Predation, competition, and nutrient recycling: a stoichiometric approach with multiple nutrients

A model for two competing prey species and one predator is formulated in which three essential nutrients can limit growth of all populations. Prey take up dissolved nutrients and predators ingest prey, assimilating a portion of ingested nutrients and recycling or respiring the balance. For all species, the nutrient contents of individuals vary and growth is coupled to increasing content of the limiting nutrient. This model was parameterized to describe a flagellate preying on two bacterial species, with carbon (C), nitrogen (N), and phosphorus (P) as nutrients. Parameters were chosen so that the two prey species would stably coexist without predators under some nutrient supply conditions. Using numerical simulations, the long-term outcomes of competition and predation were explored for a gradient of N:P supply ratios, varying C supply, and varying preference of the predator for the two prey. Coexistence and competitive exclusion both occurred under some conditions of nutrient supply and predator preference. As in simpler models of competition and predation these outcomes were largely governed by apparent competition mediated by the predator, and resource competition for nutrients whose effective supply was partly governed by nutrient recycling also mediated by the predator. For relatively small regions of parameter space, more complex outcomes with multiple attractors or three-species limit cycles occurred. The multiple constraints posed by multiple nutrients held the amplitudes of these cycles in check, limiting the influence of complex dynamics on competitive outcomes for the parameter ranges explored.     

Modeling the bacterial contribution to planktonic community respiration in the regulation of solar energy and nutrient availability

In planktonic ecosystems, algae and bacteria exhibit complex interrelationships, as algae provide an important organic matter source for microbial growth while microbial metabolism recycles limiting nutrients for algae in a loose commensalism. However, algae and bacteria can also compete for available nutrients if supplies of organic matter are sufficient to satisfy bacterial demand. We developed a stoichiometrically explicit model of bacteria–algae interactions that incorporated realistic assumptions about algal light and nutrient utilization, algal exudation of organic matter, and bacterial processing of organic matter and nutrients. The model makes specific predictions about how the relative balance of algae and bacteria should change in response to varied nutrient and light availability seen in lakes and oceans. The model successfully reproduces published empirical data and indicates that, under moderate nutrient supply, the bacterial percentage of total respiration should be maximal at intermediate light intensity.     

The impact of variable stoichiometry on predator-prey interactions: a multinutrient approach

A model for prey and predators is formulated in which three essential nutrients can limit growth of both populations. Prey take up dissolved nutrients, while predators ingest prey, assimilate a fraction of ingested nutrients that depends on their current nutrient status, and recycle the balance. Although individuals are modeled as identical within populations, amounts of nutrients within individuals vary over time in both populations, with reproductive rates increasing with these amounts. Equilibria and their stability depend on nutrient supply conditions. When nutrient supply increases, unusual results can occur, such as a decrease of prey density. This phenomenon occurs if, with increasing nutrient, predators sequester rather than recycle nutrients. Furthermore, despite use of a linear functional response for predators, high nutrient supply can destabilize equilibria. Responses to nutrient supply depend on the balance between assimilation and recycling of nutrients by predators, which differs depending on the identity of the limiting nutrient. Applied to microbial ecosystems, the model predicts that the efficiency of organic carbon mineralization is reduced when supply of mineral nutrients is low and when equilibria are unstable. The extent to which predators recycle or sequester limiting nutrients for their prey is of critical importance for the stability of predator-prey systems and their response to enrichment.     

Metabolic stoichiometry and the ecology of fear in Trinidadian guppies: consequences for life histories and stream ecosystems

Consumer-driven nutrient recycling, the release of chemicals as byproducts and excesses of consumer physiology, can alter ecosystems by changing the availability of limiting nutrients at the base of the food web. The mere presence of predators can alter consumer physiology by restricting food intake and inducing stress. Predation risk, then, can influence ecosystem function by modifying the role of prey as nutrient recyclers, yet there are few empirical tests of how predation risk alters nutrient recycling by prey. Here, we present the results of a test for the effects of predation risk on the C and N budgets of Trinidadian guppies (Poecilia reticulata). We reared female guppies for 7 weeks on diets of varying quality, and we compared control individuals to those exposed continuously to chemical cues emitted by a guppy predator, Crenicichla alta. We measured food consumption, growth rate, tissue elemental stoichiometry and N excretion by guppies on all treatments. Guppies strongly reduced food intake in the presence of predator cues; however, cue-exposed guppies assimilated nutrients more efficiently than controls. Specifically, cue-exposed guppies strongly increased N retention efficiency while only moderately increasing C efficiency. Consequently, guppies reared with predator cues excreted 39 % less N than control guppies. We suggest that reduced foraging, enhanced nutrient efficiency, and decreased N excretion are adaptive responses to the extrinsic mortality threat posed by guppy predators. The resulting substantial reduction in N excretion by guppies may influence ecosystem function in natural streams by reducing the supply of a limiting nutrient.     

Transient dynamics limit the effectiveness of keystone predation in bringing about coexistence

We analyze the transient dynamics of simple models of keystone predation, in which a predator preferentially consumes the dominant of two (or more) competing prey species. We show that coexistence is unlikely in many systems characterized both by successful invasion of either prey species into the food web that lacks it and by a stable equilibrium with high densities of all species. Invasion of the predator-resistant consumer species often causes the resident, more vulnerable prey to crash to such low densities that extinction would occur for many realistic population sizes. Subsequent transient cycles may entail very low densities of the predator or of the initially successful invader, which may also preclude coexistence of finite populations. Factors causing particularly low minimum densities during the transient cycles include biotic limiting resources for the prey, limited resource partitioning between the prey, a highly efficient predator with relatively slow dynamics, and a vulnerable prey whose population dynamics are rapid relative to the less vulnerable prey. Under these conditions, coexistence of competing prey via keystone predation often requires that the prey's competitive or antipredator characteristics fall within very narrow ranges. Similar transient crashes are likely to occur in other food webs and food web models.     

Herbivorous animals can mitigate unfavourable ratios of energy and material supplies by enhancing nutrient recycling

Recent evidence shows that high supply ratios of light and nutrients limit planktonic herbivore growth by lowering the nutritional quality of algae. Over longer time scales, however, grazers may ameliorate this effect by their impact on nutrient cycling. We examine this possibility using two species of the herbivorous zooplankter Daphnia and its algal prey under different light intensities and low phosphorus supply in laboratory microcosms. At high light, Daphnia biomass was limited for a substantial period because of low P content of algal cells. However, a gradual increase in Daphnia density eventually improved food quality through grazing and nutrient cycling and via a novel process involving positive density dependence. Competitive exclusion of one of the two Daphnia species occurred under low light but not under high light when algae were nutritionally unsuitable. Such stoichiometrically mediated interactions among herbivorous animals may represent important mechanisms that affect community structure and material flows in ecosystems.     

Your worst enemy could be your best friend: predator contributions to invasion resistance and persistence of natives

Native predators are postulated to have an important role in biotic resistance of communities to invasion and community resilience. Effects of predators can be complex, and mechanisms by which predators affect invasion success and impact are understood for only a few well-studied communities. We tested experimentally whether a native predator limits an invasive species’ success and impact on a native competitor for a community of aquatic insect larvae in water-filled containers. The native mosquito Aedes triseriatus alone had no significant effect on abundance of the invasive mosquito Aedes albopictus. The native predatory midge Corethrella appendiculata, at low or high density, significantly reduced A. albopictus abundance. This effect was not caused by trait-mediated oviposition avoidance of containers with predators, but instead was a density-mediated effect caused by predator-induced mortality. The presence of this predator significantly reduced survivorship of the native species, but high predator density also significantly increased development rate of the native species when the invader was present, consistent with predator-mediated release from interspecific competition with the invader. Thus, a native predator can indirectly benefit its native prey when a superior competitor invades. This shows the importance of native predators as a component of biodiversity for both biotic resistance to invasion and resilience of a community perturbed by successful invasion.     

High food quality of prey lowers its risk of extinction

The mineral and biochemical food quality of prey may limit predator production. This well‐studied direct bottom–up effect is especially prominent for herbivore–plant interactions. Low‐quality prey species, particularly when defended, are generally considered to be less prone to predator‐driven extinction. Undefended high‐quality prey species sustain high predator production thereby potentially increasing their own extinction risk. The food quality of primary producers is highly species‐specific. In communities of competing prey species, predators thus may supplement their diets of low‐quality prey with high‐quality prey, leading to indirect horizontal interactions between prey species of different food quality. We explore how these predator‐mediated indirect interactions affect species coexistence in a general predator–prey model that is parametrized for an experimental algae– rotifer system. To cover a broad range of three essential functional traits that shape many plant–herbivore interactions we consider differences in 1) the food quality of the prey species, 2) their competitive ability for nutrient uptake and 3) their defence against predation. As expected, low food quality of prey can, similarly to defence, provide protection against extinction by predation. Counterintuitively, our simulations demonstrate that being of high food quality also prevents extinction of that prey species and additionally promotes coexistence with a competing, low‐quality prey. The persistence of the high‐quality prey enables a high conversion efficiency and control of the low‐quality prey by the predator and allows for re‐allocation of nutrients to the high‐quality competitor. Our results show that high food quality is not necessarily detrimental for a prey species but instead can protect against extinction and promote species richness and functional biodiversity.     

Does disturbance,competition or resource limitation underlie Hieracium lepidulum invasion in New Zealand? Mechanisms of establishment and persistence,and functional differentiation among invasive and native species

The processes underlying plant invasions have been the subject of much ecological research. Understanding mechanisms of plant invasions are difficult to elucidate from observations, yet are crucial for ecological management of invasions. Hieracium lepidulum, an asteraceous invader in New Zealand, is a species for which several explanatory mechanisms can be raised. Alternative mechanisms, including competitive dominance, disturbance of resident vegetation allowing competitive release or nutrient resource limitation reducing competition with the invader are raised to explain invasion. We tested these hypotheses in two field experiments which manipulated competitive, disturbance and nutrient environments in pre‐invasion and post‐invasion vegetation. H. lepidulum and resident responses to environmental treatments were measured to allow interpretation of underlying mechanisms of establishment and persistence. We found that H. lepidulum differed in functional response profile from native species. We also found that other exotic invaders at the sites were functionally different to H. lepidulum in their responses. These data support the hypothesis that different invaders use different invasion mechanisms from one another. These data also suggest that functional differentiation between invaders and native resident vegetation may be an important contributing factor allowing invasion. H. lepidulum appeared to have little direct competitive effect on post‐invasion vegetation, suggesting that competition was not a dominant mechanism maintaining its persistence. There was weak support for disturbance allowing initial establishment of H. lepidulum in pre‐invasion vegetation, but disturbance did not lead to invader dominance. Strong support for nutrient limitation of resident species was provided by the rapid competitive responses with added nutrients despite presence of H. lepidulum. Rapid competitive suppression of H. lepidulum once nutrient limitation was alleviated suggests that nutrient limitation may be an important process allowing the invader to dominate. Possible roles of historical site degradation and/or invader‐induced soil chemical/microbial changes in nutrient availability are discussed.     

Foraging responses of predators to novel toxic prey: effects of predator learning and relative prey abundance

Learning to avoid toxic prey items may aid native predators to survive the invasion of highly toxic species, such as cane toads Bufo marinus in tropical Australia. If the predators’ initial aversion is generalized, native prey that resemble the toxic invader may receive a benefit through accidental mimicry. What ecological factors influence the acquisition of learned avoidance (and hence, the impact of invasion on both predators and native prey)? We conducted laboratory experiments to evaluate how the relative abundance of toad tadpoles compared to palatable native tadpoles (Litoria caerulea and L. rubella) affected the ability of native aquatic predators to discriminate between these two prey types. Both fish (northern trout gudgeon, Mogurnda mogurnda) and frogs (Dahl's aquatic frog, Litoria dahlii) learned to discriminate between toads and frogs within an eight‐day period. Higher abundance of toad tadpoles relative to frog tadpoles enhanced rates of predator learning, and thus reduced predation on toads and increased predation on native tadpoles. In the field, spatial and temporal variation in the relative abundance of cane toads compared to native frogs may influence the rates at which these novel toxic items are deleted from predator diets, and the duration of predator protection afforded to natives that resemble the invader.     

Invasibility of plankton food webs along a trophic state gradient

Biological invasions are becoming more common, yet the majority of introduced exotic species fail to establish viable populations in new environments. Current ecological research suggests that invasion success may be determined by properties of the native ecosystem, such as the supply rate of limiting nutrients (i.e. trophic state). We examined how trophic state influences invasion success by introducing an exotic zooplankter, Daphnia lumholtzi into native plankton communities in a series of experimental mesocosms exposed to a strong nutrient gradient. We predicted that the attributes of nutrient-enriched communities would increase the likelihood of a successful invasion attempt by D. lumholtzi . Contrary to our original predictions, we found that D. lumholtzi was often absent from mesocosms that developed under high nutrient supply rates. Instead, the presence of D. lumholtzi was associated with systems that had low nutrients, low zooplankton biomass, and high zooplankton species diversity. Using generalized estimating equations (GEE) and multivariate species data, we found that the presence–absence of D. lumholtzi could be explained by variations in zooplankton community structure, which was itself strongly influenced by nutrient supply rate. We argue that the apparent invasion success of D. lumholtzi was inhibited by the dominance of another cladoceran species, Chydorus sphaericus . These results suggest that the interaction between trophic state and species identity influenced the invasion success of introduced D. lumholtzi .     

On the influence of food quality in consumer–resource interactions

While nutrients are an important regulating factor in food webs, no theoretical studies have examined limits to consumer growth imposed by nutrient concentrations (i.e. food quality) of their prey. Empirical studies have suggested that nutrients may play a role in limiting assimilation efficiencies of herbivores. Using a simple food chain model, I find that prey nutrient concentration does directly influence the growth rate of consumers and potentially increase the stability of consumer–resource interactions. This suggests that the strength of trophic cascades and the relative importance of top–down versus bottom–up control in food webs is significantly influenced by nutrient availability in food resources of consumers. Additionally, the results imply that increases in resource input may cause a change in which resource is limiting and thereby negate any potential "paradox of enrichment".     

Differential vulnerability of prey to an invading top predator: integrating field surveys and laboratory experiments

Abstract 1. A new top predator, the dragonfly Cordulegaster boltonii, invaded Broadstone Stream (U.K.) in the mid‐1990s. This provided a rare opportunity to assess the impact of a new, large carnivore on a community that has been studied since the 1970s and has one of the most detailed food webs yet published. The vulnerability of the resident species to the invader was assessed by integrating experiments, which examined discrete stages in the predation sequence, with empirical survey data. 2. Although the new predator preyed on nearly every macro‐invertebrate in the food web, vulnerability varied considerably among prey species. Size‐related handling constraints initially set the predator's diet, resulting in strong ontogenetic shifts, with progressively larger prey being added while small prey were retained in the diet, as predators grew. Within the size range of vulnerable prey, encounter rate limited the strength of predation, with mobile, epibenthic species being most at risk. Contrary to most studies of interactions between freshwater predators (usually stoneflies) and prey (usually mayflies), the new predator did not elicit avoidance responses from its prey, probably because it combined a highly cryptic feeding posture with an extremely rapid attack response. 3. The invader exploited its prey heavily in experiments, even at prey densities orders of magnitude above ambient. In the field, electivity reflected prey availability, as determined by mobility and microhabitat use, rather than prey abundance or active predator choice. Consequently, the invader had skewed effects within the prey assemblage, with sedentary, interstitial species being far less vulnerable than more active, epibenthic species, some of which, including a previous top predator, have declined markedly since the invasion. 4. By examining the predation sequence in detail and integrating surveys with experiments, species traits and system characteristics that determine the strength of trophic interactions may be identified, and their potential importance in natural food webs assessed. In so doing, greater insight can be gained into which species (and systems) will be most vulnerable to invading or exotic predators, an imperative in both pure and applied ecology.     

Stoichiometric food quality and herbivore dynamics

Herbivores may grow with nutrient or energy limitation, depending on food abundance and the chemical composition of their food. We present a model that describes herbivore growth as a continuous function of two limiting factors. This function uses the synthesizing unit concept, has the hyperbolic Monod model as a limiting case, and has the same number of parameters as the Monod model coupled to Liebig's discontinuous minimum rule. We use the model to explore nutrient-limited herbivore growth in a closed system with algae, Daphnia and phosphorus as the limiting nutrient. Phosphorus in algae may substantially influence Daphnia growth. This influence changes over time and is most pronounced when algae and Daphnia populations fluctuate strongly. Relative to classic models that only consider food quantity as a determinant of Daphnia growth, our model shows richer dynamical behaviour. In addition to the standard positive equilibrium, which may be stable or unstable depending on nutrient availability, a new positive equilibrium may arise in our model when mortality rates are relatively high. This equilibrium is unstable and reduces the likelihood of long-term persistence of Daphnia in the system.     

Scale dependent effects of native prey diversity,prey biomass and natural disturbance on the invasion success of an exotic predator

There is growing support for the general notion that the drivers of invasion success often shift from biotic to abiotic factors with increasing spatial scale. Most of this research, however, has been conducted on a single trophic level; i.e. it has primarily looked at how the diversity of native competitors may influence invasion success. Less attention has been paid to understanding how native prey diversity may influence the invasion success of exotic predators and whether such biotic factors are scale-dependent. We used a hierarchical spatial survey of 17 stream communities to test whether native prey diversity, along with native prey biomass, algal resource abundance and annual stream discharge, influenced the abundance of an exotic crayfish predator, and whether the importance of these factors were scale-dependent. We used a hierarchical generalized linear model to evaluate the influence of these community and stream characteristics on exotic crayfish abundance at both the transect scale (1 m²) and the stream scale (400 m²). Our results indicated that at the stream scale, high stream discharge significantly limited invader abundance. However, at the smaller transect scale, native prey biomass was a significant driver of invasion success and positively correlated with invader abundance. We suggest that our results add to the emerging pattern that abiotic processes are stronger determinants of invasion success at large spatial scales, whereas biotic processes become more important with decreasing spatial scale. However, for predator invasions, prey biomass, not prey diversity may be a more important for driver of invasion success at small spatial scales.     

Consequences of symbiosis for food web dynamics

Basic Lotka-Volterra type models in which mutualism (a type of symbiosis where the two populations benefit both) is taken into account, may give unbounded solutions. We exclude such behaviour using explicit mass balances and study the consequences of symbiosis for the long-term dynamic behaviour of a three species system, two prey and one predator species in the chemostat. We compose a theoretical food web where a predator feeds on two prey species that have a symbiotic relationships. In addition to a species-specific resource, the two prey populations consume the products of the partner population as well. In turn, a common predator forages on these prey populations. The temporal change in the biomass and the nutrient densities in the reactor is described by ordinary differential equations (ODE). Since products are recycled, the dynamics of these abiotic materials must be taken into account as well, and they are described by odes in a similar way as the abiotic nutrients. We use numerical bifurcation analysis to assess the long-term dynamic behaviour for varying degrees of symbiosis. Attractors can be equilibria, limit cycles and chaotic attractors depending on the control parameters of the chemostat reactor. These control parameters that can be experimentally manipulated are the nutrient density of the inflow medium and the dilution rate. Bifurcation diagrams for the three species web with a facultative symbiotic association between the two prey populations, are similar to that of a bi-trophic food chain; nutrient enrichment leads to oscillatory behaviour. Predation combined with obligatory symbiotic prey-interactions has a stabilizing effect, that is, there is stable coexistence in a larger part of the parameter space than for a bi-trophic food chain. However, combined with a large growth rate of the predator, the food web can persist only in a relatively small region of the parameter space. Then, two zero-pair bifurcation points are the organizing centers. In each of these points, in addition to a tangent, transcritical and Hopf bifurcation a global heteroclinic bifurcation is emanating. This heteroclinic cycle connects two saddle equilibria where the predator is absent. Under parameter variation the period of the stable limit cycle goes to infinity and the cycle tends to the heteroclinic cycle. At this global bifurcation point this cycle breaks and the boundary of the basin of attraction disappears abruptly because the separatrix disappears together with the cycle. As a result, it becomes possible that a stable two-nutrient–two-prey population system becomes unstable by invasion of a predator and eventually the predator goes extinct together with the two prey populations, that is, the complete food web is destroyed. This is a form of over-exploitation by the predator population of the two symbiotic prey populations. When obligatory symbiotic prey-interactions are modelled with Liebigs minimum law, where growth is limited by the most limiting resource, more complicated types of bifurcations are found. This results from the fact that the Jacobian matrix changes discontinuously with respect to a varying parameter when another resource becomes most limiting.Revised version: 21 July 2003     

Qualitative behavior of a variable-yield simple food chain with an inhibiting nutrient

A simple food chain which consists of nutrient, prey and predator in which nutrient is growth limiting at low concentrations but growth inhibiting at high concentrations is investigated in this study. It is assumed that the nutrient concentration is separated into internal and external nutrient concentration and only the internal nutrient level is capable of catalyzing cell growth. It is shown that the dynamics of the system depend on thresholds R(0) and R(1). With inhibition, there exist initial conditions for which the predator becomes extinct but not the prey when R(0)<1. If R(0),R(1)1, the system is uniformly persistent even in the inhibited environment.     

Promotion of harmful algal blooms by zooplankton predatory activity

The relationship between algae and their zooplanktonic predators typically involves consumption of nutrients by algae, grazing of the algae by zooplankton which in turn enhances predator biomass, controls algal growth and regenerates nutrients. Eutrophication raises nutrient levels, but does not simply increase normal predator-prey activity; rather, harmful algal bloom (HAB) events develop often with serious ecological and aesthetic implications. Generally, HAB species are outwardly poor competitors for nutrients, while their development of grazing deterrents during nutrient stress ostensibly occurs too late, after the nutrients have largely been consumed already by fast-growing non-HAB species. A new mechanism is presented to explain HAB dynamics under these circumstances. Using a multi-nutrient predator-prey model, it is demonstrated that these blooms can develop through the self-propagating failure of normal predator-prey activity, resulting in the transfer of nutrients into HAB growth at the expense of competing algal species. Rate limitation of this transfer provides a continual level of nutrient stress that results in HAB species exhibiting grazing deterrents protecting them from top-down control. This process is self-stabilizing as long as nutrient demand exceeds supply, maintaining the unpalatable status of HABs; such events are most likely under eutrophic conditions with skewed nutrient ratios.     

Interpopulation variation in a fish predator drives evolutionary divergence in prey in lakes

Ecological factors are known to cause evolutionary diversification. Recent work has shown that evolution in strongly interacting predator species has reciprocal impacts on ecosystems. These divergent impacts of predators may alter the selective landscape and cause the evolution of prey. Yet, this link between intraspecific variation and evolution is unexplored. We compared the life history of a species of zooplankton (Daphnia ambigua) from lakes in New England in which the dominant planktivorous predator, the alewife (Alosa pseudoharengus), differs in feeding traits and migratory behaviour. Anadromous alewife (seasonal migrants) exhibit larger gapes, gill-raker spacing and target larger prey than landlocked alewife (year-round freshwater resident). In 'anadromous' lakes, Daphnia are abundant in the spring but extirpated by alewife predation in summer. Daphnia are rare year-round in 'landlocked' lakes. We show that Daphnia from lakes with anadromous alewife grew faster, matured earlier but at the same size and produced more offspring than Daphnia from lakes with landlocked or no alewife across multiple temperature and resource treatments. Our results are inconsistent with a response to size-selective predation but are better explained as an adaptation to colder temperatures and shorter periods of development (countergradient variation) mediated by seasonal alewife predation.     

Keystone predator effects and grazer control of planktonic primary production

If prey species exhibit trade-offs in their ability to utilize resources versus their ability to avoid predation, predators can facilitate prey turnover along gradients of productivity, shifting dominance from edible to inedible prey (the keystone predator effect). I tested this model under controlled, laboratory conditions, using a model aquatic system composed of zooplankton as the top consumer, a diverse community of algae as prey, and nutrients as basal resources. Nutrient manipulations (low and high) were crossed with presence–absence of zooplankton. Results supported theoretical predictions. Algal biomass increased in response to enrichment regardless of predator presence/absence. However, predators and nutrients had an interactive effect on algal biomass and size structure. At the low nutrient level, algal-prey were dominated by edible forms and attained similar biomass regardless of zooplankton presence/absence. At the high level of enrichment, presence of zooplankton favored higher levels of algal biomass and shifted dominance to large, inedible taxa. At the termination of the experiment, I performed a series of lab-based assays on the resultant algal community in order to quantify trade-offs among algal size classes in maximal population growth rates (as a measure of competitive ability for nutrients) and susceptibility to zooplankton grazing. Assays provided support for a size-based keystone trade-off. Small size classes of algae displayed higher maximal growth rates but were more susceptible to grazing effects. Large size classes were protected from grazing but showed low rates of population growth in response to enrichment.