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Hall, R. O. J., B. J. Koch, M. C. Marshall, B. W. Taylor, and L. M. Tronstad. 2007. How
body size mediates the role of animals in nutrient cycling in aquatic ecosystems. Page
352 in A. G. Hildrew, R. Edmonds-Brown, and D. Raffaelli, editors. Body Size: The
Structure and Function of Aquatic Ecosystems. Cambridge University Press, New York.
CHAPTER FIFTEEN
How body size mediates the role
of animals in nutrient cycling
in aquatic ecosystems
ROBERT O . HALL JR .
University of Wyoming, USA
BENJAMIN J . KOCH
University of Wyoming, USA
MICHAEL C . MARSHALL
University of Wyoming, USA
BRAD W . TAYLOR
University of Wyoming, USA
LUSHA M . TRONSTAD
University of Wyoming, USA
Introduction
Aquatic ecosystems have been fertile ground for understanding the extent to
which animals can alter nutrient cycling. Although animals have been included
in ecosystem models for years (for example, Teal, 1962), it is only more recently
that investigators have looked at animals, either as individuals, single species,
or assemblages, as agents regulating nutrient cycling (Kitchell et al., 1979;
Meyer, Schultz & Helfman, 1983; Grimm, 1988; Jones & Lawton, 1995). A recent
review details how animals can affect nutrient cycling in freshwater ecosystems
(Vanni, 2002), but the next step is to understand the controls on which animals
are important regulators of nutrient dynamics in ecosystems. One controlling
factor is determined by attributes of the animals themselves, such as their
body size.
Animals can regulate nutrient cycling directly or indirectly (Kitchell et al.,
1979; Vanni, 2002). Direct regulation is the transformation and transportation
of nutrients by animal ingestion, egestion, production and excretion. For example, animal excretion can constitute the largest source of plant-available nitrogen (N) within an ecosystem (Hall, Tank & Dybdahl, 2003) and animals can move
nutrients between habitats (Meyer et al., 1983). Perhaps more common are
indirect controls, whereby animals alter nutrient cycling by changing the biomass, production or distribution of the plants or microbes that take up
nutrients. For example, predatory fish can regulate phosphorus (P) dynamics
or nitrogen retention via a trophic cascade (Elser et al., 1998; Simon et al., 2004).
Body Size and the Structure and Function of Aquatic Ecosystems, eds. Alan G. Hildrew, David G. Raffaelli and Ronni
Edmonds-Brown. Published by Cambridge University Press. # British Ecological Society 2007.
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In this paper we consider only direct effects of animals on nutrient cycling,
because predicting indirect effects in food webs contains much more uncertainty (Wootton, 1994).
A point mentioned by Vanni (2002), that we expand on here, is the role of body
size in controlling the degree to which animals contribute to ecosystem nutrient
fluxes. Body size may control animal-mediated nutrient cycling by three main
mechanisms. First, small animals have higher metabolism and, therefore, higher
mass-specific excretion rates (Wen & Peters, 1994; Brown, Allen & Gillooly, this
volume). Thus, total biomass being equal, an assemblage with small animals may
have higher animal-mediated nutrient fluxes than one with large animals.
Second, as body size increases, allometric variation in structural tissue (e.g.
P-rich bone) may alter ratios of excreted nutrients. Third, large animals have larger
home ranges and are more likely to migrate long distances, so nutrient translocation by animals may also be a function of body size.
In this chapter we first address how body size controls nutrient fluxes in the
context of the first two mechanisms described above by using published and
unpublished data to examine the relationship between nutrient excretion and
body size. We also consider the spatial and temporal translocation of nutrients
by animal movements as a function of body size. In the second part of the
chapter we apply these findings to address how ecosystem-level nutrient cycling
will change as a function of variation in animal body size. In short, we know
excretion can vary as a function of body size, but does this variation matter in
ecosystems? We explore other factors that affect animal-mediated nutrient
cycling, such as variation in the biomass of animal assemblages and their
taxonomic composition, so that we can compare their influence to the effects
of body size. Lastly, predators, especially humans, may alter the size structure of
animal assemblages, and we consider how loss of large-bodied organism may
indirectly alter nutrient cycling (see also Jennings & Reynolds, this volume).
Body size and nutrient excretion
Rates
Aquatic animals excrete N and P in mostly mineral forms which are readily
taken up by microbes. The primary form of N is ammonium, which is excreted
via the gut in insects, or diffuses across the integument and gills of other
animals. Animals primarily excrete P in the form of PO43 . Nutrient excretion
rates vary with body size. In general, excretion rates (E) scale allometrically with
body mass (M):
E ¼ aMb
(15:1)
where a and b are constants (Huxley, 1932; Peters, 1983; Wen & Peters, 1994;
Gillooly et al., 2001). For most aquatic animals, the relationship has an exponent
b < 1 indicating that excretion rates increase at a rate less than isometric with
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increasing body size (Wen & Peters, 1994). For example, individual ammonium
excretion rates for stream invertebrates, from at least 18 taxonomic orders,
scale to the 0.85 power of body mass (Fig. 15.1), implying that larger taxa excrete
at a lower rate for their size than smaller taxa. The mechanism for the less than
proportional increase in excretion rate is probably linked to metabolism, which
scales as the 3/4 power of body size (Brown et al., 2004; Brown et al., this volume).
However, for many specific groups of animals, b can be higher or lower than 3/4.
For example, b ¼ 0.67 for N and 0.54 for P in zooplankton (Wen & Peters, 1994),
whereas macroinvertebrates (Fig. 15.1) are higher.
However, body size is not the sole factor controlling variation in animal
excretion rate. It is worth considering the influence of other variables, that
may alter or interact with the effects of body size, on animal-mediated nutrient
cycling in aquatic ecosystems. For example, temperature influences metabolic
processes, such as excretion rate (Peters, 1983; Fukuhara & Yasuda, 1989;
Zhuang, 2005) Metabolic theory (Gillooly et al., 2001; Brown et al., 2004; Brown
et al., this volume) provides a mechanistic framework for incorporating the
effects of both temperature and body size on excretion rate. Fed animals have
higher excretion rates than unfed animals (Gardner & Scavia, 1981; Grimm,
Figure 15.1 Ammonium excretion rates increase less than proportionally with body size
(b < 1) for many benthic stream invertebrate taxa, indicating that larger invertebrates
excrete ammonium at a lower rate per mg of body mass than do smaller invertebrates.
The regression line (log10 [excretion rate] ¼ 1.057 þ 0.853log10 [mean individual body
mass]; n ¼ 320, r2 ¼ 0.381, 95% CI on b [0.776 0.937]) was estimated using type II, reduced
major axis linear regression (Bohonak & van der Linde, 2004). Data points were gathered
using identical methods on field-caught animals from six streams and represent total
excretion rates computed from one or more similarly-sized individuals of the same taxon
within the same incubated container (Hall et al., 2003; R. O. Hall, unpublished data; Koch,
2005; M. C. Marshall, unpublished data).
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1988), probably because of active metabolism of recently digested and assimilated N compounds. The use of fed or unfed animals may have contributed to the
variability in Fig. 15.1 and make studies where methods differ less comparable.
Taxonomic differences can also explain some of the variation in invertebrate
nutrient excretion rates (Wen & Peters, 1994). For example, Conroy et al. (2005)
found taxonomic differences in excretion rates of P, but not of N, between two
species of mussels in the genus Dreissena. Interestingly, in contrast to nearly all
other freshwater invertebrate taxa studied to date, N and P excretion rates for
Dreissena increase disproportionately with body size (b ¼ 1.379), such that larger
individuals excrete nutrients at a higher mass-specific rate than do smaller
individuals (Conroy et al., 2005). The mechanisms behind this relationship are
unclear, although it highlights the importance of recognizing taxonomy in
studies of animal-mediated nutrient cycling.
To examine taxonomic and size variation in excretion rates among fishes, we
compared published fish excretion rates of individuals (n ¼ 156 for P and 163 for
N) and species means (n ¼ 30 species for P and N) among freshwater representatives of 14 families, including Anostomidae, Aspredinidae, Catostomidae,
Cetopsidae, Characidae, Characidiidae, Cichlidae, Clupeidae, Curimatidae,
Loricariidae, Parodontidae, Pimelodidae, Salmonidae and Trichomycteridae
(Schaus et al., 1997b; Gido, 2002; Vanni et al., 2002; Andre, Hecky & Duthie,
2003; B. J. Koch, unpublished data). Individual rates are the excretion of a single
fish (many individuals in a species were measured) and species means were
calculated by averaging the excretion and size of all the individuals in that
species. All studies measured ammonium, but Schaus et al. (1997a) and Andre
et al. (2003) measured soluble reactive P, Vanni et al. (2002) estimated total
dissolved P, while Gido (2002) measured total reactive P. We converted wet
mass to dry mass by assuming dry mass was 25% of wet mass (Schaus et al.,
1997a; Gido, 2002; Andre et al., 2003), or used measured values directly (Vanni
et al., 2002; B. J. Koch, unpublished data).
Excretion of individuals within a species scaled with body size similarly, and
were higher or lower than the species means (Table 15.1). The P excretion of
three species scaled less than 1 (Table 15.1; Fig. 15.2a), meaning that the massspecific excretion rates declined with increasing size. However, N excretion of
species showed greater variability (b < 1, b ¼ 1, b > 1), indicating that both size
and taxonomy influence rates (Table 15.1; Fig. 15.2b). When fish species means
were considered, excretion scaled proportionally with dry mass (that is b 1;
Table 15.1, Figs. 15.2c,d). These data cannot disentangle the relative contribution of phylogeny vs. size because they are not independent. However, comparing species means to individual species, we can conclude that fish scale similarly
to each other. Additionally, measurements were collected by different researchers under different conditions, which may cause high variation in excretion
rates among all fishes.
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Table 15.1 Reduced major axis regression estimates for nitrogen and phosphorus excretion
(log10 g N or P fish1 h1) and size (log10 dry mass, g) in five groups of fish (see Fig. 15.2).
Data for Mbuna Cichlidae, Carpiodes carpio, Ictiobus bubalus and Dorosoma cepedianum
estimates are excretion rates from individual fish within a taxon. We also calculated the
mean excretion rate and mean size of 30 fish species taken from Gido (2002); Vanni et al.
(2002); Andre et al. (2003); Schaus et al. (1997b); and Koch (unpublished data) and
regressed mean excretion rate on mean body size. The bootstrapped 95% confidence
intervals of the exponents are in parentheses.
Taxa
Nitrogen
n
Mbuna*
Cichlidae
Carpiodesx
carpio
Ictiobusy
bubalus
Dorosomayx
cepedianum
Species
means
Intercept Exponent
Phosphorus
r2
n
Intercept Exponent
r2
40 2.04
0.759 (0.664–0.886) 0.769 37
0.975
0.886 (0.567–1.24)
10 2.96
0.789 (0.525–1.06)
0.770 10
1.39
0.733 (0.543–0.848) 0.875
16 2.27
0.983 (0.764–1.43)
0.633 16
0.803
0.568 (0.347–0.906) 0.301
93 2.13
1.14 (1.04–1.24)
0.883 93
1.40
0.921 (0.844–0.997) 0.781
30 2.41
0.953 (0.851–1.05)
0.930 30 0.916
1.07 (0.903–1.32)
x
Gido (2002)
Vanni et al. (2002)
*
Andre et al. (2003)
y
Schaus et al. (1997b)
y
The relative importance of taxonomy, body size and temperature in controlling nutrient excretion rates is only just beginning to be explored, and
adequately testing the interactions among these factors will require richer
datasets and resolved molecular phylogenies. In addition, determining the
basis of taxonomic variation in excretion rates remains a challenge. Body
nutrient composition and diet may both play roles. Given that ammonium
excretion rates for stream invertebrates are higher for fed than unfed animals
(Grimm, 1988), predators, which feed sporadically, may have more variable
excretion rates over time than continuously feeding grazers and detritivores.
Stoichiometric differences in animal nutrient use might also drive taxonomic
variation (Elser & Urabe, 1999). Predators, with relatively N-rich diets, may have
higher N excretion rates than other feeding groups. Understanding when to
account for taxonomic variation and when body size alone is sufficient for
studies of animal-mediated nutrient cycling is central to predict successfully
the role of animals in the nutrient dynamics of aquatic ecosystems.
0.176
0.831
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Figure 15.2 Phosphorus
(a, c) and nitrogen (b, d)
excretion rates (mg P or
N fish1 h1) versus dry
mass (g) for individual
fish of several taxa (a, b)
and means of 30 fish
species (c, d) from the
literature (Schaus et al.,
1997b; Gido, 2002;
Vanni et al., 2002; Andre
et al., 2003; B. J. Koch,
unpublished data). See
Table 15.1 for
regression coefficients.
Ratios of N and P
Not only will the amount of N and P excreted by animals be important in
ecosystem nutrient cycling, but the ratio of these nutrients may also drive
microbial assemblage structure and productivity (Elser et al., 1988). Nutrient
ratios in food sources, animal composition and excretion (that is, ecological
stoichiometry) have received much attention in aquatic ecology (Sterner &
Elser, 2002). Stoichiometric theory predicts that the N:P in excretion is a positive
function of the N:P of ingested food, and a negative function of the N:P requirement of the consumer (Sterner, 1990). Data show that the link between N:P in
the zooplankton body and excreted N:P is not nearly as strong as the link with
the N:P of their food (Elser & Urabe, 1999); that is, most of the variance in
excreted N:P is accounted for by variation in the food. Few analyses show how
body size drives the N:P in excretion in animals; indeed, there is little information on animal C:N:P content solely as a function of body size (Sterner & Elser,
2002). One hypothesis might be that aquatic animals should increase their N:P
content as size increases, because increased size should lead to decreased
demand for P as growth rate declines (Elser et al., 1996). Given higher body
N:P, big animals should have lower excreted N:P than small ones. However,
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this effect may be hidden by phylogeny and allometric constraints, as taxonomy
correlates with body size because large animals are often vertebrates that have
high P storage in bone apatite, and presumably a high N:P in excreta.
Data on aquatic animals suggest that excreted N:P increases with body size.
Wen and Peters (1994), showed that log N excretion rate (mg N/d) increased more
steeply with body mass than did excreted P for zooplankton. The difference in
the exponents is 0.13, which corresponds to the exponent for N:P of excretion
vs. body mass. Thus the N:P of excretion increases with body mass, suggesting
that mechanisms other than growth rate control the relationship of excreted
N:P with body size.
Data from some vertebrates also suggest increases in the N:P excreted with
body size. Excretion N:P in fishes and amphibians from a Piedmont stream in
Venezuela was positively related to body size, which agrees with qualitative
predictions based on a decreasing body N:P with increasing body mass in
vertebrates (Vanni et al., 2002b). For example, bony-scaled armoured catfishes
(Loricariidae) had particularly low body N:P and therefore high N:P in excretion
(Vanni et al., 2002). Tadpoles (families Bufonidae and Ranidae) had low excreted
N:P; because they do not have ossified bones (low skeletal demand for P). These
studies, although few, suggest that not only will body size determine the rates of
nutrient regeneration, but it will also determine the ratio of these nutrients,
with the data so far suggesting mostly increasing N:P with body size.
Mechanisms for this increase are unclear, and certainly vary across taxa. For
example, vertebrates will have proportionally more bone as their size increases
(Sterner & Elser, 2002), which will increase P demand (lowering P excretion)
with body size.
Body size and nutrient translocation
Aquatic animals can alter nutrient cycling by moving nutrients from one location to another, thus subsidizing the receiving habitat (Kitchell et al., 1979;
Vanni, 2002). In some instances this nutrient movement is between habitats
within an ecosystem such as, for example, benthic feeding fish that excrete
nutrients in the pelagic zone (Vadeboncoeur, Vander Zanden & Lodge, 2002) or
haemulid grunts that feed in seagrass beds at night and rest above coral heads
during the day, where they release nutrients that stimulate coral growth (Meyer
et al., 1983). In other cases, animals move nutrients between ecosystems on a
daily basis; e.g. ocean-foraging river otters (Lontra canadensis) excrete nutrients in
discrete locations in terrestrial habitat (Ben-David et al., 2005). Less mobile or
small-sized animals may actually concentrate nutrients at high levels in localized areas (Reinertsen et al., 1986). In contrast, Pacific salmon (Onchorhynchus
spp.) transport nutrients from the ocean to rivers via an annual long-distance
spawning migration (Gende et al., 2002). The degree of movement will be
determined in part by the speed at which animals move and the behavioural
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constraints on their home range. Both of these controls on movements should
scale with body size.
The distance moved by aquatic animals will depend on their body size because
swimming speed scales with animal body size (Peters, 1983). For a given time
travelled, a big animal can migrate further than a small one. Over large size
ranges, an animal’s Reynolds number constrains movement (e.g. zooplankter
versus a salmon). Small animals (e.g. rotifers) move very slowly because their
short length confers a low Reynolds number, and therefore viscous forces
are much higher than inertial forces. Within fishes that have high Reynolds
numbers, swimming speed scales at about M0.14 (Weihs, 1977) assuming
M / length2.6 (Peters, 1983). These modelled swimming speeds include both
Reynolds number effects plus allometric scaling of swimming force and metabolic costs. Animals with lower Reynolds numbers have a steeper positive
relationship between body mass and swimming speed, probably because of
the more pronounced effects of viscous forces at small sizes. Swimming speed
in diving beetles (Dytiscidae), increases as M0.36 (Nachtigall, 1977) assuming
M / L2.5 (Benke et al., 1999). Thus, the decline in swimming speed for small
animals probably decreases more quickly with body size than it does for fish.
Behavioural constraints on home-range size and migration will also control
nutrient movement by animals. Home range scales with body size in mammals
at roughly M1 (Jetz et al., 2004). Home-range sizes of fishes are similar to
mammals, scaling as M1.1, while insects and crustaceans are at M0.7 and molluscs at M0.55 (Alimov, 2003). Given that distance moved will scale as the squareroot of area, distance moved for fishes should then scale as approximately M0.5.
This rate of increase with body size in the actual distance moved by animals is
higher than that for speed alone, because home range is determined by many
more attributes than is speed. These include, for example, resource requirements and interactions with conspecifics (Jetz et al., 2004). Animals that transport substantial nutrients among habitats are likely to be large, as in Pacific
salmon (Gende et al., 2002), river otters, (Ben-David et al., 2005), and the longdistance migratory fish, sapuara (Semaprochilodus kneri) (Winemiller & Jepsen,
2004). It is important to consider the strong effect of behaviour; the much
smaller sapuara migrates long distances along rivers, and therefore transfers
nutrients much further than does the coastal river otter. Coral reef fishes are
large enough to travel long distances, but many stay in one spot on the reef all
their lives. Thus, while large animals are more likely to move nutrients, behavioural characteristics also control this distance.
Consequences of size-varying nutrient cycling
Variation in body-size distributions
Because excretion rates typically increase less than proportionally with animal
body size, variation in size distributions can partially control animal-driven
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nutrient mineralization and storage in ecosystems. Here we ask to what degree
does variation in animal size distribution regulate nutrient mineralization?
Researchers have described a wide variety of biomass-size distributions (also
called size spectra) for aquatic animal assemblages, including flat or smooth,
uni-, bi- and poly-modal, and step or asymptotic functions. Size distributions
can vary considerably in space and time within and among aquatic habitats
(Hanson, Prepas & Mackay, 1989; Stead et al., 2005), complicating generalizations
(see Warwick, this volume). The diversity of methods in body-size estimations (for
example, Morin & Nadon, 1991; Ramsay et al., 1997; Baca & Threlkeld, 2000) and
analytical techniques, such as different sieve or size classes, further complicate
size-spectra summaries (Cyr & Pace, 1993; Robson, Barmuta & Fairweather, 2005).
However, when only the invertebrate portions of published aquatic assemblage
spectra are included (that is, smaller and larger portions excluded), clearer patterns of shape categories emerge. Most size spectra have biomass peaks that are
skewed left, meaning larger animals generally account for most of the total
biomass, even though they may be outnumbered by smaller ones.
Size distributions in lakes vary as a function of habitat. Studies that include
multiple habitat types within the same lake suggest that pelagic and littoral
assemblages tend to have bimodal distributions of invertebrates (Hanson et al.,
1989; Cyr & Pace, 1993; Rasmussen, 1993) and polymodal distributions when
fishes are included (Gaedke, 1992), whereas profundal (and sublittoral) distributions tend to be unimodal (Hanson et al., 1989). The magnitude and locations
of biomass peaks and troughs also vary among habitats within lakes; littoral
habitats have peaks at larger body sizes. For example, the two biomass maxima
for littoral habitats tended to occur between 1–4 mg and 64–256 mg wet mass
(Rasmussen, 1993), whereas the two peak densities of pelagic zooplankton
occurred between 0.044–0.125 mg and 2.0–11.3 mg dry mass for small and large
animals, respectively (Cyr & Pace, 1993).
Streams generally have unimodal biomass size distributions (Cattaneo, 1993;
Bourassa & Morin, 1995; Mercier et al., 1999; Schmid, Tokeshi & Schmid-Araya,
2002). Body-size maxima, as equivalent to a spherical diameter, were between
2–4 mm in streams (Cattaneo, 1993), and the average individual biomass
increased slightly with increasing trophic status from 24–40 mg dry mass in
oligotrophic to urban eutrophic streams, respectively (Bourassa & Morin,
1995). Overall, although unimodality is robust across many streams, total biomass can vary by an order of magnitude (for example, Bourassa & Morin, 1995)
suggesting possible dramatic differences in animal driven nutrient fluxes
within a stream system.
Estimating nutrient flux from biomass size distributions
Animal assemblages with different size distributions should have different
nutrient supply rates to ecosystems, all else being equal. To illustrate this
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Figure 15.3 (a–c) Representative
animal size spectra from three
littoral ecosystems: (a) Lake
Brome, (b) Lake Waterloo, (c) Lake
Bromont (Rasmussen, 1993).
Total biomass (mg dry mass m2)
has been normalized to 1000 mg
dry mass m2 for the three
communities. Size classes are
Log2 (mg dry mass). (d–f) Modelled
P fluxes (mg P m2 h1) supplied
by excretion for the three
assemblages, assuming a
negative relationship between
mass-specific excretion rate and
body size. Total nutrient flux
varies nearly two-fold for the
three communities (60, 115 and
104 mgP m2 h1 for panels d, e
and f, respectively) and the
shapes of nutrient flux
distributions changed relative to
size spectra.
point we used data-capturing software to extract published size spectra from
plots. We gathered three representative aquatic animal size spectra: a bimodal
distribution with proportionally more large individuals (Fig. 15.3a), a strongly
peaked bimodal distribution (Fig. 15.3b) and a unimodal distribution (Fig. 15.3c,
Rasmussen, 1993). We assumed dry mass was 25% of wet mass (Feller &
Warwick, 1988) and normalized the literature spectra data to have equivalent
total biomasses (1000 mg dry mass m2) while preserving the same distribution
shape in the original data sets. For each of these three animal assemblages, we
then calculated the P flux supplied by excretion for each size class (Figs. 15.3d–f ),
using a negative relationship between mass-specific excretion rate and body size
(mg P mg dry mass1 h1 ¼ 0.0954[dry mass](0.541); Wen & Peters, 1994). While
this analysis accounts for variation in animal excretion rate due to body size, it
does not incorporate the effects of potentially different temperatures or taxonomic composition among animal assemblages. Nevertheless, despite total
biomass being the same for the three communities, total nutrient flux (cumulative area of rectangles) from each of the three animal communities is not
equivalent, varying by almost a factor of two in this example (60, 115 and 104 mg
P m2 h1 for Figs. 15.3d,e & f, respectively). Furthermore, the shapes of the
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nutrient flux distributions differ from their respective biomass size spectra. For
example, although larger animals comprise most of the total biomass in
Fig. 15.3a, small- and medium-sized animals supply the bulk of the nutrient
flux from this assemblage (Fig. 15.3d). Thus the size spectra of animal communities have important consequences on the supply and cycling of nutrients, and
those size classes that contribute most to total assemblage nutrient flux are not
necessarily the most biomass-rich size classes in the assemblage.
Predator control of prey body size and nutrient cycling
The well-known impact of predators on prey size structure may alter nutrient
cycling in aquatic ecosystems. Fish predators can decrease average size of prey
by eating large zooplankton (for example, Brooks & Dodson, 1965; Li, Wetterer &
Hairston, 1985) and large benthic invertebrates in lakes (Blumenshine, Lodge &
Hodgson, 2000). Alternatively, planktonic invertebrate predators, such as
Chaoborus, select small zooplankton (for example, Dodson, 1974), increasing
average prey body size. In streams, predatory invertebrates, fish and mammals
tend to consume the largest individuals of their prey (Quinn & Kinnison, 1999;
Allan, 2001; Woodward & Warren, this volume).
In addition to changes in size structure via consumptive effects, the presence
of predators can alter prey-size distribution simply through non-consumptive
effects, such as chemical cues (for example, Tollrian, 1995; Peckarsky et al.,
2002) and excretion (Ramcharan, France & McQueen, 1996). Simultaneous to
their effects on body size, predators can also affect prey physiology by increasing the allocation of nutrients to structural cells, (for example, Lively, 1986;
Vanni, 1987; Crowl & Covich, 1990; Stibor, 1992; Barry, 1994; Arendt & Wilson,
2000; Dahl & Peckarsky, 2002), which may change the composition of consumer-mineralized nutrients.
Altered size structure of the prey assemblage may change nutrient cycling,
because mass-specific excretion rate decreases with increasing animal size.
Additionally, body size affects the nutrient ratios at which animals excrete.
Changes in excretion N:P can alter the supply of the nutrient that limits primary
producers. Elser et al. (1988) suggest that phytoplankton communities are more
likely P-limited when the zooplankton assemblage includes large-bodied individuals and N-limited when the zooplankton assemblage is mainly small-bodied
individuals.
Understanding how changes in the size structure of prey can affect nutrient
cycling is not straightforward, because predators can simultaneously alter prey
abundance and biomass, and regenerate nutrients by consuming prey. Bartell
(1981) modelled P cycling under differing levels of predation using previously
published data on zooplankton size and biomass in lakes, and a mass-specific
excretion model for zooplankton. Nutrient fluxes from zooplankton did
not always increase when the assemblage switched from large-bodied to the
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small-bodied individuals that have greater mass-specific excretion rates. In fact,
P fluxes either remained similar, increased or decreased when lakes were
altered from low to high planktivore abundance, depending on changes in
total zooplankton biomass. However, nutrients may be more available in lakes
with abundant zooplanktivorous fish, because smaller zooplankton turn P over
faster than larger-bodied zooplankton (Henry, 1985). In addition to zooplankton, fish can also be an important source of nutrients to primary producers.
Some studies have reported that the nutrient flux from zooplankton is much
larger than fluxes from fish (Ramcharan et al., 1996), while others found the
reverse (Vanni & Findlay, 1990; Carpenter et al., 1992). Boers, Vanballegooijen &
Uunk, (1991) showed that the main P source switched from zooplankton to fish
as planktivore biomass increased.
Regardless of which animal supplies more nutrients, their body size can affect
nutrient cycling. To illustrate how size structure can change nutrient supply and
demand we use lakes with low and high planktivorous fish abundance. In lakes
with low planktivore abundance, both large and small zooplankton may be
present (Fig. 15.4a), but the assemblage is mainly composed of small zooplankton when planktivores are abundant (solid line, Fig. 15.4c). Compensatory
increases in the number of small zooplankton may result when fish are present
(dashed line, Fig. 15.4c); however, most studies show an overall decrease in total
zooplankton biomass (for example, Vanni & Findlay, 1990). When the density of
planktivorous fish is low (that is, both large and small zooplankton are present),
zooplankton excrete at a range of N:P ratios (grey line is N; black line is P;
Figure 15.4b); however, zooplankton excrete at a lower N:P ratio when planktivorous fish are abundant (causing N to be potentially limiting). Based on
modelling by Bartell (1981), changes in zooplankton size structure may either
increase, decrease or not change lake nutrient fluxes (Fig. 15.4d), depending on
compensatory changes in assemblage biomass. In contrast to planktivorous
fish, planktonic-invertebrate predators selectively consume small zooplankton,
resulting in a large-bodied prey assemblage excreting at a high N:P ratio.
Depending on biomass, prey nutrient fluxes could change in either direction
but may cause P to be limiting.
The effect of predators on zooplankton body size in temperate lakes is well
known; however, to our knowledge no studies have investigated how shifts in
body size of stream invertebrates could alter nutrient cycling. Because stream
predators selectively consume large-bodied prey, similar to planktivores feeding
on zooplankton, we suggest that a decline in N:P mineralization and an increase
in mineralization rates may hold for streams. However, even with the advances
in methods to estimate pools and fluxes of nutrients in streams, the effects of
predators on prey body size and nutrient cycling has not been investigated, even
though in certain cases stream invertebrates can be an important source of
ammonium (Grimm, 1988; Hall et al., 2003; Koch, 2005).
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Figure 15.4 Harvesting and predators can alter the size structure of their prey, which can
change nutrient cycling. (a) In an assemblage with low harvesting or planktivore density
(plankton-eating fish), large animals persist but the small animals are most abundant.
(b) Nitrogen (grey line) and phosphorus (black line) mass-specific excretion rates are
inversely related to body size, thus smaller animals excrete at a lower N:P than larger
animals. (c) When harvesting or planktivore density is high, only small animals will be
abundant, which may cause compensatory increases in density or biomass (dashed line).
(d) Nutrient cycling by the small-bodied assemblage may result in compensatory
increases, decreases or no change in nitrogen and phosphorus supply by animals, but
nutrient ratios will probably be altered.
The effect of harvesting-induced changes in animal size
structure on nutrient cycling
Harvesting by humans affects the size structure of aquatic animal assemblages,
and these altered size distributions may affect the rates and types of nutrients
mineralized by animals (Jennings & Reynolds, this volume; Persson & De Roos,
this volume). Similar to many other animals, humans selectively harvest large
individuals and species (Pauly et al., 1998; Jackson et al., 2001; Roy et al., 2003;
Allan et al., 2005). Size-selective harvesting can substantially change species
composition and food-web structure (for example, removal of predators), leading to fishing down the food web – a process by which larger species, often
predators, with slower growth rates are successively removed from the assemblage, leaving smaller species with faster growth rates (and thus higher massspecific nutrient excretion) that occupy lower trophic levels (Pauly et al., 1998;
Welcomme, 1999). In addition, size-selective harvesting can decrease body size
indirectly, by causing earlier maturation at smaller sizes via rapid evolutionary
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change or increased resource availability that accelerates growth and decreases
time to maturity of the remaining individuals (Trippel, 1995). Taken together,
human harvesting generally decreases or eliminates the biomass of large animals from an ecosystem (Myers & Worm, 2003; Allan et al., 2005; Ward & Myers,
2005).
There are several mechanisms by which harvest-induced changes in animal
body size may alter the role of aquatic animals in mineralizing nutrients.
Foremost, size-selective harvesting results in the loss of large-bodied individuals
and species with high excretion rates per individual, but low mass-specific
excretion. There are also important differences in the ratios at which limiting
nutrients, such as N and P, are released by animals of different size (Wen &
Peters, 1994; Schindler & Eby, 1997; Sterner & Elser, 2002; Vanni et al., 2002). As a
result, the removal of large individuals may disproportionately reduce the
amount of N relative to P supplied by animal assemblages (Fig. 15.4a,b), assuming there is no compensatory increase in abundances of smaller individuals or
species (solid line; Fig. 15.4c). If there are compensatory increases in abundance
of smaller individuals or species (dashed line; Fig. 15.4c) with higher massspecific mineralization rates, then the total supply of nutrients by the assemblage experiencing harvesting may equal or surpass the amount supplied by the
assemblage before harvesting (Fig. 15.4d). In addition, because home-range size
and migration distance increases with body size (Brown, 1995; Alimov, 2003;
Jetz et al., 2004), reduced body size due to harvesting could also decrease the
spatial scale over which nutrients are distributed by animals. This impact has
been realized; harvesting of large, migratory salmon may have decreased
marine nutrient loads to inland rivers, potentially lowering their productivity
(Thomas et al., 2003). Moreover, the larger animals, which are often the first and
most intensely harvested, generally have longer lifespans and more stable
population cycles than the smaller, short-lived species that are less frequently
harvested. Therefore, the removal of large, long-lived animals could increase the
fluctuations of nutrients mineralized by animal populations.
Overharvesting of large animals is a hallmark of all aquatic environments
(Myers & Worm, 2003; Allan et al., 2005). However, surprisingly little is known
about how the removal of larger animals alters the type or supply rate of
nutrients mineralized by animal assemblages and, more importantly, whether
such changes in nutrients are large enough to alter ecosystem-level processes. In
the Baltic sea, Hjerne and Hansson (2002) estimated that the removal of N and P
in fish biomass by harvesting to be 1.4–7% of the total nutrient load, although
the nutrient loss due to decreased mineralization by fish was not quantified.
Although information is available on how predators can mediate nutrient
mineralization rates by altering the size-structure of their prey, the process
and long-term effects of harvesting by humans are likely to be very different.
Humans typically remove the biomass of the largest animals, rarely switch
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prey until populations are severely reduced or regulatory restrictions are
imposed, and harvest at maximal rates, which are often supported by external
factors such as economic subsidies. In freshwater, species removals for biomanipulation (Horppila, 1998; Tarvainen, Sarvala & Helminen, 2002), and declines
in introduced species, affect nutrient fluxes (Kraft, 1993); however, few studies
have documented the direct effects of size-selective harvesting on nutrient
fluxes. One reason is the mismatch in the data that are available on nutrient
mineralization rates and harvesting rates of aquatic animals between marine
and freshwater ecosystems. There are comparatively better data on catch size
and body size of marine animals (Pauly et al., 1998; Myers & Worm, 2003; Ward &
Myers, 2005) than freshwater animals (Allan et al., 2005), whereas there are more
empirical data on nutrient regeneration rates for freshwater animals (Sterner &
Elser, 2002). In marine systems, it may be useful to apply bioenergetic models to
estimate the amount and type of nutrients lost from these systems as a result of
having removed 80% of the large predatory fish biomass (Myers & Worm, 2003).
Predicting the effects of harvesting-induced changes in body size on nutrient
cycling is a new challenge that could improve our understanding of the role of
animals in ecosystem functioning, and provide urgently needed guidance for
managing and restoring these systems.
The next steps?
Given that animals can often be important regenerators, storers and transporters of nutrients in ecosystems (Kitchell et al., 1979; Gende et al., 2002; Vanni,
2002; Koch, 2005), body size may be the single most important trait of the
animals themselves in controlling these processes. There are plenty of avenues
in which to further explore the role of body size in conjunction with other
animal attributes (for example, phylogeny), and ecosystem processes. Below we
give some of these examples.
1.
2.
3.
Taxonomic identity probably determines a large fraction of variation in
excretion rates, and taxonomy covaries with body size. To what degree
does size alone determine nutrient excretion rates? Can we integrate size
and phylogeny to improve predictions of nutrient excretion rate?
Body size allows us to examine how traits of animals impact ecosystem
processes, but we cannot forget that the attributes of the ecosystems themselves will, in part, determine the impact. For example, plant nutrient
demand, disturbance and hydrologic flushing rates are certainly important.
How important is animal assemblage structure relative to physical controls
and plant/microbial demand for nutrients?
We can only speculate as to the potential role of many fisheries on changes
to nutrient cycling. Some are well known, (for example, salmon), but most
are unknown (for example, groundfish stocks). These human-induced
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changes present an opportunity to examine how changes in aquatic animal
assemblages affect ecosystem processes and may provide the means to
compare the relative importance of direct versus indirect effects of assemblage and size structure on nutrient cycling.
Acknowledgements
Mike Vanni, Emidio Andre, Keith Gido and Maynard Schaus kindly provided
tables of their published data for analysis. Two anonymous reviewers provided
useful comments on an earlier draft of this manuscript. Financial support was
provided by National Science Foundation; Environmental Protection Agency;
and the Juneau Pacific Northwest Research Station, USDA Forest Service.
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