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C H A P T E R F I F T E E N

How body size mediates the roleof animals in nutrient cyclingin aquatic ecosystems

ROBERT O. HALL JR.University of Wyoming, USA

BENJAMIN J. KOCHUniversity of Wyoming, USA

MICHAEL C. MARSHALLUniversity of Wyoming, USA

BRAD W. TAYLORUniversity of Wyoming, USA

LUSHA M. TRONSTADUniversity of Wyoming, USA

IntroductionAquatic 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 exam-

ple, animal excretion can constitute the largest source of plant-available nitro-

gen (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 bio-

mass, 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 RonniEdmonds-Brown. Published by Cambridge University Press. # British Ecological Society 2007.

Brad Taylor

Text Box

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.


In this paper we consider only direct effects of animals on nutrient cycling,

because predicting indirect effects in food webs contains much more uncer-

tainty (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 trans-

location 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 excretionRates

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

B O D Y S I Z E A N D N U T R I E N T C Y C L I N G 287


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, b¼ 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�1.057þ 0.853log10 [mean individual body

mass]; n¼ 320, r2¼ 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).

R . O . H A L L E T A L .288


1988), probably because of active metabolism of recently digested and assimi-

lated 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 (b¼1.379), 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 (n¼ 156 for P and 163 for

N) and species means (n¼30 species for P and N) among freshwater representa-

tives 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 mass-

specific excretion rates declined with increasing size. However, N excretion of

species showed greater variability (b<1, b¼ 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 contribu-

tion of phylogeny vs. size because they are not independent. However, compar-

ing species means to individual species, we can conclude that fish scale similarly

to each other. Additionally, measurements were collected by different research-

ers under different conditions, which may cause high variation in excretion

rates among all fishes.



The relative importance of taxonomy, body size and temperature in control-

ling 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.

Table 15.1 Reduced major axis regression estimates for nitrogen and phosphorus excretion

(log10 �g N or P fish�1 h�1) 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 Phosphorus

n Intercept Exponent r2 n Intercept Exponent r2

Mbuna*

Cichlidae

40 2.04 0.759 (0.664–0.886) 0.769 37 0.975 0.886 (0.567–1.24) 0.176

Carpiodesx

carpio

10 2.96 0.789 (0.525–1.06) 0.770 10 1.39 0.733 (0.543–0.848) 0.875

Ictiobusy

bubalus

16 2.27 0.983 (0.764–1.43) 0.633 16 0.803 0.568 (0.347–0.906) 0.301

Dorosomayx

cepedianum

93 2.13 1.14 (1.04–1.24) 0.883 93 1.40 0.921 (0.844–0.997) 0.781

Species

means

30 2.41 0.953 (0.851–1.05) 0.930 30 �0.916 1.07 (0.903–1.32) 0.831

xGido (2002)yVanni et al. (2002)* Andre et al. (2003)ySchaus et al. (1997b)

R . O . H A L L E T A L .290


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 require-

ment 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 informa-

tion 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,

Figure 15.2 Phosphorus

(a, c) and nitrogen (b, d)

excretion rates (mg P or

N fish�1 h�1) 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.



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 translocationAquatic animals can alter nutrient cycling by moving nutrients from one loca-

tion 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 local-

ized 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

R . O . H A L L E T A L .292


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 meta-

bolic 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 mol-

luscs at M0.55 (Alimov, 2003). Given that distance moved will scale as the square-

root 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 require-

ments and interactions with conspecifics (Jetz et al., 2004). Animals that trans-

port 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 long-

distance 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, behav-

ioural characteristics also control this distance.

Consequences of size-varying nutrient cyclingVariation 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



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 pat-

terns 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) distri-

butions 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 2.0–11.3mg 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 bio-

mass 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

R . O . H A L L E T A L .294


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 m�2) 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 mass�1 h�1¼ 0.0954[dry mass](0.54�1); 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 taxo-

nomic composition among animal assemblages. Nevertheless, despite total

biomass being the same for the three communities, total nutrient flux (cumu-

lative 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 m�2 h�1 for Figs. 15.3d,e & f, respectively). Furthermore, the shapes of the

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 m�2)

has been normalized to 1000 mg

dry mass m�2 for the three

communities. Size classes are

Log2 (mg dry mass). (d–f) Modelled

P fluxes (mg P m�2 h�1) 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 m�2 h�1 for panels d, e

and f, respectively) and the

shapes of nutrient flux

distributions changed relative to

size spectra.



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 commun-

ities 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 increas-

ing 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 con-

sumer-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 indi-

viduals 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

R . O . H A L L E T A L .296


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 zooplank-

ton, 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 zooplank-

ton 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 plank-

tivorous 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).



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), lead-

ing to fishing down the food web – a process by which larger species, often

predators, with slower growth rates are successively removed from the assem-

blage, leaving smaller species with faster growth rates (and thus higher mass-

specific 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

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.

R . O . H A L L E T A L .298


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 ani-

mals 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), assum-

ing 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 mass-

specific mineralization rates, then the total supply of nutrients by the assem-

blage 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



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 biomani-

pulation (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 transport-

ers 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. 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?

2. Body size allows us to examine how traits of animals impact ecosystem

processes, but we cannot forget that the attributes of the ecosystems them-

selves 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?

3. 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

R . O . H A L L E T A L .300


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 assem-

blage and size structure on nutrient cycling.

AcknowledgementsMike 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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