Causes of the species-area relationship by trophic level in a field-based microecosystem

Using a natural microecosystem, I test the contribution of the metapopulation effect to the species-area relationship, relative to that of the combined effects of habitat heterogeneity and sampling. The relative contributions were approximately equal, but with further relaxation of the fragmented community, the metapopulation effect is expected to increase. Predators had a greater slope to their species-area relationship than non-predators, and the habitat-plus-sampling effect was greater in predators than non-predators. This is the first attempt, to my knowledge, to quantify the causes of the species-area relationship.     

Testing sex-allocation theory: flowers vs seeds in hermaphrodite plants

Predators are usually thought to be rarer (in the sense of having lower population densities) than non-predators. Recent analyses have suggested that this is not the case because a decline in species richness compensates for the well-known decline in number of individuals with increasing trophic rank. I show that a variety of invertebrate communities contain more species of predators than would be expected from the number of predatory individuals. This is not due to differences in dominance or taxonomic resolution between predatory and non-predatory guilds, and implies that predators are indeed relatively rare. I suggest that patterns of energy flow and body size make it likely that there will be a higher proportion of predatory species than individuals in a community, provided that predators have moderately specialized diets.     

Antipredator behaviour and predator recognition in Belding's ground squirrels

This study evaluates whether Belding's ground squirrels (Spermophilus beldingi) recognize predators under natural conditions. I observed these squirrels for 300 h during two consecutive summers, during which I described 1029 aerial and terrestrial interactions, including 299 interactions with animals known to prey on squirrels. Squirrels responded differentially to predators and non-predators, to predators that hunt differently, and to contextually different interactions with the same predator. Responses shown in encounters with predators included Trill and Chirp vocalizing, upright Posting, crouching, running to burrow entrances, entering burrows, Approaching or chasing predators, and doubling-back on pursuing predators. Ground squirrels appear to adjust their antipredator behaviour depending on the amount and kind of danger they face during an encounter.     

Background level of risk determines how prey categorize predators and non-predators

Much of the plasticity that prey exhibit in response to predators is linked to the prey''s immediate background level of risk. However, we know almost nothing of how background risk influences how prey learn to categorize predators and non-predators. Learning non-predators probably represents one of the most underappreciated aspects of anti-predator decision-making. Here, we provide larval damselfish (Pomacentrus chrysurus) with a high or low background risk and then try to teach them to recognize a cue as non-threatening through the process of latent inhibition. Prey from the low-risk background that were pre-exposed to the novel odour cues in the absence of negative reinforcement for 3 days, and then provided the opportunity to learn to recognize the odour as threatening, failed to subsequently respond to the odour as a threat. Fish from the high-risk background showed a much different response. These fish did not learn the odour as non-threatening, probably because the cost of falsely learning an odour as non-threatening is higher when the background level of risk is higher. Our work highlights that background level of risk appears to drive plasticity in cognition of prey animals learning to discriminate threats in their environment.     

By their genes ye shall know them: genomic signatures of predatory bacteria

Predatory bacteria are taxonomically disparate, exhibit diverse predatory strategies and are widely distributed in varied environments. To date, their predatory phenotypes cannot be discerned in genome sequence data thereby limiting our understanding of bacterial predation, and of its impact in nature. Here, we define the ‘predatome,'' that is, sets of protein families that reflect the phenotypes of predatory bacteria. The proteomes of all sequenced 11 predatory bacteria, including two de novo sequenced genomes, and 19 non-predatory bacteria from across the phylogenetic and ecological landscapes were compared. Protein families discriminating between the two groups were identified and quantified, demonstrating that differences in the proteomes of predatory and non-predatory bacteria are large and significant. This analysis allows predictions to be made, as we show by confirming from genome data an over-looked bacterial predator. The predatome exhibits deficiencies in riboflavin and amino acids biosynthesis, suggesting that predators obtain them from their prey. In contrast, these genomes are highly enriched in adhesins, proteases and particular metabolic proteins, used for binding to, processing and consuming prey, respectively. Strikingly, predators and non-predators differ in isoprenoid biosynthesis: predators use the mevalonate pathway, whereas non-predators, like almost all bacteria, use the DOXP pathway. By defining predatory signatures in bacterial genomes, the predatory potential they encode can be uncovered, filling an essential gap for measuring bacterial predation in nature. Moreover, we suggest that full-genome proteomic comparisons are applicable to other ecological interactions between microbes, and provide a convenient and rational tool for the functional classification of bacteria.     

The role of differential reinforcement in predator avoidance learning

Little is known about how predator recognition develops under natural conditions. Predispositions to respond to some stimuli preferentially are likely to interact with the effects of experience. Convergent evidence from several studies suggests that predator-nai;ve tammar wallabies (Macropus eugenii) have some ability to respond to vertebrate predators differently from non-predators and that antipredator responses can be selectively enhanced by experience. Here, we examined the effects of differential reinforcement on responses to a model fox (Vulpes vulpes), cat (Felis catus) and conspecific wallaby. During training, tammars experienced paired presentations of a model fox and a simulated capture, as well as presentations of a wallaby and a cat alone. Training enhanced responses to the fox, relative to the conspecific wallaby, but acquired responses to the two predators did not differ, despite repeated, non-reinforced presentations of the cat. Results suggest that experience interacts with the wallabies' ability to perceive predators as a natural category.     

On reduced size in spiders from marginal habitats

Summary Four heathland spider species, Agroeca proxima, Centromerita concinna, Theridion simile, and Philodromus histrio, were studied in the Kalmthout National Nature Reserve in northern Belgium. They were caught by pitfall trapping or sweeping in different Calluna heath plots where the vegetation was in varying stages of development after being burnt, mowed, or grazed. Each species proved to thrive in a different plot, its numbers being greater and its size larger (cephalothorax width) in that plot. For the first two species positive correlations were found, for males as well as for females, between average size and numbers caught during a complete year cycle in a particular habitat.In contrast to non-predators, which are smaller when their populations are denser, spiders show a functional response that explains their increase in size with increasing density. It is suggested that in this respect a fundamental difference exists between predators and non-predators.     

How does the presence of predators influence the persistence of antipredator behavior?

We developed a virtual world to study the effect of predators on predator recognition. We trained a neural network to discriminate between the shapes of simulated aerial and terrestrial predators and non-predators. Then, the network's weighting values were fixed into the genomes of a set of autonomous agents. These animats were required to eat, avoid death due to starvation, and avoid predation, by fleeing from approaching predators. We systematically varied the predator's lethality, the mutation rate, the cost of fleeing a predator, and the presence or absence of aerial and terrestrial predators. We used ANOVA to analyse the average recognition ability (a measure of directional selection) and the standard deviation of recognition ability (a measure of relaxed selection) after 500 generations of selection. Mutation rate and the cost of flight had the greatest effect on both the average and standard deviation of recognition abilities. The loss of all predators relaxed selection on predator recognition abilities. The loss of specific predators had complex effects on recognition abilities. Persistence is largely influenced by escape costs.     

Can prey exhibit threat-sensitive generalization of predator recognition? Extending the Predator Recognition Continuum Hypothesis

Despite the importance of predator recognition in mediating predator-prey interactions, we know little about the specific characteristics that prey use to distinguish predators from non-predators. Recent experiments indicate that some prey who do not innately recognize specific predators as threats have the ability to display antipredator responses upon their first encounter with those predators if they are similar to predators that the prey has recently learned to recognize. The purpose of our present experiment is to test whether this generalization of predator recognition is dependent on the level of risk associated with the known predator. We conditioned fathead minnows to chemically recognize brown trout either as a high or low threat and then tested the minnows for their responses to brown trout, rainbow trout (closely related predator) or yellow perch (distantly related predator). When the brown trout represents a high-risk predator, minnows show an antipredator response to the odour of brown trout and rainbow trout but not to yellow perch. However, when the brown trout represents a low-risk predator, minnows display antipredator responses to brown trout, but not to the rainbow trout or yellow perch. We discuss these results in the context of the Predator Recognition Continuum Hypothesis.     

Coral reef fish rapidly learn to identify multiple unknown predators upon recruitment to the reef

Organisms often undergo shifts in habitats as their requirements change with ontogeny.Upon entering a new environment, it is vitally important to be able to rapidly assess predation risk. Predation pressure should selectively promote mechanisms that enable the rapid identification of novel predators. Here we tested the ability of a juvenile marine fish to simultaneously learn the identity of multiple previously unknown predators. Individuals were conditioned with a 'cocktail' of novel odours (from two predators and two non-predators) paired with either a conspecific alarm cue or a saltwater control and then tested for recognition of the four odours individually and two novel odours (one predator and one non-predator) the following day. Individuals conditioned with the 'cocktail' and alarm cue responded to the individual 'cocktail' odours with an antipredator response compared to controls. These results demonstrate that individuals acquire recognition of novel odours and that the responses were not due to innate recognition of predators or due to a generalised response to novel odours. Upon entering an unfamiliar environment prey species are able to rapidly assess the risk of predation, enhancing their chances of survival, through the assessment of chemical stimuli.     

Species richness of moss landscapes unaffected by short-term fragmentation

Theory predicts that habitat fragmentation and varying corridor length and width will affect animal populations in adjoining habitat patches due to varying migration rates. Previous work on the moss/microarthropod microcosm showed that connecting moss patches with moss corridors maintained species richness and individual species abundance. By contrast, in this study there was little evidence for differences in species richness between landscapes of varying connectivity and corridor length and width. The γ diversity, the cumulative species richness of entire connected systems, followed the same pattern. Similar non-significant results were obtained for species abundance. Contrary to a previous study, I found no evidence that populations of predators were more affected by fragmentation than non-predators. Since this experiment ran during temperate environmental conditions and the previous experiments ran during more extreme conditions, I hypothesise that corridors may be more useful in reducing species extinction during extreme environmental conditions.     

Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues

While ocean acidification is predicted to threaten marine biodiversity, the processes that directly impact species persistence are not well understood. For marine species, early life history stages are inherently vulnerable to predators and an innate ability to detect predators can be critical for survival. However, whether or not acidification inhibits predator detection is unknown. Here, we show that newly hatched larvae of the marine fish Amphiprion percula innately detect predators using olfactory cues and this ability is retained through to settlement. Aquarium-reared larvae, not previously exposed to predators, were able to distinguish between the olfactory cues of predatory and non-predatory species. However, when eggs and larvae were exposed to seawater simulating ocean acidification (pH 7.8 and 1000 p.p.m. CO₂) settlement-stage larvae became strongly attracted to the smell of predators and the ability to discriminate between predators and non-predators was lost. Newly hatched larvae were unaffected by CO₂ exposure and were still able to distinguish between predatory and non-predatory fish. If this impairment of olfactory preferences in settlement-stage larvae translates to higher mortality as a result of increased predation risk, there could be direct consequences for the replenishment and the sustainability of marine populations.
Ecology Letters (2010) 13: 68–75     

Innate predator recognition in giant pandas

Innate predator recognition confers a survival advantage to prey animals. We investigate whether giant pandas exhibit innate predator recognition. We analyzed behavioral responses of 56 naive adult captive giant pandas (Ailuropoda melanoleuca), to urine from predators and non-predators and water control. Giant pandas performed more chemosensory investigation and displayed flehmen behaviors more frequently in response to predator urine compared to both non-predator urine and water control. Subjects also displayed certain defensive behaviors, as indicated by vigilance, and in certain cases, fleeing behaviors. Our results suggest that there is an innate component to predator recognition in captive giant pandas, although such recognition was only slight to moderate. These results have implications that may be applicable to the conservation and reintroduction of this endangered species.     

Captive-born collared peccary (<Emphasis Type="Italic">Pecari tajacu</Emphasis>, Tayassuidae) fails to discriminate between predator and non-predator models

Captive animals may lose the ability to recognize their natural predators, making conservation programs more susceptible to failure if such animals are released into the wild. Collared peccaries are American tayassuids that are vulnerable to local extinction in certain areas, and conservation programs are being conducted. Captive-born peccaries are intended for release into the wild in Minas Gerais state, southeastern Brazil. In this study, we tested the ability of two groups of captive-born collared peccaries to recognize their predators and if they were habituated to humans. Recognition tests were performed using models of predators (canids and felids) and non-predators animals, as well as control objects, such as a plastic chair; a human was also presented to the peccaries, and tested as a separate stimulus. Anti-predator defensive responses such as fleeing and threatening displays were not observed in response to predator models. Predator detection behaviors both from visual and olfactory cues were displayed, although they were not specifically targeted at predator models. These results indicate that collared peccaries were unable to recognize model predators. Habituation effects, particularly on anti-predator behaviors, were observed both with a 1-h model presentation and across testing days. Behavioral responses to humans did not differ from those to other models. Thus, if these animals were to be released into the wild, they should undergo anti-predator training sessions to enhance their chances of survival.     

Double meaning of courtship song in a moth

Males use courtship signals to inform a conspecific female of their presence and/or quality, or, alternatively, to ‘cheat’ females by imitating the cues of a prey or predator. These signals have the single function of advertising for mating. Here, we show the dual functions of the courtship song in the yellow peach moth, Conogethes punctiferalis, whose males generate a series of short pulses and a subsequent long pulse in a song bout. Repulsive short pulses mimic the echolocation calls of sympatric horseshoe bats and disrupt the approach of male rivals to a female. The attractive long pulse does not mimic bat calls and specifically induces mate acceptance in the female, who raises her wings to facilitate copulation. These results demonstrate that moths can evolve both attractive acoustic signals and repulsive ones from cues that were originally used to identify predators and non-predators, because the bat-like sounds disrupt rivals, and also support a hypothesis of signal evolution via receiver bias in moth acoustic communication that was driven by the initial evolution of hearing to perceive echolocating bat predators.     

Predator discrimination and 'personality' in captive Vancouver Island marmots (Marmota vancouverensis)

A major impediment to recovering declining populations successfully is the mortality of reintroduced or translocated animals. We generally assume that captive-born animals may lose their antipredator behaviour abilities in captivity, but studies rarely compare predator recognition abilities of captive-born and wild-captured animals to test this. To identify whether predator discrimination abilities of the critically endangered Vancouver Island marmots Marmota vancouverensis were lost in captivity, we presented wild-captured and captive-born marmots with taxidermic mounts of predators (a cougar Felis concolor and wolf Canis lupus ) together with control stimuli (marmot, domestic goat Capra aegagrus , the cart on which all stimuli were presented and a 'blank' no-stimulus control). Regardless of specific predator discrimination abilities, for some species overall 'personality' may be associated with response to predators and subsequent survival. Thus, to quantify overall reactivity in the presence of a predator, we also conducted a mirror-image stimulus (MIS) presentation experiment where marmots were video-recorded with or without the presence of a wolf. Marmots discriminated among these stimuli, responding the most to the wolf and cougar. The MIS results suggest that marmots varied along a continuum of reactivity. The amount of reactivity was unaffected by the presence of a wolf, and was correlated with our highest level of responsiveness (vigilance at the burrow and time within the burrow) to the wolf. Taken together, we conclude that marmots differentiate predators from non-predators and that this ability has not been lost under the conditions in which they have been reared.     

Alien predators are more dangerous than native predators to prey populations

Alien predators are widely considered to be more harmful to prey populations than native predators. To evaluate this expectation, we conducted a meta-analysis of the responses of vertebrate prey in 45 replicated and 35 unreplicated field experiments in which the population densities of mammalian and avian predators had been manipulated. Our results showed that predator origin (native versus alien) had a highly significant effect on prey responses, with alien predators having an impact double that of native predators. Also the interaction between location (mainland versus island) and predator origin was significant, revealing the strongest effects with alien predators in mainland areas. Although both these results were mainly influenced by the huge impact of alien predators on the Australian mainland compared with their impact elsewhere, the results demonstrate that introduced predators can impose more intense suppression on remnant populations of native species and hold them further from their predator-free densities than do native predators preying upon coexisting prey.     

Do Père David's Deer Lose Memories of Their Ancestral Predators?

Whether prey retains antipredator behavior after a long period of predator relaxation is an important question in predator-prey evolution. Père David''s deer have been raised in enclosures for more than 1200 years and this isolation provides an opportunity to study whether Père David''s deer still respond to the cues of their ancestral predators or to novel predators. We played back the sounds of crows (familiar sound) and domestic dogs (familiar non-predators), of tigers and wolves (ancestral predators), and of lions (potential naïve predator) to Père David''s deer in paddocks, and blank sounds to the control group, and videoed the behavior of the deer during the experiment. We also showed life-size photo models of dog, leopard, bear, tiger, wolf, and lion to the deer and video taped their responses after seeing these models. Père David''s deer stared at and approached the hidden loudspeaker when they heard the roars of tiger or lion. The deer listened to tiger roars longer, approached to tiger roars more and spent more time staring at the tiger model. The stags were also found to forage less in the trials of tiger roars than that of other sound playbacks. Additionally, it took longer for the deer to restore their normal behavior after they heard tiger roars, which was longer than that after the trial of other sound playbacks. Moreover, the deer were only found to walk away after hearing the sounds of tiger and wolf. Therefore, the tiger was probably the main predator for Père David''s deer in ancient time. Our study implies that Père David''s deer still retain the memories of the acoustic and visual cues of their ancestral predators in spite of the long term isolation from natural habitat.     

Predators are less likely to misclassify masquerading prey when their models are present

Masquerading animals have evolved striking visual resemblances to inanimate objects. These animals gain protection from their predators not simply by avoiding detection, but by causing their predators to misclassify them as the ‘models’ that they appear to resemble. Using domestic chicks as predators and twig-mimicking caterpillars as prey, we demonstrated that masquerading prey were more likely to be misclassified as their models when viewed in isolation from their models than when viewed alongside examples of their model, although they benefitted from masquerade to some extent in both conditions. From this, we predict a selection pressure on masqueraders to use microhabitats that reduce the risk of them being viewed simultaneously with examples of their model, and/or to more closely resemble their model in situations where simultaneous viewing is commonplace.     

Phylogenetic signal,function and integration in the subunits of the carnivoran mandible

Complex phenotypes could be interpreted as the result of functional integration between identifiable subunits. Common developmental or ecological factors may favour macroevolutionary morphological integration so that functional subunits also covary above the species level. We investigate shape variation and functional integration in two subunits of the mammalian mandible: the corpus and the ramus in a subset of extant terrestrial Carnivora using geometric morphometric and comparative methods. More specifically, we test if corpus and ramus shape exhibit similar degree of homoplasy and if these traits covary above species level. Additionally, broad functional categorisations (predaceous and non predaceous) are investigated to test if differences in morphological variation and integration at macroevolutionary scale occur. Principal components of shape data show a significant phylogenetic signal in both mandibular subunits, with the ramus exhibiting a higher degree of homoplasy than the corpus. Functional groups (predators and non-predators) are significantly distinct in corpus shape, while in the ramus significance emerges only after removing the phylogenetic signal. Partial Least Square shows that mandibular corpus and ramus region covaries above species level even if this trend is not supported when employing comparative methods. Only in a subset of predaceous species covariation still hold. We conclude that mandibular subunits of Carnivora differ considerably in shape among predaceous and non-predaceous species because of the adaptive selection pressure imposed by catching and hold of live prey. This selective process also favoured macroevolutionary integration in predaceous carnivorans.