Masting behaviour in a Mediterranean pine tree alters seed predator selection on reproductive output

• Context‐dependency in species interactions is widespread and can produce concomitant patterns of context‐dependent selection. Masting (synchronous production of large seed crops at irregular intervals by a plant population) has been shown to reduce seed predation through satiation (reduction in rates of seed predation with increasing seed cone output) and thus represents an important source of context‐dependency in plant‐animal interactions. However, the evolutionary consequences of such dynamics are not well understood.
• Here we describe masting behaviour in a Mediterranean model pine species (Pinus pinaster) and present a test of the effects of masting on selection by seed predators on reproductive output. We predicted that masting, by enhancing seed predator satiation, could in turn strengthen positive selection by seed predators for larger cone output. For this we collected six‐year data (spanning one mast year and five non‐mast years) on seed cone production and seed cone predation rates in a forest genetic trial composed by 116 P. pinaster genotypes.
• Following our prediction, we found stronger seed predator satiation during the masting year, which in turn led to stronger seed predator selection for increased cone production relative to non‐masting years.
• These findings provide evidence that masting can alter the evolutionary outcome of plant‐seed predator interactions. More broadly, our findings highlight that changes in consumer responses to resource abundance represent a widespread mechanism for predicting and understanding context dependency in plant‐consumer evolutionary dynamics.

     

Predation risk affects the levels of maternal immune factors in avian eggs

Predation risk is an environmental stressor that can induce changes in prey behavior and physiology. Perception of predation risk may indirectly affect offspring traits and future fitness prospects via impacts on the condition of parents. Females may influence the survival of their offspring via maternal effects, especially when breeding in stressful conditions. We investigated the effects of continuous predation risk perceived by mothers on the maternal allocation of immune factors and carotenoids in eggs of the pied flycatcher Ficedula hypoleuca. We collected eggs from wild pied flycatchers that bred in the vicinity of a predator nest (pygmy owl Glaucidium passerinum), were exposed to cues of a mammalian nest predator (urine of least weasel Mustela nivalis), or received appropriate controls for these two groups. Pied flycatchers transferred more immunoglobulin in eggs under high predation risk in both owl and mammalian predator treatments. The presence of owl nests also lowered the level of lysozyme transferred in the eggs in one of the two study years. Predation risk did not modify egg size or overall carotenoid levels. Our results show that continuous predation risk perceived by females during egg‐laying affects egg composition. This different allocation of maternal immune factors may be an adaptive response evolved to increase the probability of offspring survival.     

Exclusion cage studies on the impact of predation on Helicoverpa armigera in cotton

The impact of predation on Helicoverpa armigera was studied in four field cage exclusion trials on cotton in Kenya. H. armigera egg cohorts were introduced inside predator‐free and open control cages, and the impact of local predator populations on the cohort was examined. Fourteen days after inoculation, exclusion cages had four times more larvae than controls, indicating a strong impact of predation. Ants and Anthocoridae were the predominant predator groups. Exclusion cages had more damaged fruiting plant parts (squares, flowers and bolls) than the control. In the absence of predators, natural mortality of H. armigera was greater as cotton matured, and is likely to be linked to the host plant condition.     

Within‐patch oviposition site shifts by spider mites in response to prior predation risks decrease predator patch exploitation

In egg‐laying animals with no post‐oviposition parental care, between‐ or within‐patch oviposition site selection can determine offspring survival. However, despite the accumulation of evidence supporting the substantial impact predators have on oviposition site selection, few studies have examined whether oviposition site shift within patches (“micro‐oviposition shift”) reduces predation risk to offspring. The benefits of prey micro‐oviposition shift are underestimated in environments where predators cannot disperse from prey patches. In this study, we examined micro‐oviposition shift by the herbivorous mite Tetranychus kanzawai in response to the predatory mite, Neoseiulus womersleyi, by testing its effects on predator patch exploitation in situations where predatory mites were free to disperse from prey patches. Adult T. kanzawai females construct three‐dimensional webs on leaf surfaces and usually lay eggs under the webs; however, females that have experienced predation risks, shift oviposition sites onto the webs even in the absence of current predation risks. We compared the predation of eggs on webs deposited by predator‐experienced females with those on leaf surfaces. Predatory mites left prey patches with more eggs unpredated when higher proportions of prey eggs were located on webs, and egg survival on webs was much higher than that on leaf surfaces. These results indicate that a micro‐oviposition shift by predator‐experienced T. kanzawai protects offspring from predation, suggesting adaptive learning and subsociality in this species. Conversely, fecundity and longevity of predator‐experienced T. kanzawai females were not reduced compared to those of predator‐naïve females; we could not detect any costs associated with the learned micro‐oviposition shift. Moreover, the previously experienced predation risks did not promote between‐patch dispersal of T. kanzawai females against subsequently encountered predators. Based on these results, the relationships of between‐patch oviposition site selection and micro‐oviposition shift are discussed.     

Risk‐taking behaviour may explain high predation mortality of GH‐transgenic common carp Cyprinus carpio

The competitive ability and habitat selection of juvenile all‐fish GH‐transgenic common carp Cyprinus carpio and their size‐matched non‐transgenic conspecifics, in the absence and presence of predation risk, under different food distributions, were compared. Unequal‐competitor ideal‐free‐distribution analysis showed that a larger proportion of transgenic C. carpio fed within the system, although they were not overrepresented at a higher‐quantity food source. Moreover, the analysis showed that transgenic C. carpio maintained a faster growth rate, and were more willing to risk exposure to a predator when foraging, thereby supporting the hypothesis that predation selects against maximal growth rates by removing individuals that display increased foraging effort. Without compensatory behaviours that could mitigate the effects of predation risk, the escaped or released transgenic C. carpio with high‐gain and high‐risk performance would grow well but probably suffer high predation mortality in nature.     

Different nest predator guild associated with egg size in the Patagonian temperate forest

Capsule: Studies of nest predation using artificial nests need to consider the effect of egg size on the types of predator that are detected.

Aims: To estimate the nest predation rate in the Patagonian temperate forest and evaluate the influence of egg size on predator guild.

Methods: On different plant species, we placed 108 nests each containing eggs of either Atlantic Canary Serinus canaria or Common Quail Coturnix coturnix, and a model clay egg of equal size to the real egg. Nest predators were identified from the marks left on the clay eggs or by videos recorded using camera traps.

Results: 86% of the nests were predated. Birds, mainly Chimango Caracara Milvago chimango, were the main nest predators. A marsupial, the Monito del Monte Dromiciops gliroides, and rodents also contributed to nest predation. Nest predation rates were similar for both egg sizes but the nest predator guild was different. Birds and rodents preyed on both eggs but the Monito del Monte consumed mainly small eggs.

Conclusion: Egg size did not influence the rate of nest predation but, instead, affected the nest predator guild. Consequently, in order to avoid underestimating the impacts of small predators, egg size should be considered in studies of nest predation.     

Evaluating the enemies hypothesis in a clover‐cabbage intercrop: effects of generalist and specialist natural enemies on the turnip root fly (Delia floralis)

• 1 The relative importance of the resource concentration hypothesis and the enemies hypothesis was investigated for the turnip root fly Delia floralis in a cabbage–red clover intercropping system compared with a cabbage monoculture.
• 2 Delia floralis egg densities were measured as well as the activity‐densities of generalist predators in a field experiment during two growing seasons. In the second year, a study of egg predation with artificially placed eggs was conducted, in addition to a predator exclusion experiment, to estimate total predation during the season. Parasitization rates were estimated from samples of pupae.
• 3 Delia floralis oviposition was greater in the monoculture during both years. The predator activity‐densities differed between treatments and study years. The known natural enemies of Delia spp., Bembidion spp. and Aleochara bipustulata showed a strong response to a cultivation system with higher activity‐densities in the monoculture. The response, however, appeared to be caused primarily by habitat preferences and not by D. floralis egg densities.
• 4 The reduction in the number of D. floralis pupae in the intercropping may be explained by a disruption in oviposition behaviour caused by the presence of clover because neither predation, nor parasitization rates differed between cultivation systems.

     

Seed predation of Copaifera langsdorffii (Fabaceae): a tropical tree with supra‐annual fruiting

Seed predation is an important ecological and evolutionary force that directly affects the distribution of plant species. Copaifera langsdorffii is a tropical tree species with supra‐annual fruiting, which has its seeds predated by a specialist endogenous insect (Rynochenus brevicollis: Curculionidae) in the Brazilian savanna. Three hypotheses were addressed: (i) the predator satiation hypothesis, (ii) the resource concentration hypothesis and (iii) the larger seed predation hypothesis. A total of 112 individual C. langsdorffii were monitored monthly from January to August during four consecutive years (from 2008 to 2011) to determine the presence of fruits on each plant. All trees produced fruits in the year 2008, whereas none of them produced flowers or fruits in 2009 or 2010. Moreover, only 65 individuals (58%) marked in 2008 produced fruits in 2011. The number of fruits per plant was approximately 21% greater in 2008 than in 2011, while the percentage of seed predation was 76% greater in 2011, thereby supporting the predator satiation hypothesis. The percentage of seeds predated was not affected by the number of fruits per plant. Therefore, our data did not support the resource concentration hypothesis. Plants producing large seeds experienced more seed predation by R. brevicollis, supporting the larger seed predation hypothesis. In addition, we also observed a positive relationship between seed volume and adult R. brevicollis weight. This study demonstrates the importance of supra‐annual fruiting for increasing survivorship of C. langsdorffii seeds both at the individual and the population level, and suggests that seed predators select plants producing large seeds as a way of increasing the number of offspring.     

Seasonal variation of egg size and number in a Daphnia pulex population

Seasonal variation of egg size and number was examined in a Daphnia pulex population inhabiting a vernal pond. In this population, size at maturity declines at midseason, probably as an adaptive response to size-selective predation by larvae of the salamander Ambystoma. The larger early season individuals produce more and larger eggs than the smaller late season individuals. Age at maturity does not vary between seasons. Laboratory experiments indicate that temperature may affect egg size, egg number and size at maturity. However, field data suggest that temperature accounts for only a small fraction of the total variation in egg size and number. Indirect measures of nutrition indicate that food limitation does not cause the seasonal decline in egg size and number. The seasonal change in reproductive traits is well correlated with changes in invertebrate and vertebrate predation. Examination of predator feeding preferences and their impact on Daphnia mortality indicate that variation of reproductive traits is most likely a complex adaptation to changing predation regimes.     

Predation-mediated Mortality of Early Life Stages: A Field Experiment with Nymphs of an Herbivorous Stick Insect (Metriophasma diocles)

We quantified predation pressure on first instar nymphs of a stick insect in predator‐exclusion experiments in the forest of Barro Colorado Island, Panamá. After considering intrinsic mortality (19%) and potential emigration (negligible), we estimated that 54 percent of the nymphs died due to predation in a two‐week period. Predation on nymphs was highest at night and may explain the low abundance of Metriophasma diodes in the understory.     

Tracking day and night provides insights into the relative importance of different wader chick predators

Poor reproductive success driven by nest and chick predation severely limits the population recovery of waders breeding on lowland wet grassland. Managing predation requires knowledge of the predators and because these can be grouped into nocturnal or diurnal hunters, detecting the timing of predation can help assess their relative impacts. Wader nest studies investigating the timing of egg predation have identified nocturnal mammals, primarily Red Foxes Vulpes vulpes, as the most important nest predators, but quantifying predator importance for highly mobile wader chicks is more difficult. Manual radiotelemetry can detect whether chicks are alive but cannot detect the time of predation, and predator identity can be determined only in the few cases where remains are recovered. As an alternative we used automatic radio tracking stations (ARTS) to constantly record the signals and predation timing of 179 radiotagged Lapwing Vanellus vanellus chicks, combining this with manual telemetry, inference about predator identity from predated remains and site‐level Fox, mustelid and avian predator activity monitoring. This approach succeeded in detecting the time of predation for 60% of the 155 chicks that were predated. Diurnal chick predation accounted for a larger number of predation events, but nocturnal predation was more intensive in terms of predation likelihood per hour. Mammalian predation during both day and night had a larger impact on chick survival than did avian predation. Raptors were primarily responsible for predation by birds and Foxes for predation by mammals, with Foxes also having a larger influence on daily chick predation rates than other predators. Chick predation increased seasonally, implying that earlier‐hatching breeding attempts are more likely to be successful. Higher Fox, raptor and mustelid activity resulted in higher proportions of chicks being predated by those predators, so quantifying the activity of those three predator groups on a site could be a quicker alternative to studying chicks when investigating which predator species to target with site‐specific predation management.     

Responses of pre‐dispersal seed predators to sequential flowering of Dipterocarps in Malaysia

Many species of Dipterocarpaceae and other plant families reproduce synchronously at irregular, multi‐year intervals in Southeast Asian forests. These community‐wide general flowering events are thought to facilitate seed survival through satiation of generalist seed predators. During a general flowering event, closely related Shorea species (Dipterocarpaceae) stagger their flowering times by several weeks, which may minimize cross pollination and interspecific competition for pollinators. Generalist, pre‐dispersal seed predators might also track flowering hosts and influence predator satiation. We addressed the question of whether pre‐dispersal seed predation differed between early and late flowering Shorea species by monitoring flowering, fruiting and seed predation intensity over two general flowering events at the Pasoh Research Forest, Malaysia. Pre‐dispersal insect seed predators killed up to 63 percent of developing seeds, with Nanophyes shoreae, a weevil that feeds on immature seeds being the most important predator for all Shorea species. This weevil caused significantly greater pre‐dispersal seed predation in earlier flowering species. Long larval development time precluded oviposition by adults that emerged from the earliest flowering Shorea on the final flowering Shorea. In contrast, larvae of weevils that feed on mature seeds before seed dispersal (Alcidodes spp.), appeared in seeds of all Shorea species almost simultaneously. We conclude that general flowering events have the potential to satiate post‐dispersal seed predators and pre‐dispersal seed predators of mature fruit, but are less effective at satiating pre‐dispersal predators of immature fruit attacking early flowering species.     

The evolution of vertebrate eye size across an environmental gradient: phenotype does not predict genotype in a Trinidadian killifish

Vertebrates exhibit substantial variation in eye size. Eye size correlates positively with visual capacity and behaviors that enhance fitness, such as predator avoidance. This foreshadows a connection between predation and eye size evolution. Yet, the conditions that favor evolutionary shifts in eye size, besides the well‐known role for light availability, are unclear. We tested the influence of predation on the evolution of eye size in Trinidadian killifish, Rivulus hartii. Rivulus are located across a series of communities where they coexist with visually oriented piscivores ("high predation" sites), and no predators (“Rivulus‐only” sites). Wild‐caught Rivulus from high predation sites generally exhibited a smaller relative eye size than communities that lack predators. Yet, such differences were inconsistent across rivers. Second‐generation common garden reared fish revealed repeatable decreases in eye size in Rivulus from high predation sites. We performed additional experiments that tested the importance of light and resources on eye size evolution. Sites that differ in light or resource availability did not differ in eye size. Our results argue that differences in predator‐induced mortality underlie genetically‐based shifts in vertebrate eye size. We discuss the drivers of eye size evolution in light of the nonparallel trends between the phenotypic and common garden results.     

Adaptive Sex‐Specific Cognitive Bias in Predation Behaviours of Japanese Pygmy Squid

Errors in decision‐making in animals can be partially explained by adaptive evolution, and error management theory explains that cognitive biases result from the asymmetric costs of false‐positive and false‐negative errors. Error rates that result from the cognitive bias may differ between sexes. In addition, females are expected to have higher feeding rates than males because of the high energy requirements of gamete production. Thus, females may suffer relatively larger costs from false‐negative errors (i.e. non‐feeding) than males, and female decisions would be biased to reduce these costs if the costs of false‐positive errors are not as high. Females would consequently overestimate their capacity in relation to the probability of predation success. We tested this hypothesis using the Japanese pygmy squid Idiosepius paradoxus. Our results show that size differences between the squid and prey shrimp affected predatory attacks, and that predatory attacks succeeded more often when the predator was relatively larger than the prey. Nevertheless, compared to male predatory attacks, female squid frequently attacked even if their size was relatively small compared to the prey, suggesting that the females overestimated their probability of success. However, if the females failed in the first attack, they subsequently adjusted their attack threshold: squid did not attack again if the prey size was relatively larger. These results suggest a sex‐specific cognitive bias, that is females skewed judgment in decision‐making for the first predation attack, but they also show that squid can modify their threshold to determine whether they should attack in subsequent encounters.     

Maternally induced intraclutch cannibalism: an adaptive response to predation risk?

Theory on condition‐dependent risk‐taking indicates that when prey are in poor condition, their anti‐predator responses should be weak. However, variation in responses resulting from differences in condition is generally considered an incidental by‐product of organisms living in a heterogeneous environment. Using Leptinotarsa decemlineata beetles and stinkbug (Podisus maculiventris) predators, we hypothesised that in response to predation risk, parents improve larval nutritional condition and expression of anti‐predator responses by promoting intraclutch cannibalism. We showed that mothers experiencing predation risk increase production of unviable trophic eggs, which assures provisioning of an egg meal to the newly hatched offspring. Next, we experimentally demonstrated that egg cannibalism reduces L. decemlineata vulnerability to predation by improving larval nutritional condition and expression of anti‐predator responses. Intraclutch cannibalism in herbivorous insects might be a ubiquitous strategy, aimed to overcome the dual challenge of feeding on protein‐limited diets while living under constant predation threat.     

Divergent natural selection promotes immigrant inviability at early and late stages of evolutionary divergence

Natural selection's role in speciation has been of fundamental importance since Darwin first outlined his theory. Recently, work has focused on understanding how selection drives trait divergence, and subsequently reproductive isolation. “Immigrant inviability,” a barrier that arises from selection against immigrants in their nonnative environment, appears to be of particular importance. Although immigrant inviability is likely ubiquitous, we know relatively little about how selection acts on traits to drive immigrant inviability, and how important immigrant inviability is at early‐versus‐late stages of divergence. We present a study evaluating the role of predation in the evolution of immigrant inviability in recently diverged population pairs and a well‐established species pair of Brachyrhaphis fishes. We evaluate performance in a high‐predation environment by assessing survival in the presence of a predator, and swimming endurance in a low‐predation environment. We find strong signatures of local adaptation and immigrant inviability of roughly the same magnitude both early and late in divergence. We find remarkably conserved selection for burst‐speed swimming (important in predator evasion), and selection for increased size in low‐predation environments. Our results highlight the consistency with which selection acts during speciation, and suggest that similar factors might promote initial population differentiation and maintain differentiation at late stages of divergence.     

Size selection by a gape‐limited predator of a marine snail: Insights into magic traits for speciation

The intertidal snail Littorina saxatilis has repeatedly evolved two parallel ecotypes assumed to be wave adapted and predatory shore crab adapted, but the magnitude and targets of predator‐driven selection are unknown. In Spain, a small, wave ecotype with a large aperture from the lower shore and a large, thick‐shelled crab ecotype from the upper shore meet in the mid‐shore and show partial size‐assortative mating. We performed complementary field tethering and laboratory predation experiments; the first set compared the survival of two different size‐classes of the crab ecotype while the second compared the same size‐class of the two ecotypes. In the first set, the large size‐class of the crab ecotype survived significantly better than the small size‐class both on the upper shore and in the laboratory. In the second set, the small size‐class of the crab ecotype survived substantially better than that of the wave ecotype both on the upper shore and in the laboratory. Shell‐breaking predation on tethered snails was almost absent within the lower shore. In the laboratory shore crabs (Pachygrapsus marmoratus) with larger claw heights selected most strongly against the small size‐class of the crab ecotype, whereas those with medium claw heights selected most strongly against the thin‐shelled wave ecotype. Sexual maturity occurred at a much larger size in the crab ecotype than in the wave ecotype. Our results showed that selection on the upper shore for rapid attainment of a size refuge from this gape‐limited predator favors large size, thick shells, and late maturity. Model parameterization showed that size‐selective predation restricted to the upper shore resulted in the evolution of the crab ecotype despite gene flow from the wave ecotype snails living on the lower shore. These results on gape‐limited predation and previous ones showing size‐assortative mating between ecotypes suggest that size may represent a magic trait for the thick‐shelled ecotype.     

Predatory blue crabs induce byssal thread production in hooked mussels

Abstract. Blue crabs (Callinectes sapidus) prey on hooked mussels (Ischadium recurvum) growing epizoically on oyster clumps in estuaries along the Louisiana coast. In prey size‐selection experiments, blue crabs preferred small mussels (<30‐mm shell length) to larger mussels, possibly because handling time increased with mussel size. When crabs were given a choice of solitary mussels versus mussels in clumps on oysters in the laboratory, mortality was lower by 86% in clumped mussels. However, no size selection by crabs occurred with mussels in clumps, likely because smaller mussels escaped predation in crevices between larger mussels or oysters. When individuals of two size classes of mussels were exposed to water containing the scent of crabs and of mussels consumed by blue crabs, an increase in byssal thread production was induced in all mussels, but byssal thread production rate was higher for small mussels than for large mussels. We conclude that increased predation risk for small mussels has resulted in higher size‐specific production of byssal threads, and that predator‐induced production of byssal threads, which may increase clumping behavior, may reduce their risk of mortality to predatory blue crabs.     

Impact of predation on early stages of the armoured catfish Hoplosternum thoracatum (Siluriformes-Callichthyidae) and implications for the syntopic occurrence with other related catfishes in a neotropical multi-predator swamp

This study investigated the role of predators in preventing competitive exclusion among three closely related armoured catfishes (Callichthys callichthys, Hoplosternum littorale and H. thoracatum) that occur synthopically in multi-predator freshwater swamps of Suriname, South America. The potential impact of predation on armoured catfish was determined by combining laboratory measurements of predation rates on five early developmental stages of the armoured catfish H. thoracatum for 24 aquatic predators with field studies of the density of the predators in the swamps. The contribution of a particular predator to the total predation pressure on its prey was determined to a large extent by the density of the predator in the swamp. Seemingly innocuous predators with low or moderate predation rates in the laboratory may be extremely important in the swamps due to their high abundance. Small-sized omnivorous fishes and aquatic invertebrates were major predators of early developmental stages of armoured catfish. Both qualitative and quantitative ontogenetic changes in the predation pressure on armoured catfish were observed. Major predation on eggs, larvae and juveniles of H. thoracatum resulted from a different set of predators in each developmental stage of the prey. In all developmental stages of H. thoracatum the predation pressure involved several predator species and not a single, dominant predator. The potential predation pressure of the 24 predators taken together and the number of predators that were able to prey on H. thoracatum decreased sharply with increasing age (size) of the prey. Even if egg (nest) predation is prevented by the guarding male, the potential impact of the 24 predators on the populations of armoured catfish is large. Predation may account for the high mortality of H. thoracatum observed in the swamps. The high predation pressure on callichthyid catfishes may help to explain the coexistence of three closely related and morphologically quite similar armoured catfishes in Surinamese swamps.     

Arthropod predation limits the population density of an herbivorous lady beetle,Henosepilachna niponica (Lewis)

1. The possible impact of arthropod predation on inter-population variation in adult density of a thistle-feeding lady beetle, Henosepilachna niponica (Lewis ) was evaluated by means of predator exclusion experiments conducted in the field.
2. The population density of newly-emerged adults at one habitat in the upstream area (site F) was significantly lower than at another in the downstream area (site A) although the egg density was nearly identical in the two habitats.
3. In the habitat with lower adult density, egg mortality was higher due to higher levels of predation. A predator exclusion experiment demonstrated that arthropod predation was the main factor causing high mortality during the immature stages, and physical factors such as heavy rains were unlikely to influence larval survivals.
4. Earwigs, ground beetles, predaceous stink bugs, and spiders were identified as the main predators in the study area. Of these, an earwig, Anechura harmandi (Burr ) was more predominant than other predators and was significantly more abundant in the habitat with low adult densities.