Damage released prey alarm substances or predator odours? Risk assessment by an aquatic oligochaete

Although the abilities of prey to detect and respond to chemical substances associated with a predator have been widely reported, the factors promoting the evolution of responses to prey alarm cues vs. predator odours are still vague. In this article, we combined field research with laboratory experiments to explore which chemical substance associated with predator activity (predator odour, conspecific or heterospecific alarm substances) induces defence responses in the aquatic oligochaete Stylaria lacustris, which is vulnerable to common littoral predators. The field results indicated that predators injure the oligochaetes and a great proportion, up to 45% of individuals in the population, were found to be damaged. The results of the laboratory experiments revealed that chemical odours from damselfly larvae feeding on S. lacustris did not induce the defence response in the oligochaetes. On the contrary, oligochaetes detected and responded to alarm substances from damaged conspecifics alone and substances from damaged cladoceran Daphnia magna. We discussed conditions favouring the responses to damage released prey alarm cues instead of predator odours in Stylaria lacustris. Our data suggest that the selection of responses to alarm cues from damaged prey vs. predator odours may be dependent on three factors: (1) non-species-specific predation, (2) divergence of food niche of the different stages of the predator and (3) complex food web with multiple predators. Handling editor: S. Declerk     

Response to conspecific and heterospecific alarm cues by pumpkinseeds in simple and complex habitats: field verification of an ontogenetic shift

Three focal size classes [small (<40 mm, standard length, L _S), medium (40–80 mm L _S) and large (>80 mm L _S)] of pumpkinseed Lepomis gibbosus were exposed to conspecific or one of three heterospecific chemical alarm cues under one of three levels of habitat complexity (low, intermediate and high). Under low and intermediate habitat complexities, pumpkinseeds <80 mm L _S exhibited a significant antipredator response when exposed to the chemical alarm cues of heterospecific prey guild members (largemouth bass Micropterus salmonides and hypoxanthine‐3‐ N ‐oxide, the putative Ostariophysan alarm 'pheromone'), while pumpkinseeds >80 mm L _S exhibited a foraging response. Under highly complex habitats, pumpkinseeds of all three size classes exhibited an antipredator response. Moreover, under all three habitat conditions, pumpkinseeds of all size classes exhibited an antipredator response to conspecific alarm cues. There was no change in behaviour under any treatment combination in response to an allopatric heterospecific control (swordtails Xiphophorus helleri ). These results provide the first field verification of the size dependent use of chemical alarm cues by centrarchids and demonstrate that microhabitat complexity significantly influences the threat‐sensitive use of these cues.     

Chemical cues related to conspecific size in pintado catfish, Pseudoplatystoma coruscans

The pintado (Pseudoplatystoma coruscans) is a ferocious carnivorous catfish with evident cannibalistic behaviour; its nocturnal habits are related to its ability to use predominately chemical sensorial modalities. This study investigated whether the pintado distinguishes conspecifics of different body sizes using chemical cues, which may reflect different physiological conditions such as hunger or stress. Pintados were observed when receiving water conditioned by either larger or similar-size conspecifics. A control group consisted of pintados receiving unconditioned water. Twelve repetitions were used for each condition. Feeding-like behaviours were investigated in the receiver fish and showed that they responded only to the conditioned water. Furthermore, a higher frequency of responses occurred when the water was conditioned by a similar-size conspecific. Thus, it is concluded that pintados are able to recognize conspecific size by chemical cues related to size and that this ability contributes to the individual's decision making on whether to approach or to avoid the conspecific.     

Degradation of chemical alarm cues and assessment of risk throughout the day

The use of chemical information in assessment of predation risk is pervasive across animal taxa. However, by its very nature, chemical information can be temporally unreliable. Chemical cues persist for some period of time after they are released into the environment. Yet, we know surprisingly little about the rate of degradation of chemical cues under natural conditions and hence little about how they function in temporal risk assessment under natural conditions. Here, we conducted an experiment to identify a concentration of fresh alarm cues that evoke a strong antipredator response in coral reef damselfish, Pomacentrus ambonensis. We then tested the rate at which these alarm cues degraded under natural conditions in ocean water, paying attention to whether the rate of degradation varied throughout the day and whether the temporal pattern correlated with physicochemical factors that could influence the rate of degradation. Fresh alarm cues released into ocean water evoke strong avoidance responses in juvenile fish, while those aged for 30 min no longer evoke antipredator responses. Fish exposed to cues aged for 10 or 20 min show intermediate avoidance responses. We found a marked temporal pattern of response throughout the day, with much faster degradation in early to mid‐afternoon, the time of day when solar radiation, temperature, dissolved oxygen, and pH are nearing their peak. Ecologists have spent considerable effort elucidating the role of chemical information in mediating predator–prey interactions, yet we know almost nothing about the temporal dynamics of risk assessment using chemical information. We are in dire need of additional comparative field experiments on the rate of breakdown of chemical cues, particularly given that global change in UV radiation, temperature, and water chemistry could be altering the rates of degradation and the potential use of this information in risk assessment.     

Size dependent predation risk in cryptic and conspicuous insects

It is not clear which selective pressures balance the strong fecundity advantage associated with large female body size in insects. A positively size-dependent mortality risk could provide a solution. In aviary experiments with artificial larvae, we studied if larger larvae of folivorous insects are more readily found (= detectability) and/or attacked (= acceptability) by birds. As size and colouration are likely to interact in determining birds’ responses, both cryptic and conspicuous prey items were used. As detectability is likely to be context-dependent, both simple (smooth) and complex (plants) backgrounds were used in respective experiments. In the conspicuous larvae, acceptability correlated negatively with prey size. However, their detectability was context dependent, being positively correlated with size on the simple background, whereas no significant effect was found on the complex background. Surprisingly, cryptic larvae showed no correlation between detectability and size, and there was only a weak tendency for birds to attack large larvae more readily. On the basis of a quantitative model, we conclude that the effect of positively size dependent bird predation, as a single factor, is not likely to counterbalance the fecundity advantage in cryptic species, and may thus not be crucial in determining the optimum for body sizes in these insects. In conspicuous species, there is a potential for different outcomes, because detectability and acceptability affect survival in different directions. The net outcome is, therefore, likely to be highly context-dependent. Furthermore, our results provide an explanation for the recently reported absence of systematic body-size differences between cryptic and conspicuous Lepidopteran larvae: although conspicuous larvae benefit from increasing their warning signal when growing larger, they also suffer a much sharper rise in detectability. Estonian Science Foundation grant # 5746; Centre for International Mobility (Finland).     

Feeding responses of the red fox (<Emphasis Type="Italic">Vulpes vulpes</Emphasis>) to different wild rabbit (<Emphasis Type="Italic">Oryctolagus cuniculus</Emphasis>) densities: a regional approach

We investigate the feeding responses of the red fox (Vulpes vulpes) at a regional scale to different densities of European wild rabbit (Oryctolagus cuniculus) in central–southern Spain. Rabbit abundance indices were obtained in 86 localities during summer 2002. The diet of the fox was studied by analysis of 114 scats collected in 47 of these localities. The feeding response of the fox was examined by a representation of the dry weight percent of rabbit in the diet as a function of the abundance of rabbits; this used data only from those localities where at least 3 scats were collected (70 fox scats from 18 localities). We evaluated the relationship between rabbit abundance and the diversity of the diet of the fox. The feeding patterns of red foxes approximated to Holling’s type III functional response, typical of opportunistic predators. There was a negative relationship between the diversity of the fox’s diet and the abundance of rabbits. Therefore, the fox apparently behaves as a facultative predator, feeding on rabbits when they are abundant and shifting to other prey (and hence a more diverse diet) when rabbits are scarce. These findings are the first step towards understanding the potential role of red foxes in regulating rabbit populations in central–southern Spain.     

Three approaches to estimate wolf Canis lupus predation rates on moose Alces alces populations

We employed three different methods to estimate predation rates on moose in a newly colonized wolf territory in Norway. In the first two methods, we estimated predation rates based on the difference in calf/cow ratios outside and inside the wolf pack territory from (1) hunter observations and (2) aerial surveys. In the last method, (3) we estimated loss of calves of radio-collared cows inside and outside the wolf pack territory. The difference in mortality rates estimated between the area subject to predation and the area outside the wolf pack territory essentially constitutes the additive component of predation. We also tested the sensitivity of violating the assumptions of methods 1 and 2 related to equal fecundity and mortality because of other factors than predation inside and outside the wolf pack territory. Predation rates varied considerably between years and methods used, with hunter observations (method 1) giving the lowest and aerial surveys (method 2) giving the highest estimates. Method 3 (radio telemetry) was the most direct assessment of predation and probably the best approach to estimate predation rates in moose. However, all three methods show the same yearly changes and may therefore be appropriate to question trends trough time or between areas.     

Ratio-dependent response of a temperate Australian estuarine system to sustained nitrogen loading

Classical resource- and the less studied ratio-dependent models of predator–prey relationships provide divergent predictions as to the sustained ecological effects of bottom-up forcing. While resource-dependent models, which consider only instantaneous prey density in modelling predator responses, predict community responses that are dependent on the number of trophic levels in a system, ratio-dependent models, which consider the number of prey per consumer, predict proportional increase in each level irrespective of chain length. The two models are only subtly different for systems with two or three trophic levels but in the case of four trophic levels, predict opposite effects of enrichment on primary producers. Despite the poor discriminatory power of tests of the models in systems with two or three trophic levels, field tests in estuarine and marine systems with four trophic levels have been notably absent. Sampling of phytoplankton, macroinvertebrates, invertebrate-feeding fishes, piscivorous fishes in Kooloonbung Creek, Hastings River estuary, eastern Australia, subject to over 20 years of sewage discharge, revealed increased abundances in all four trophic levels at the disturbed location relative to control sites. Increased abundance of phytoplankton at the disturbed site was counter to the predictions of resource-dependent models, which posit a reduction in the first trophic level in response to enrichment. By contrast, the increase in abundance of this first trophic level and the proportionality of increases in abundances of each of the four trophic groups to nitrogen loading provided strong support for ratio dependency. This first evidence of ratio dependence in an estuarine system with four trophic levels not only demonstrates the applicability of ecological theory which seeks to simplify the complexity of systems, but has implications for management. Although large nutrient inputs frequently induce mortality of invertebrates and fish, we have shown that smaller inputs may in fact enhance biomass of all trophic levels.     

Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics

To clarify functional and numerical responses to temporal and spatial variations of resources (resource tracking), and the population characteristics of the ladybird beetle Harmonia axyridis, I analyzed the results of a 3-year field observation at 24 sites (seven plant species) on eight species of aphids. The seasonal changes in the number of beetles estimated by the Jolly–Seber method were significantly correlated with those of aphids in the total area. The estimated values of population parameters suggested frequent immigration and emigration of the H. axyridis population, although reproductive rates between spring and summer were rather stable all 3 years (1.87–3.49). The staying time and the daily number of adults and eggs at each site were influenced not only by a single factor but also by interactions among time and quantity and quality of the prey. The adult movement showed two patterns, which corresponded with the movement within and between the subpopulations when an assemblage of H. axyridis occurring on the plants of the same species or genus was regarded as a subpopulation. Adult movement intensely occurred within a subpopulation, although the beetles moving between subpopulations had a significantly greater chance to reach the habitat with a high aphid density. The habitats of H. axyridis could be categorized into a suitable habitat for survival and reproduction and a temporal refuge. The results obtained here suggest that H. axyridis, with high ability of prey searching and reproduction, maintains a stable population in heterogeneous and temporal habitats by its resource tracking mechanisms. Received: March 8, 1999 / Accepted: April 25, 2000     

Olfactorily-mediated cortisol response to chemical alarm cues in zebrafish Danio rerio

Chemical cues released as a by-product of predation mediate antipredator behaviour, but little is known about the physiological responses to olfactory detection of predation risk. In this study, zebrafish Danio rerio were exposed to either chemical alarm cues from conspecifics, or water (control). Compared with water controls, D. rerio exposed to alarm cues responded behaviourally with antipredator behaviours such as erratic dashing and an increase in time spent near the bottom of the test aquarium. Danio rerio were sacrificed 5 min after exposure to test cues (alarm cues or water). Enzyme-linked immunosorbent assay (ELISA) revealed whole-body levels of cortisol that were significantly higher for fish exposed to alarm cues (mean ± SE, 11.9 ± 3.4 ng g⁻¹) than control fish (1.5 ± 0.7 ng g⁻¹). These data provide a benchmark for future studies of the proximate mechanisms of olfactorily mediated antipredator responses, modelling effects on aquatic life in a changing climate and, as a model organism, Danio rerio can further our understanding of anxiety in humans.     

Predator avoidance in phytophagous mites: response to present danger depends on alternative host quality

We studied whether volatiles released by putative host plants affect the antipredator response of an herbivorous mite, Tetranychus urticae, when the patch was invaded by Phytoseiulus persimilis. Tetranychus urticae laid a lower number of eggs on tomato leaves than on lima bean leaves, suggesting that lima bean is a preferred host food source for T. urticae. In addition, T. urticae preferred lima bean plant volatiles to tomato plant volatiles in a Y-tube olfactometer test. To investigate the antipredator response of T. urticae, we examined the migration of T. urticae from a lima bean leaf disc to a neighbouring leaf disc (either a tomato or lima bean leaf disc) when ten predators were introduced into the original lima bean disc. A Parafilm bridge allowed for migration between the leaf discs. No migrations occurred between leaf discs when there were no predators introduced to the original leaf disc. However, when predators were introduced migrations did occur. When the neighbouring leaf disc was upwind of the original disc, the migration rate of the mite from original lima bean leaf disc to a neighbouring tomato leaf disc was significantly lower than that to a neighbouring lima bean leaf disc. By contrast, when the neighbouring leaf disc was downwind of the original leaf disc, there was no difference in the migration rates between lima bean leaf discs and tomato leaf discs. The number of T. urticae killed by P. persimilis for each treatment was not different, and this clearly shows that the danger was the same in all treatments regardless of the decision made by T. urticae. From these results, we conclude that T. urticae change their antipredator response by evaluating the difference in host plant volatiles in the patch they inhabit.     

Modelling of predator–prey trophic interactions. Part II: Three trophic levels

A general class of lumped parameter models describing the local dynamics of a tri-trophic chain in a controlled environment is analyzed in detail. The trophic functions characterizing the interactions are defined only by some properties and allow us to treat both prey-dependent and ratio-dependent models in a unified manner. Conditions for existence and stability of extinction and coexistence equilibrium states are determined. Some peculiar aspects of the dynamics of the system depending on the bioecological parameters are presented, with particular attention to bistability situations, limit cycles and chaotic behaviours.     

Invasive plant architecture alters trophic interactions by changing predator abundance and behavior

As primary producers, plants are known to influence higher trophic interactions by initiating food chains. However, as architects, plants may bypass consumers to directly affect predators with important but underappreciated trophic ramifications. Invasion of western North American grasslands by the perennial forb, spotted knapweed (Centaurea maculosa), has fundamentally altered the architecture of native grassland vegetation. Here, I use long-term monitoring, observational studies, and field experiments to document how changes in vegetation architecture have affected native web spider populations and predation rates. Native spiders that use vegetation as web substrates were collectively 38 times more abundant in C. maculosa-invaded grasslands than in uninvaded grasslands. This increase in spider abundance was accompanied by a large shift in web spider community structure, driven primarily by the strong response of Dictyna spiders to C. maculosa invasion. Dictyna densities were 46–74 times higher in C. maculosa-invaded than native grasslands, a pattern that persisted over 6 years of monitoring. C. maculosa also altered Dictyna web building behavior and foraging success. Dictyna webs on C. maculosa were 2.9–4.0 times larger and generated 2.0–2.3 times higher total prey captures than webs on Achillea millefolium, their primary native substrate. Dictyna webs on C. maculosa also captured 4.2 times more large prey items, which are crucial for reproduction. As a result, Dictyna were nearly twice as likely to reproduce on C. maculosa substrates compared to native substrates. The overall outcome of C. maculosa invasion and its transformative effects on vegetation architecture on Dictyna density and web building behavior were to increase Dictyna predation on invertebrate prey ≥89 fold. These results indicate that invasive plants that change the architecture of native vegetation can substantially impact native food webs via nontraditional plant → predator → consumer linkages.     

Function of the web box as an anti-predator barrier in the spider mite,<Emphasis Type="Italic"> Schizotetranychus recki</Emphasis>

Spider mites inhabiting Sasa bamboo show considerable variation in traits believed to be the result of coevolution between predator and prey. In Schizotetranychus recki Ehara inhabiting the hairy leaves of a dwarf bamboo, Sasa senanensis, all quiescent stages, including eggs, appear within web boxes in the leaf hairs of their host plant, and this habit is thought to be a trait involved in predator avoidance. To test this hypothesis, the survival rates of S. recki eggs inside a web box and those freed of a web box were assessed in relation to six predator species that co-occur with the spider mite in the field. The results clearly show that the webbing behavior (web box) of S. recki has a function in avoiding five predator species. However, one predator species, Agistemus summersi Ehara, preyed more on eggs protected by a web box. This suggests that this predator species has a special trait to overcome the nest barriers.     

The effect of hunger level on predation dynamics in the spider Nesticodes rufipes: a functional response study

It is well known that a predator has the potential to regulate a prey population only if the predator responds to increases in prey density and inflicts greater mortality rates. Predators may cause such density-dependent mortality depending on the nature of the functional and numerical responses. As spiders are usually faced with a shortage of prey, the killing behavior of the spider Nesticodes rufipes at varying densities of Musca domestica was examined here through laboratory functional response experiments where spiders were deprived of food for 5 (well-fed) or 20 days (hungry). An additional laboratory experiment was also carried out to assess handling time of spiders. The number of prey killed by spiders over 24- and 168-h periods of predator–prey interaction was recorded. Logistic regression analyses revealed the type II functional response for both well-fed and hungry spiders. We found that the lower predation of hungry spiders during the first hours of experimentation was offset later by an increase in predation (explained by estimated handling times), resulting in similarity of functional response curves for well-fed and hungry spiders. It was also observed that the higher number of prey killed by well-fed spiders over a 24-h period of spider–prey interaction probably occurred due to their greater weights than hungry spiders. We concluded that hungry spiders may be more voracious than well-fed spiders only over longer time periods, since hungry spiders may spend more time handling their first prey items than well-fed spiders.     

Influence of ultraviolet-B radiation on growth,prevalence of deformities,and susceptibility to predation in Cascades frog (<Emphasis Type="Italic">Rana cascadae</Emphasis>) larvae

Ambient levels of ultraviolet-B radiation (UVB) have a variety of detrimental effects on aquatic organisms. These include death and effects on growth, development, physiology, and behavior. Amphibians show all of these effects. However, the effects vary with species, life history stage, and ecological context. Little is known about the implications of the detrimental effects of UVB on ecological dynamics. Our study was designed to test how UVB may affect predator–prey interactions, an important ecological dynamic. Specifically, we tested the effect of UVB on the susceptibility of Cascades frog (Rana cascadae) larvae to predation by rough-skinned newts (Taricha granulosa). We also further examined the sublethal effects of UVB on growth and development in Cascades frog larvae. We found no direct effect of UVB exposure on survival. However, UVB-exposed frog larvae displayed decreased growth and increased prevalence of deformities. UVB also caused increased susceptibility to predation, but there was a significant treatment–block interaction. UVB increased susceptibility to predation in two out of five blocks of Cascades frogs. The other three blocks did not show an effect of UVB on susceptibility to predation. Our study suggests that UVB can alter susceptibility to predation in at least one amphibian species. UVB-induced alteration of predator–prey interactions could potentially lead to changes at the population, community, and ecosystem levels. Handling editor: K. Martens     

The hypersensitive response is associated with host and nonhost resistance to Phytophthora infestans

The interaction between Phytophthora infestans (Mont.) de Bary and Solanum was examined cytologically using a diverse set of wild Solanum species and potato (S. tuberosum L.) cultivars with various levels of resistance to late blight. In wild Solanum species, in potato cultivars carrying known resistance (R) genes and in nonhosts the major defense reaction appeared to be the hypersensitive response (HR). In fully resistant Solanum species and nonhosts, the HR was fast and occurred within 22 h. This resulted in the death of one to three cells. In partially resistant clones, the HR was induced between 16 and 46 h, and resulted in HR lesions consisting of five or more dead cells, from which hyphae were occasionally able to escape to establish a biotrophic interaction. These results demonstrate the quantitative nature of the resistance to P. infestans. The effectiveness of the HR in restricting growth of the pathogen differed considerably between clones and correlated with resistance levels. Other responses associated with the defense reaction were deposition of callose and extracellular globules containing phenolic compounds. These globules were deposited near cells showing the HR, and may function in cell wall strengthening. Received: 22 April 1999 / Accepted: 4 November 1999     

Consumption of aphids by spiders and the effect of additional prey: evidence from microcosm experiments

Spiders are common generalist predators in agroecosystems and have been suggested to lower herbivore abundance in crops. It is not clear, however, if spiders can effectively suppress pest populations, and if so, by what mechanisms. In a microcosm experiment, we examined the consumption of the bird cherry-oat aphid, Rhopalosiphum padi L. (Homoptera: Aphididae), a pest species in wheat fields, by three spider species that differ in their hunting methods. We then tested the effect of additional prey type on the ability of erigonid spiders to reduce aphids. In a 48-h experiment Mermessus denticulatus (Banks) (Araneae: Linyphiidae; Erigoninae) consumed more aphids than did Enoplognatha gemina Bosmans and Van Keer (Araneae: Theridiidae) and Bathyphantes cf. extricatus (O·P.-Cambridge) (Araneae: Linyphiidae; Linyphiinae). This difference may be due to the ability of erigonids to forage actively on the vegetation in addition to using their webs to catch prey. In a 7-week experiment, we provided springtails (Collembola) in high and low densities as additional prey to mated erigonids, prior to aphid introduction. Spiders in the low-density springtail treatment built more webs on the vegetation, and caused a 50% reduction in aphid populations. There were significantly fewer aphids in the low-density springtail treatment, but not in the high-density treatment, in comparison to the control (high-density springtails without spiders). The results suggest that additional prey density affects predatory interactions between M. denticulatus and R. padi and that erigonids, which occur in high densities in wheat fields in the Negev desert, may be involved in aphid suppression in these agroecosystems.

Sharks modulate their escape behavior in response to predator size,speed and approach orientation

Escape responses are often critical for surviving predator–prey interactions. Nevertheless, little is known about how predator size, speed and approach orientation impact escape performance, especially in larger prey that are primarily viewed as predators. We used realistic shark models to examine how altering predatory behavior and morphology (size, speed and approach orientation) influences escape behavior and performance in Squalus acanthias, a shark that is preyed upon by apex marine predators. Predator models induced C-start escape responses, and increasing the size and speed of the models triggered a more intense response (increased escape turning rate and acceleration). In addition, increased predator size resulted in greater responsiveness from the sharks. Among the responses, predator approach orientation had the most significant impact on escapes, such that the head-on approach, as compared to the tail-on approach, induced greater reaction distances and increased escape turning rate, speed and acceleration. Thus, the anterior binocular vision in sharks renders them less effective at detecting predators approaching from behind. However, it appears that sharks compensate by performing high-intensity escapes, likely induced by the lateral line system, or by a sudden visual flash of the predator entering their field of view. Our study reveals key aspects of escape behavior in sharks, highlighting the modulation of performance in response to predator approach.