Host Phenology Research Articles

Host phenology regulates parasite-host demographic cycles and eco-evolutionary feedbacks.

Parasite–host interactions can drive periodic population dynamics when parasites overexploit host populations. The timing of host seasonal activity, or host phenology, determines the frequency and demographic impact of parasite–host interactions, which may govern whether parasites sufficiently overexploit hosts to drive population cycles. We describe a mathematical model of a monocyclic, obligate‐killer parasite system with seasonal host activity to investigate the consequences of host phenology on host–parasite dynamics. The results suggest that parasites can reach the densities necessary to destabilize host dynamics and drive cycling as they adapt, but only in some phenological scenarios such as environments with short seasons and synchronous host emergence. Furthermore, only parasite lineages that are sufficiently adapted to phenological scenarios with short seasons and synchronous host emergence can achieve the densities necessary to overexploit hosts and produce population cycles. Host‐parasite cycles also generate an eco‐evolutionary feedback that slows parasite adaptation to the phenological environment as rare advantageous phenotypes can be driven extinct due to a population bottleneck depending on when they are introduced in the cycle. The results demonstrate that seasonal environments can drive population cycling in a restricted set of phenological patterns and provide further evidence that the rate of adaptive evolution depends on underlying ecological dynamics.

Climate-driven variation in biotic interactions provides a narrow and variable window of opportunity for an insect herbivore at its ecological margin.

Climate-driven geographic range shifts have been associated with transitions between dietary specialism and generalism at range margins. The mechanisms underpinning these often transient niche breadth modifications are poorly known, but utilization of novel resources likely depends on phenological synchrony between the consumer and resource. We use a climate-driven range and host shift by the butterfly Aricia agestis to test how climate-driven changes in host phenology and condition affect phenological synchrony, and consider implications for host use. Our data suggest that the perennial plant that was the primary host before range expansion is a more reliable resource than the annual Geraniaceae upon which the butterfly has become specialized in newly colonized parts of its range. In particular, climate-driven phenological variation in the novel host Geranium dissectum generates a narrow and variable 'window of opportunity' for larval productivity in summer. Therefore, although climatic change may allow species to shift hosts and colonise novel environments, specialization on phenologically limited hosts may not persist at ecological margins as climate change continues. We highlight the potential role for phenological (a)synchrony in determining lability of consumer-resource associations at range margins and the importance of considering causes of synchrony in biotic interactions when predicting range shifts. This article is part of the theme issue 'Species' ranges in the face of changing environments (Part II)'.

Variation of Stem Radius in Response to Defoliation in Boreal Conifers

In the long term, defoliation strongly decreases tree growth and survival. Insect outbreaks are a typical cause of severe defoliation. Eastern spruce budworm (Choristoneura fumiferana Clem.) outbreaks are one of the most significant disturbances of Picea and Abies boreal forests. Nevertheless, in boreal conifers, a 2-year defoliation has been shown to quickly improve tree water status, protect the foliage and decrease growth loss. It suggests that defoliation effects are time-dependent and could switch from favorable in the short term to unfavorable when defoliation duration exceeds 5–10 years. A better understanding of the effect of defoliation on stem radius variation during the needle flushing time-window could help to elucidate the relationships between water use and tree growth during an outbreak in the medium term. This study aims to assess the effects of eastern spruce budworm (Choristoneura fumiferana Clem.) defoliation and bud phenology on stem radius variation in black spruce [Picea mariana (Mill.) B.S.P.] and balsam fir [Abies balsamea (L.) Mill.] in a natural stand in Quebec, Canada. We monitored host and insect phenology, new shoot defoliation, seasonal stem radius variation and daytime radius phases (contraction and expansion) from 2016 to 2019. We found that defoliation significantly increased stem growth at the beginning of needle flushing. Needles flushing influenced the amplitude and duration of daily stem expansion and contraction, except the amplitude of stem contraction. Over the whole growing season, defoliation increased the duration of stem contraction, which in turn decreased the duration of stem expansion. However, the change (increase/decrease) of the duration of contraction/expansion reflects a reduced ability of the potential recovery from defoliation. Black spruce showed significantly larger 24-h cycles of stem amplitude compared to balsam fir. However, both species showed similar physiological adjustments during mild stress, preventing water loss from stem storage zones to support the remaining needles’ transpiration. Finally, conifers react to defoliation during a 4-year period, modulating stem radius variation phases according to the severity of the defoliation.

Predicting the occurrence of host‐associated differentiation in parasitic arthropods: a quantitative literature review

AbstractParasite populations associated with different host species can encounter a variety of isolating reproductive barriers, leading to each population independently accumulating genome‐wide genetic differences due to their host associations. This phenomenon is called host‐associated differentiation (HAD) and has been proposed as an indicator of early diversification among parasitic arthropods. Although many parasite–host case study systems have been tested for the genetic signature of HAD (e.g., FST≥0.15 between sympatric, host‐associated populations in the absence of allopatry), it is unknown which isolating reproductive barriers best predict the general occurrence of HAD. HAD development has been attributed to biological and ecological factors that either directly generate reproductive isolation between parasites living on different hosts, such as ‘immigrant inviability’ (i.e., lower fitness of immigrants in non‐native environments), or that promote the accumulation of host‐specific genetic adaptations, such as the gallmaking feeding mode. In fact, some of these factors are shared across multiple case studies, suggesting that the occurrence of HAD is generalizable and can be predicted based on the incidence of significant biological and ecological factors. By means of a discriminant function analysis (DFA), this research assessed 108 arthropod parasite–host case studies for ecological and biological factors significantly correlated with the occurrence of HAD and whether these factors could be used to distinguish the presence of HAD from its absence. The DFA demonstrated that case studies that developed HAD could be distinguished from case studies that did not develop HAD. The results of the DFA were corroborated by a ‘non‐iterative partial least squares’ (NIPALS) discriminant model and a nominal logistic regression. Case studies with HAD could be robustly separated from case studies without HAD based on the incidence of these predictive factors: immigrant inviability, gallmaking, endophagy, recent range invasions of either hosts or parasites, differential host phenology, and differential parasite morphology. These results were used in an infinite random forest analysis to generate a hierarchy of conditional probabilities that separated HAD presence from absence. The results provide researchers with a tool for reliably predicting which untested parasite–host system would likely develop HAD. Immigrant inviability, gallmaking, and their combination were strongly correlated with the presence of HAD, which indicated parasite–host systems with these traits were highly likely to develop HAD. Contrary to expectation, endophagous feeding was negatively correlated with HAD presence, which indicated phytophagous endophagous feeders (excepting gallmakers) were highly unlikely to develop HAD. Furthermore, parasitoids were shown to be just as likely to develop HAD as not. Unfortunately, potentially significant predictive factors (e.g., allochrony) were excluded from analysis because too few case studies have been specifically tested for these factors. Furthermore, this analysis was biased by the lack of ‘negative’ publication results and the overrepresentation of research laboratories that primarily study HAD. Future research should accumulate novel HAD case studies that specifically test for allochrony, differential microbial associations, and morphological differentiation.

Microbial effects on plant phenology and fitness.

Plant development and the timing of developmental events (phenology) are tightly coupled with plant fitness. A variety of internal and external factors determine the timing and fitness consequences of these life-history transitions. Microbes interact with plants throughout their life history and impact host phenology. This review summarizes current mechanistic and theoretical knowledge surrounding microbe-driven changes in plant phenology. Overall, there are examples of microbes impacting every phenological transition. While most studies have focused on flowering time, microbial effects remain important for host survival and fitness across all phenological phases. Microbe-mediated changes in nutrient acquisition and phytohormone signaling can release plants from stressful conditions and alter plant stress responses inducing shifts in developmental events. The frequency and direction of phenological effects appear to be partly determined by the lifestyle and the underlying nature of a plant-microbe interaction (i.e., mutualistic or pathogenic), in addition to the taxonomic group of the microbe (fungi vs. bacteria). Finally, we highlight biases, gaps in knowledge, and future directions. This biotic source of plasticity for plant adaptation will serve an important role in sustaining plant biodiversity and managing agriculture under the pressures of climate change.

Livestock grazing, climatic variation, and breeding phenology jointly shape disease dynamics and survival in a wild amphibian

Wildlife responses to infectious disease can be influenced by environmental stressors that alter host-pathogen dynamics. We investigated how livestock grazing, climatic variation, and breeding phenology influence disease prevalence and annual survival in boreal toad (Anaxyrus boreas boreas) populations challenged with Batrachochytrium dendrobatidis (Bd), a fungal pathogen implicated in global amphibian declines. We conducted a five-year (2015–2019) capture-recapture study of boreal toads (n = 1301) inhabiting pastures grazed by cattle in western Wyoming, USA. We employed structural equation models to determine whether the effects of climatic variation on Bd prevalence were direct or mediated through effects on breeding phenology and multi-state models to explore the interplay of grazing, weather, and Bd infection on adult survival. Higher winter snowpack was linked with shorter spring breeding seasons, which were associated with lower Bd prevalence. Boreal toads infected with Bd suffered increased mortality, but only at relatively cool temperatures. Although cattle grazing created warmer microclimates, likely by reducing vegetation cover, grazing-induced habitat changes did not scale up to influence adult survival. Our results suggest that boreal toads in cooler environments face increased risk of disease-induced mortality, possibly because infected individuals are not able to elevate body temperature to reduce or clear infection. More generally, we demonstrate that host-pathogen dynamics can be shaped jointly by independent and interactive effects of livestock grazing, breeding season length, and climatic variation. Future investigations of wildlife responses to disease therefore may benefit from considering anthropogenic land use and climatic regimes, including the effect of weather on host phenology.

Modelling parasitoid virulence evolution with seasonality

A recommendation of: Hannelore MacDonald, Erol Akçay, Dustin Brisson Host phenology can drive the evolution of intermediate virulence strategies in some obligate-killer parasites https://doi.org/10.1101/2021.03.13.435259

Population, Virulence, and Mycotoxin Profile of Fusarium spp. Associated With Basal Rot of Allium spp. in Vietnam.

Fusarium basal rot (FBR) is particularly problematic to Allium producers worldwide. In Vietnam, information on the profile of FBR is scarce, even though the presence of Fusarium spp. in Allium plants has long been recorded. In this study, a total of 180 isolates of Fusarium spp. were recovered from Allium bulbs/plants showing symptoms of FBR in 34 commercial Allium fields around Da Lat, Lam Dong, Vietnam. These isolates were identified to the species level by sequencing the internal transcribed spacer region and the translation elongation factor 1α gene. F. oxysporum was most prevalent (81%) in samples from all locations and Allium varieties, followed by F. solani (15%) and F. proliferatum (4%), which were only found in onion (Allium cepa L.). Pathogenicity tests on onion seedlings (56 isolates) and mini bulbs (10 isolates) indicated that onion can be infected by all of these species but virulence varied greatly between isolates. Moreover, isolates that were virulent on seedlings were sometimes not virulent on bulbs and vice versa, which points to a specialization of isolates for the host phenology. Mycotoxin analyses showed that the highest amounts of beauvericin were detected in seedlings and bulbs infected by F. oxysporum, whereas F. proliferatum was mainly responsible for the presence of fumonisin B1 in bulbs, suggesting a natural occurrence of beauvericin and fumonisin B1 in onions infected by these pathogens.

Temporal resource partitioning mitigates interspecific competition and promotes coexistence among insect parasites.

A key to understanding life's great diversity is discerning how competing organisms divide limiting resources to coexist in diverse communities. While temporal resource partitioning has long been hypothesized to reduce the negative effects of interspecific competition, empirical evidence suggests that time may not often be an axis along which animal species routinely subdivide resources. Here, we present evidence to the contrary in the world's most biodiverse group of animals: insect parasites (parasitoids). Specifically, we conducted a meta-analysis of 64 studies from 41 publications to determine if temporal resource partitioning via variation in the timing of a key life-history trait, egg deposition (oviposition), mitigates interspecific competition between species pairs sharing the same insect host. When competing species were manipulated to oviposit at (or near) the same time in or on a single host in the laboratory, competition was common, and one species was typically inherently superior (i.e. survived to adulthood a greater proportion of the time). In most cases, however, the inferior competitor could gain a survivorship advantage by ovipositing earlier (or in a smaller number of cases later) into shared hosts. Moreover, this positive (or in a few cases negative) priority advantage gained by the inferior competitor increased as the interval between oviposition times became greater. The results from manipulative experiments were also correlated with patterns of life-history timing and demography in nature: the more inherently competitively inferior a species was in the laboratory, the greater the interval between oviposition times of taxa in co-occurring populations. Additionally, the larger the interval between oviposition times of competing taxa, the more abundant the inferior species was in populations where competitors were known to coexist. Overall, our findings suggest that temporal resource partitioning via variation in oviposition timing may help to facilitate species coexistence and structures diverse insect communities by altering demographic measures of species success. We argue that the lack of evidence for a more prominent role of temporal resource partitioning in promoting species coexistence may reflect taxonomic differences, with a bias towards larger-sized animals. For smaller species like parasitic insects that are specialized to attack one or a group of closely related hosts, have short adult lifespans and discrete generation times, compete directly for limited resources in small, closed arenas and have life histories constrained by host phenology, temporal resource subdivision via variation in life history may play a critical role in allowing species to coexist by alleviating the negative effects of interspecific competition.

Genotype-environment interaction reveals varied developmental responses to unpredictable host phenology in a tropical insect.

Understanding the genetic architecture of life history plasticity may inform resilience under environmental change, but relatively little is known for the inhabitants of unpredictable wet-dry tropical environments. Here, I explore the quantitative genetics of juvenile growth and development relative to hostplant phenology in the butterfly Eurema hecabe. Wet season generations of this species breed explosively on leguminous annuals whereas dry season generations subsist at low density upon an alternative perennial host. The wet-to-dry season transition is temporally unpredictable and marked by widespread host defoliation, forcing a large cohort of stranded larvae to either pupate prematurely or prolong development in the hope of renewed foliage production. A split-brood experiment demonstrated greater performance on high quality annual as opposed to perennial host foliage and a marked decline under the stressed conditions faced by stranded wet season larvae. Genetic variances for rates of growth and development were equivalent among high quality treatments but strikingly elevated under resource stress, and the associated cross-environment genetic correlations were indistinguishable from zero. The results demonstrate genotype-environment interaction involving both rank order and variance scale, thereby revealing genetic variance for norms of reaction that may reflect variable risk aversion given an unpredictable tropical host phenology.

The powdery mildew disease of rubber (Oidium heveae) is jointly controlled by the winter temperature and host phenology.

Rubber powdery mildew disease (Oidium heveae) is a serious threat to natural rubber production (Hevea brasiliensis) in some rubber developing regions of the world. Both phenological- and meteorological-related factors have been reported influencing the powdery mildew disease. However, few studies have investigated the effects of both phenological- and meteorological-related factors on the disease. The objective of this study is to quantify the contributions of phenological- and meteorological-related factors to affect the disease. We used the partial least squares (PLS) regression method to comprehensively quantify the effects of thirty-five phenological related factors and six meteorological factors on the infection level of powdery mildew of rubber trees over 9-year records (2003-2011). The relative contributions of significant factors were further investigated by the variation partition analysis. We found that the most influential variables were the mean temperature during winter and the duration of leaf development to maturation which explained 32 and 26% of the variations in the infection level. We found the controlling role of winter mean temperature, for the first time, on the infection level of powdery mildew. The controlling role of winter temperature may have directly increase the infection level when winter temperature is high and indirectly increase the infection level through prolonging the duration of leaf development to maturation, although the duration itself had smaller influences. We detected a warming trend of the winter temperatures from 2003 to 2011, which indicates that the infection level of powdery mildew will be increased if the winter warming continues.

Prediction of leaf Bloch disease risk in Norwegian spring wheat based on weather factors and host phenology

Leaf blotch diseases (LBD), such as Septoria nodorum bloch (Parastagnospora nodorum), Septoria tritici blotch (Zymoseptoria tritici) and Tan spot (Pyrenophora tritici-repentis) can cause severe yield losses (up to 50%) in Norwegian spring wheat (Triticum aestivum) and are mainly controlled by fungicide applications. A forecasting model to predict disease risk can be an important tool to optimize disease control. The association between specific weather variables and the development of LBD differs between wheat growth stages. In this study, a mathematical model to estimate phenological development of spring wheat was derived based on sowing date, air temperature and photoperiod. Weather factors associated with LBD severity were then identified for selected phenological growth stages by a correlation study of LBD severity data (17 years). Although information regarding host resistance and previous crop were added to the identified weather factors, two purely weather-based risk prediction models (CART, classification and regression tree algorithm) and one black box model (KNN, based on K nearest neighbor algorithm) were most accurate to predict moderate to high LBD severity (>5% infection). The predictive accuracy of these models (76–83%) was compared to that of two existing models used in Norway and Denmark (60 and 61% accuracy, respectively). The newly developed models performed better than the existing models, but still had the tendency to overestimate disease risk. Specificity of the new models varied between 49 and 74% compared to 40 and 37% for the existing models. These new models are promising decision tools to improve integrated LBD management of spring wheat in Norway.

Invasive grass negatively affects growth and survival of an imperiled butterfly

With only ~1% of native prairie remaining in North America, populations of many prairie-obligate species, including the imperiled Dakota skipper butterfly, have drastically declined in recent decades. Unfortunately, population recovery is impeded by an insufficient understanding of Dakota skipper biology. Because larvae have never been naturally observed in the wild, even basic life history elements including preferred host plant(s) are not well understood, and potential hosts have been inferred from grasses inhabiting remnant sites rather than direct observations. To improve our understanding of Dakota skipper biology and habitat needs and inform recovery efforts, we conducted a no-choice performance experiment offering larvae 1 of 5 commonly occurring native grasses and 2 pervasive invasive grass species found across their historic range. We monitored larvae during key life history intervals and evaluated host plant quality by measuring larval and pupal mass, time to pupation, and survivorship. Larvae fed on all offered host grasses, but mass, phenology, and survivorship varied among treatments. Larvae reared on prairie dropseed and porcupine grass had the highest survival, the shortest time to adulthood, and the greatest mass, whereas larvae provided smooth brome and Kentucky bluegrass fared poorly for all observed metrics. All other grasses offered during the study were deemed ‘medium’ quality. Our results suggest that although larvae can feed on a variety of potential host plants, these hosts vary in quality. Invasive grasses across prairies in North America may pose an ecological trap to the conservation of Dakota skipper and other prairie-obligate Lepidoptera.

The role of host phenology for parasite transmission

Phenology is a fundamental determinant of species distributions, abundances, and interactions. In host–parasite interactions, host phenology can affect parasite fitness due to the temporal constraints it imposes on host contact rates. However, it remains unclear how parasite transmission is shaped by the wide range of phenological patterns observed in nature. We develop a mathematical model of the Lyme disease system to study the consequences of differential tick developmental-stage phenology for the transmission of B. burgdorferi. Incorporating seasonal tick activity can increase B. burgdorferi fitness compared to continuous tick activity but can also prevent transmission completely. B. burgdorferi fitness is greatest when the activity period of the infectious nymphal stage slightly precedes the larval activity period. Surprisingly, B. burgdorferi is eradicated if the larval activity period begins long after the end of nymphal activity due to a feedback with mouse population dynamics. These results highlight the importance of phenology, a common driver of species interactions, for the fitness of a parasite.

Brood parasitism, provisioning rates and breeding phenology of male and female magpie hosts

Parental care is a costly behaviour that raises the prospects of offspring survival. In species with biparental care these costs are shared by both parents, although there may be a conflict regarding the relative investment of each sex. Avian brood parasites leave all the costs of rearing offspring to their hosts. The magnitude of these costs and their consequences on the relative role of both sexes in parental care and future reproduction remain mostly unknown. Here, we investigate whether provisioning rate of nestlings by magpie hosts Pica pica differs between broods parasitized by the great spotted cuckoo Clamator glandarius and non‐parasitized broods, and whether the relative contribution of each sex to provisioning is affected by parasitism. Furthermore, we explore the effect of parasitism on magpie's future reproduction. We found that provisioning rate was similar in parasitized and non‐parasitized broods, and that the relative contribution of males and females was also similar, irrespectively of the parasitism status. However, rearing parasitic offspring seems to have a negative long‐term effect on magpie's breeding phenology in the following breeding season. Our results suggest that, although brood parasitism by great spotted cuckoos does not seem to influence the relative contribution of both sexes to parental care, it may entail long‐term extra costs in terms of breeding delay for magpies.

Intraspecific variation of body size in fleas: effects of host sex and flea phenology.

We investigated the effects of host sex and flea phenology (estimated as periods of high versus low abundance) on individual body size in four fleas of small mammals. Amalaraeus penicilliger and Ctenophthalmus uncinatus are ectoparasites of the bank vole Myodes glareolus, whereas Doratopsylla dasycnema and Palaeopsylla soricis are ectoparasites of the common shrew Sorex araneus. We found significant effects of host sex and phenology on the body size of all flea species, although there was no general trend in the directions of these effects. Larger A. penicilliger were found on female hosts, whereas larger P. soricis were found on male hosts. In the remaining species, larger fleas were collected from male hosts during periods of high abundance (male C. uncinatus and female D. dasycnema) and from female hosts during periods of low abundance (male C. uncinatus). Regarding phenology, larger fleas were recorded during periods of either high (A. penicilliger, C. uncinatus, D. dasycnema) or low (C. uncinatus, P. soricis) abundance, but this depended on flea and/or host sex. We conclude that the directions of the host sex and phenology effects varied between flea species. Furthermore, the direction of the host sex effect was mediated by the effect of phenology and vice versa.

Host phenologies and the life history of horsehair worms (Nematomorpha, Gordiida) in a mountain stream in northern Japan

AbstractThe occurrence of many parasites and their hosts vary conspicuously by season due to their periodic life history events. Nematomorphs are common parasites in terrestrial‐aquatic ecotones, but it is still unknown how the nematomorphs complete their complex life cycles by using multiple hosts that are potentially seasonally variable. In this study, we examined the life history of a nematomorph (Gordionus sp.) inhabiting a mountain stream in northern Japan by the seasonal survey of their infection on aquatic and terrestrial hosts and laboratory experiments. Adults of Gordionus sp. entered into stream from early June to mid‐July. The laboratory experiment suggested that the newly hatched larvae become infective to intermediate host (aquatic insect larvae) from September to November, depending on the water temperature. The nematomorph larvae infected aquatic insect hosts with diverse emergence phenology, which result in prolonged temporal window for the trophic transmission between aquatic and terrestrial hosts. The common definitive host (Pterostichus thunbergi) seemed to survive multiple years, which would allow the nematomorph larvae to fully develop within the infected host. Trophically transmitted parasites sometimes track a specific pathway of prey–predator interactions within a food web and thus are sensitive to temporal match–mismatch between intermediate and definitive hosts. Contrary to this, the nematomorphs we studied may benefit from using temporally diverse pathways across aquatic and terrestrial food webs, which may result in maintaining the populations in their seasonal environment.

Comparison of Survival and Development of Gypsy Moth Lymantria dispar L. (Lepidoptera: Erebidae) Populations from Different Geographic Areas on North American Conifers.

Host utilization information is critical to managers for estimating the hosts at risk and potential geographic range for gypsy moths from different geographic origins. In this study, the development and survival of gypsy moths from all three subspecies on 13 North American conifers and three broadleaf hosts were compared. There was variation in the ability of gypsy moth larvae from different geographic origins to utilize (survive and develop on) key North American conifers. However, that variation was not consistent within gypsy moth subspecies, but instead was more consistent with populations from different origins being preadapted to utilize different hosts and having different biologic traits. Some Asian populations developed and survived well on some conifers while populations from Europe and North America gained weight faster and/or survived better than some Asian populations. Although development was slower and survival poorer on several of the conifers, first instar larvae were able to utilize conifers unless the needles were tough or feeding deterrents were present. Host phenology was also critical since the early instars fed preferentially on new foliage or buds. Gypsy moth larvae can utilize many hosts, so this makes it a very adaptable invasive species that warrants taking measures to prevent its spread.

Exploring the role of host specialisation and oxidative stress in interspecific lifespan variation in subtropical tephritid flies

In herbivorous insects, the degree of host specialisation may be one ecological factor that shapes lifespan. Because host specialists can only exploit a limited number of plants, their lifecycle should be synchronised with host phenology to allow reproduction when suitable hosts are available. For species not undergoing diapause or dormancy, one strategy to achieve this could be evolving long lifespans. From a physiological perspective, oxidative stress could explain how lifespan is related to degree of host specialisation. Oxidative stress caused by Reactive Oxygen Species (ROS) might help underpin ageing (the Free Radical Theory of Aging (FRTA)) and mediate differences in lifespan. Here, we investigated how lifespan is shaped by the degree of host specialisation, phylogeny, oxidative damage accumulation and antioxidant protection in eight species of true fruit flies (Diptera: Tephritidae). We found that lifespan was not constrained by species relatedness or oxidative damage (arguing against the FRTA); nevertheless, average lifespan was positively associated with antioxidant protection. There was no lifespan difference between generalist and specialist species, but most of the tephritids studied had long lifespans in comparison with other dipterans. Long lifespan may be a trait under selection in fruit-feeding insects that do not use diapause.

Induced phenological avoidance: A neglected defense mechanism against seed predation in plants

Abstract Flowering phenology is an important life‐history trait affecting plant reproductive performance and is influenced by various abiotic and biotic factors. Pre‐dispersal seed predation and pollination are expected to impose counteracting selection pressure on flowering phenology, with pre‐dispersal seed predation expected to favour off‐peak flowering and pollination to favour synchronous flowering. Here we studied the effect of pre‐dispersal seed predation by the beetle Byturus ochraceus, a specialist seed herbivore, on the flowering phenology of Geum urbanum. This forest understorey plant species is self‐pollinating, so that the influence of seed predation can be studied independent from pollination. We measured in detail the timing and predation rate of individual flowers during two consecutive years in more than 60 individuals. We tested the hypotheses that pre‐dispersal seed predation exerts selection for within‐season compensatory flowering as well as for induced phenological avoidance in the following season. We found no indication for compensatory flowering within a growing season, but plants that experienced predation shifted their flowers to the end of the flowering season the subsequent year. This induced phenological avoidance points to a plastic response to pre‐dispersal seed predation that may be adaptive. Importantly, the delay in flower production came at a cost, since flowers later in the season had a reduced seed output, presumably because of increasing light limitation following forest canopy closure. Synthesis. Herbivory by specialist enemies can cause serious fitness decline in hosts. We here show that induced shifts in phenology can form an important defense strategy against pre‐dispersal seed predation. The induced mismatches between herbivore and host phenology are anticipated to be adaptive when herbivory is predictable across successive flowering periods.