Density-dependent effects of prey defences

In this study, we show that the protective advantage of a defence depends on prey density. For our investigations, we used the predator-prey model system Chaoborus-Daphnia pulex. The prey, D. pulex, forms neckteeth as an inducible defence against chaoborid predators. This morphological response effectively reduces predator attack efficiency, i.e. number of successful attacks divided by total number of attacks. We found that neckteeth-defended prey suffered a distinctly lower predation rate (prey uptake per unit time) at low prey densities. The advantage of this defence decreased with increasing prey density. We expect this pattern to be general when a defence reduces predator success rate, i.e. when a defence reduces encounter rate, probability of detection, probability of attack, or efficiency of attack. In addition, we experimentally simulated the effects of defences which increase predator digestion time by using different sizes of Daphnia with equal vulnerabilities. This type of defence had opposite density-dependent effects: here, the relative advantage of defended prey increased with prey density. We expect this pattern to be general for defences which increase predator handling time, i.e. defences which increase attacking time, eating time, or digestion time. Many defences will have effects on both predator success rate and handling time. For these defences, the predator’s functional response should be decreased over the whole range of prey densities. Received: 15 September 1999 / Accepted: 23 December 1999     

Response of predators to prey abundance: separating the effects of prey density and patch size

We tested the relative and combined effects of prey density and patch size on the functional response (number of attacks per unit time and duration of attacks) of a predatory reef fish (Cheilodactylus nigripes (Richardson)) to their invertebrate prey. Fish attacked prey at a greater rate and for longer time in large than small patches of prey, but large patches had naturally greater densities of prey. We isolated the effects of patch size and prey density by reducing the density of prey in larger patches to equal that of small patches; thereby controlling for prey density. We found that the intensity at which fish attacked prey (combination of attack rate and duration) was primarily a response to prey density rather than the size of patch they occupied. However, there was evidence that fish spent more time foraging in larger than smaller patches independent of prey density; presumably because of the greater total number of prey available. These experimental observations suggest that fish can distinguish between different notions of prey abundance in ways that enhance their rate of consumption. Although fish may feed in a density dependent manner, a critical issue is whether their rate of consumption outstrips the rate of increase in prey abundance to cause density dependent mortality of prey.     

Density-dependent effects of multiple predators sharing a common prey in an endophytic habitat

Multiple predator species feeding on a common prey can lead to higher or lower predation than would be expected by simply combining their individual effects. Such emergent multiple predator effects may be especially prevalent if predators share feeding habitat. Despite the prevalence of endophagous insects, no studies have examined how multiple predators sharing an endophytic habitat affect prey or predator reproduction. We investigated density-dependent predation of Thanasimus dubius (Coleoptera: Cleridae) and Platysoma cylindrica (Coleoptera: Histeridae) on a bark beetle prey, Ips pini (Coleoptera: Scolytidae), in a laboratory assay. I. pini utilize aggregation pheromones to group-colonize and reproduce within the stems of conifers. T. dubius and P. cylindrica exploit these aggregation pheromones to arrive simultaneously with the herbivore. Adult T. dubius prey exophytically, while P. cylindrica adults enter and prey within the bark beetle galleries. Larvae of both predators prey endophytically. We used a multiple regression analysis, which avoids confounding predator composition with density, to examine the effects of varying predator densities alone and in combination on herbivore establishment, herbivore reproduction, and predator reproduction. Predators reduced colonization success by both sexes, and decreased I. pini reproduction on a per male and per female basis. The combined effects of these predators did not enhance or reduce prey establishment or reproduction in unexpected manners, and these predators were entirely substitutable. The herbivores net replacement rate was never reduced significantly below one at prey and predator densities emulating field conditions. Similar numbers of each predator species emerged from the logs, but predator reproduction suffered from high intraspecific interference. The net replacement rate of P. cylindrica was not affected by conspecifics or T. dubius. In contrast, the net replacement rate of T. dubius decreased with the presence of conspecifics or P. cylindrica. Combinations of both predators led to an emergent effect, a slightly increased net replacement rate of T. dubius. This may have been due to predation by larval T. dubius on pupal P. cylindrica, as P. cylindrica develops more rapidly than T. dubius within this shared habitat.     

Latitudinal variation in spongivorous fishes and the effectiveness of sponge chemical defenses

It has been proposed that predation pressure declines with increasing latitude and a positive correlation exists between predation intensity and the investment into chemical defenses. However, little direct evidence supports the idea that tropical species are better defended chemically than their temperate counterparts. Temperate reefs of the South Atlantic Bight (SAB) off Georgia, USA, provide a unique opportunity to study tropical sponges in a temperate environment. We documented sponge species richness and abundance, sponge predator density, and examined the ability of eight sponge species to chemically deter predation by fishes on two reefs in the SAB. We used rarefaction analysis and ANOVA to compare our results for sponge species richness and density, respectively, with similar published studies conducted on reefs of the sub-tropical Atlantic (i.e., Florida Keys). These analyses were combined with similar statistical comparisons for spongivorous fish species richness and density. Results showed that sponge species richness was lower, but sponge density was higher, on the temperate SAB reefs than on the subtropical reefs. Both spongivorous fish diversity and density were lower on the SAB reefs. The greater abundance of sponges and lower density of predators on SAB reefs suggest a lower frequency of predation on sponges on SAB reefs. Of the eight sponge species assayed from the SAB reefs, five possessed chemical extracts that were significantly less deterrent to fish predators than their tropical/subtropical conspecifics. When the results were combined across all sponge species, the chemical deterrence of fish predators was significantly lower for extracts obtained from the temperate sponge community as compared to the tropical/subtropical assemblage. These results support the more general hypothesis that a lower density and diversity of sponge predators occurs at high as compared to low latitudes in the western Atlantic and may contribute to decreased investment in chemical defenses.     

Behavioral responses to prey density by three acarine predator species with different degrees of polyphagy

Behavioral responses by three acarine predators, Phytoseiulus persimilis, Typhlodromus occidentalis, and Amblyseius andersoni (Acari: Phytoseiidae), to different egg and webbing densities of the spider mite Tetranychus urticae (Acari: Tetranychidae) on rose leaflets were studied in the laboratory. Prey patches were delineated by T. urticae webbing and associated kairomones, which elicit turning back responses in predators near the patch edge. Only the presence of webbing affected predator behavior; increased webbing density did not increase patch time. Patch time increased with increased T. urticae egg density in the oligophagous P. persimilis, but was density independent in the polyphagous species T. occidentalis and A. andersoni. Patch time in all three species was more strongly correlated with the number of prey encounters and attacks than with the actual prey number present in the patch. Patch time was determined by (a) the turning back response near the patch edge; this response decayed through time and eventually led to the abandonment of the patch, and (b) encounters with, and attacks upon, prey eggs; these prolonged patch time by both an increment of time spent in handling or rejecting prey and an increment of time spent searching between two successive prey encounters or attacks. Although searching efficiency was independent of prey density in all three species, the predation rate by P. persimilis decreased with prey density because its searching activity (i.e. proportion of total patch time spent in searching) decreased with prey density. Predation rates by T. occidentalis and A. andersoni decreased with prey density because their searching activity and success ratio both decreased with prey density. The data were tested against models of predator foraging responses to prey density. The effects of the degree of polyphagy on predator foraging behavior were also discussed.     

Influence of prey body characteristics and performance on predator selection

At the time of settlement to the reef environment, coral reef fishes differ in a number of characteristics that may influence their survival during a predatory encounter. This study investigated the selective nature of predation by both a multi-species predator pool, and a single common predator (Pseudochromis fuscus), on the reef fish, Pomacentrus amboinensis. The study focused on the early post-settlement period of P. amboinensis, when mortality, and hence selection, is known to be highest. Correlations between nine different measures of body condition/performance were examined at the time of settlement, in order to elucidate the relationships between different traits. Single-predator (P. fuscus) choice trials were conducted in 57.4-l aquaria with respect to three different prey characteristics [standard length (SL), body weight and burst swimming speed], whilst multi-species trials were conducted on open patch reefs, manipulating prey body weight only. Relationships between the nine measures of condition/performance were generally poor, with the strongest correlations occurring between the morphological measures and within the performance measures. During aquaria trials, P. fuscus was found to be selective with respect to prey SL only, with larger individuals being selected significantly more often. Multi-species predator communities, however, were selective with respect to prey body weight, with heavier individuals being selected significantly more often than their lighter counterparts. Our results suggest that under controlled conditions, body length may be the most important prey characteristic influencing prey survival during predatory encounters with P. fuscus. In such cases, larger prey size may actually be a distinct disadvantage to survival. However, these relationships appear to be more complex under natural conditions, where the expression of prey characteristics, the selectivity fields of a number of different predators, their relative abundance, and the action of external environmental characteristics, may all influence which individuals survive.     

Population dynamics of prey exhibiting inducible defenses: the role of associated costs and density-dependence

The effect of antipredator behavior on the dynamics of a resource-consumer model was analyzed in relation to the magnitude of associated costs, and the strength of density-dependence. For this purpose, I present a deterministic continuous resource-consumer model that exhibits biomass conversion, structural homogeneity, and competition for renewable and fixed resources as separate processes. Antipredator behavior is incorporated as an inducible response to consumer density, and has metabolic and feeding costs. By means of numerical methods, I show: (1) that antipredator behavior is stabilizing for certain parameter ranges, where other stabilizing forces do not dominate the dynamics; (2) intraspecific competition for both fixed and renewable resources have a stabilizing role; (3) metabolic cost is always stabilizing, and feeding cost can be stabilizing or destabilizing, depending on the relative strength of the two competition forces.     

The impact of mortality on predator population size and stability in systems with stage-structured prey

The relationships between a predator population's mortality rate and its population size and stability are investigated for several simple predator-prey models with stage-structured prey populations. Several alternative models are considered; these differ in their assumptions about the nature of density dependence in the prey's population growth; the nature of stage-transitions; and the stage-selectivity of the predator. Instability occurs at high, rather than low predator mortality rates in most models with highly stage-selective predation; this is the opposite of the effect of mortality on stability in models with homogeneous prey populations. Stage-selective predation also increases the range of parameters that lead to a stable equilibrium. The results suggest that it may be common for a stable predator population to increase in abundance as its own mortality rate increases in stable systems, provided that the predator has a saturating functional response. Sufficiently strong density dependence in the prey generally reverses this outcome, and results in a decrease in predator population size with increasing predator mortality rate. Stability is decreased when the juvenile stage has a fixed duration, but population increases with increasing mortality are still observed in large areas of stable parameter space. This raises two coupled questions which are as yet unanswered; (1) do such increases in population size with higher mortality actually occur in nature; and (2) if not, what prevents them from occurring? Stage-structured prey and stage-related predation can also reverse the 'paradox of enrichment', leading to stability rather than instability when prey growth is increased.     

Effects of prey availability, facultative plant feeding, and plant defenses on a generalist insect predator

This study examined the effects of feeding interval, access to host plants (thus, a source of sap), and plant defenses on the predatory insect, Podisus maculiventris Say (Hemiptera: Pentatomidae). The experiment consisted of a 2 × 2 design with two feeding intervals (1 day or 5 days) and predators living on either tomato plants or plastic plants. Females fed every day had greater body weights and egg hatch rates than females fed every five days. Females on tomato plants lived longer than females on plastic plants. However, access to plants did not alleviate the effects of low prey level on predator weight or reproductive output. In a second experiment, third instar nymphs were placed on either tomato plants or plastic plants for four days to examine the effects of tomato trichome defenses on these predators. Nymphs on tomato plants experienced 50% mortality compared to 15% mortality for nymphs on plastic plants. Some nymphs living on tomato plants were trapped by the hairy trichomes of the plant; others had gummed up legs from the exudates of the plants’ glandular trichomes, which inhibited their movement and ability to feed on prey. Although predators appeared to benefit from feeding on tomato plants, their ability to live on the plants was negatively affected by the defensive features of the plants. The potential effects of trichome defenses on predator survival and population dynamics must be considered when evaluating the benefits of plants on insect predator life histories and efficacy as biological control agents.     

The effect of predator and prey density on the induced defence of a ciliate

1. The level of antipredator defence should be proportional to the actual attack probability to minimize the cost of defence and maximize the net benefit.
2. The hypothesis that the induced antipredator morphology of Euplotes octocarinatus is a graded response to the actual risk of predation by Stylonychia mytilus was tested by manipulating the density of both prey and predator populations.
3. The magnitude of the response was graded according to both predator and prey density. A dense prey population may be protective since a prey is more exposed to a predator's attack as a solitary individual.
4. The results suggest that Euplotes is able to 'estimate' the real risk of predation and respond appropriately, without mobilizing more resources than needed.
5. Separation of the prey and predator with a nylon net revealed that the response was not induced by a water-transmitted factor but that direct cell-to-cell contacts were important. This finding departs from those of other studies.     

Relative growth rates of predator and prey dinosaurs reflect effects of predation

Hadrosaurs grew rapidly, and quantifying their growth is key to understanding life-history interactions between predators and prey during the Late Cretaceous. In this study, we longitudinally sampled a sequence of lines of arrested growth (LAGs) from an essentially full-grown hadrosaur Hypacrosaurus stebingeri (MOR 549). Spatial locations of LAGs in the femoral and tibial transverse sections of MOR 549 were measured and circumferences were calculated. For each bone, a time series of circumference data was fitted to several stochastic, discrete growth models. Our results suggest that the femur and the tibia of this specimen of Hypacrosaurus probably followed a Gompertz curve and that LAGs reportedly missing from early ontogeny were obscured by perimedullary resorption. In this specimen, death occurred at 13 years and took approximately 10-12 years to reach 95 per cent asymptotic size. The age at growth inflection, which is a proxy for reproductive maturity, occurred at approximately 2-3 years. Comparisons with several small and large predatory theropods reveal that MOR 549 grew faster and matured sooner than they did. These results suggest that Hypacrosaurus was able to partly avoid predators by outgrowing them.     

Non-lethal effects of invertebrate predators on Daphnia: morphological and life-history consequences of water mite kairomone

1. Here, we report morphological and life-historical changes in the cladoceran Daphnia ambigua in response to chemical cues released by the predatory water mite Piona chilensis . Both species are common inhabitants of southern temperate lakes.
2. We found significant differences in adult body size at first, second and third reproduction. Also, individuals exposed to kairomones had longer tail spines at first reproduction, and the resultant offspring had smaller bodies and shorter tail spines.
3. Exposure to mite cues did not exert effects on brood size at first reproduction, but decreased offspring number in subsequent broods. Similarly, only the second and third reproduction events were delayed by kairomone exposure.
4. The intrinsic population growth rate of predator-induced animals was lower than that in controls, but simulations based on a parameterized matrix model showed that the fitness costs could be overcome if the reported phenotypic responses reduced predation rate moderately. The gain in protection from predators needed to cancel out the reduction in fitness associated with predator cues was directly related to juvenile survival and fertility, and inversely related to adult survival.
5. This is the first work reporting phenotypic plasticity in Cladocera in response to kairomones released by water mites, which are conspicuous predators in many austral fresh waters.     

The effects of predator presence and shoal size on foraging in bluntnose minnows,Pimephales notatus

Synopsis Shoals of 3, 5, 7, 10, 15, and 20 bluntnose minnows,Pimephales notatus, were allowed to forage in the absence and presence of a fish predator, which was separated from the shoal by a clear plexiglass partition. A typical dilution effect was observed in that individual fish in larger shoals were approached less frequently by the predator. In the absence of a predator, foraging latency decreased significantly and the rate of foraging increased with increasing shoal size. Foraging latency for each shoal size tended to increase in the presence of a predator and foraging rate decreased, significantly for shoals of 7, 15, and 20 fish. Members of larger shoals were safer and enjoyed a greater level of food consumption, perhaps due to decreased individual vigilance for predators and social facilitation. However, foraging effort decreased when a predator was present, as more time was allocated to predator avoidance.     

Post-settlement effects of habitat type and predator size on cannibalism of glaucothoe and juveniles of red king crab Paralithodes camtschaticus

Postlarval (glaucothoe) and juvenile (first crab stage, C1) red king crab Paralithodes camtschaticus actively select structurally complex substrata for settlement. Such habitats may provide them with shelter from predation during critical early stages. We tested this hypothesis by placing glaucothoe and juvenile crab in aquaria with or without natural or artificial habitats, and with or without predators (1-3-year-old red king crab) of two different sizes. Predators caused increased mortality of glaucothoe, but predator size, habitat presence and habitat type had no effect on survival. Predators caused significant mortality of C1 crabs in the absence of habitat, and mortality was inversely related to predator size. Density of glaucothoe on habitats was similar with or without predators, but density of C1 crab on habitats was higher than that of glaucothoe, and increased in the presence of large predators. Active selection for complex substrata by settling glaucothoe does not reduce cannibalism, but may pre-position them for improved survival after metamorphosis. In contrast, juvenile crabs modify their behavior to achieve higher densities in refuge habitats, which tends to dampen the effect of predation. These survival strategies may have evolved to compensate for the greater risk of predation in open habitats.     

How predator functional responses and Allee effects in prey affect the paradox of enrichment and population collapses

In Rosenzweig-MacArthur models of predator-prey dynamics, Allee effects in prey usually destabilize interior equilibria and can suppress or enhance limit cycles typical of the paradox of enrichment. We re-evaluate these conclusions through a complete classification of a wide range of Allee effects in prey and predator's functional response shapes. We show that abrupt and deterministic system collapses not preceded by fluctuating predator-prey dynamics occur for sufficiently steep type III functional responses and strong Allee effects (with unstable lower equilibrium in prey dynamics). This phenomenon arises as type III functional responses greatly reduce cyclic dynamics and strong Allee effects promote deterministic collapses. These collapses occur with decreasing predator mortality and/or increasing susceptibility of the prey to fall below the threshold Allee density (e.g. due to increased carrying capacity or the Allee threshold itself). On the other hand, weak Allee effects (without unstable equilibrium in prey dynamics) enlarge the range of carrying capacities for which the cycles occur if predators exhibit decelerating functional responses. We discuss the results in the light of conservation strategies, eradication of alien species, and successful introduction of biocontrol agents.     

Predator-induced changes in morphology of a prey fish: the effects of food level and temporal frequency of predation risk

In a series of experiments, we investigated the effects of food availability and risk frequency on the dynamics of predator-induced changes in growth and morphology of prey fish using goldfish (Carassius auratus) as our test species. In experiment 1, we fed goldfish high or low food rations and exposed them to either alarm cues from conspecifics, cues from swordtails or a water control. After 60 days, goldfish in the alarm cue treatment significantly increased their body depth and body weight but had smaller body length than goldfish exposed to swordtails cues or water, likely reducing their vulnerability to gape-limited predators. Importantly, food level had an impact on the amplitude of the morphological changes. In experiment 2, goldfish were exposed to two different frequencies of predation cues or a water control for 50 days. The cues were either continued or discontinued from day 51 to 100, and all cues were resumed from day 101 to 150. We found that goldfish exposed to predation cues increased their depth and weight at a faster rate than did the goldfish exposed to water, and of particular significance was the fact that frequency of risk had an effect on the amplitude of the change. When the cues were interrupted, the increase in growth rate parameters was reduced to the level of the goldfish exposed to water. However, when the cues were resumed, the rate increased to match the growth rate of the goldfish that were continuously exposed to the cues. Finally, we staged encounters between goldfish of differing morphologies and yellow perch (Perca flavescens) and found that deep-bodied goldfish had better survival than the shallow-bodied ones. These experiments illustrate the dynamic nature of inducible morphological defences.