although
competition in fish assemblages can affect small-scale
species distributions (Matthews 1998; Jackson et al.
2001), there have been few demonstrations of species
exclusions. However, predation can affect the size
composition of lake fish assemblages. Locally, ecosystem size affects body size distributions via physical constraints (small ecosystems favour small
species with large population sizes to reduce extinction risk) and biotic interactions (large ecosystems
harbour large, often predatory, species, which can
reduce the number of small species) while, regionally, body size distributions in glaciated areas are
determined by changes in the relative importance of
small resident versus large vagile species.
It is now recognised that many body size distributions have more than one mode. A variety of mechanisms have been proposed that could generate
multimodal distributions. As discussed above, NAFF
species size distributions are consistent with the ecosystem size/trophic structure hypothesis. A number of
major fish taxa have shown reductions in body size
as species move from large to small channels over
evolutionary time (references in Griffiths 2010), a
trend consistent with an ecosystem size effect. The
changes in body size and trophic structure with ecosystem size suggest that bimodality in lake assemblages results from species stacking, whereas
bimodality in some rivers and in habitat generalists
Table 2. Effect of sampling scale on the moments and size extremes of (log) body size distributions of lacustrine species. The continental and regional scale
values are derived only from those regions well represented (36–164 lakes) at the local scale (Hudson, Great Lakes, N. Appalachia, Gulf and Atlantic Florida).
Scale
Mean
Minimum
Maximum
SD
Skewness
Continental
Regional
Local
1.41
1.44 0.03
1.48 0.01
0.53
0.62 0.05
1.21 0.02
2.48
2.39 0.04
2.16 0.03
0.46
0.45 0.01
0.33 0.01
0.12
0.12 0.07
0.13 0.04*
*P < 0.05
264
Kurtosis
1.00
1.03 0.05*
0.05 0.09
N
1
5
393
Body size distributions in freshwater fish
(Griffiths 2012) is due to the occurrence of large,
migratory species.
Acknowledgements
My thanks to Simon Blanchet, Christine Griffiths, Bernard
Hugueny, Jason Knouft, Andrew Rypel, Kyle Young and an
anonymous reviewer for helpful comments, which greatly
improved the manuscript, and to Christine Griffiths for setting
up Hartigans dip test in R.
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Supporting Information
Additional Supporting Information may be found in
the online version of this article:
Figure S1. Hartigans’ dip statistic as a function of
sample size, generated from the strongly bimodal size
distribution of generalist North American freshwater
fish species listed by Griffiths (2012).
Figure S2. Examples of size-frequency distributions with kurtosis <-1 for fish species found in (a)
Alder lake (Rahel 1984), (b) Griffin lake (Keller &
Crisman, 1990), (c) Lake Erie (Tonn et al., 1990),
(d) Conesus lake (Bloomfield, 1978).
Figure S3. Mean moments (1 SE) of 100 samples
taken at random from the lake species pool.
Table S1. Data sources used in the analyses.
Table S2. The dip statistic as a function of kurtosis
(all values negative), species richness (N, range 15–
88 species) and lake group (Great Lakes, Finger
Lakes areas)(R2 = 0.78).
267