Does This Look Infected? Hidden Host Plant Infection by the Pathogen Botrytis cinerea Alters Interactions between Plants, Aphids and Their Natural Enemies in the Field.

Few studies have considered whether hidden (asymptomatic) plant pathogen infection alters ecological interactions at the higher trophic levels, even though such infection still affects plant physiology. We explored this question in two field experiments, where two varieties of lettuce (Little Gem, Tom Thumb) infected with Botrytis cinerea were either (1) naturally colonised by aphids or (2) placed in the field with an established aphid colony. We then recorded plant traits and the numbers and species of aphids, their predators, parasitoids and hyperparasitoids. Infection significantly affected plant quality. In the first experiment, symptomatically infected plants had the fewest aphids and natural enemies of aphids. The diversity and abundance of aphids did not differ between asymptomatically infected and uninfected Little Gem plants, but infection affected the aphid assemblage for Tom Thumb plants. Aphids on asymptomatically infected plants were less attractive to predators and parasitoids than those on uninfected plants, while hyperparasitoids were not affected. In the second experiment, when we excluded natural enemies, aphid numbers were lower on asymptomatically and symptomatically infected plants, but when aphid natural enemies were present, this difference was removed, most likely because aphids on uninfected plants attracted more insect natural enemies. This suggests that hidden pathogen infection may have important consequences for multitrophic interactions.

Does urbanisation lead to parallel demographic shifts across the world in a cosmopolitan plant?

Urbanisation is occurring globally, leading to dramatic environmental changes that are altering the ecology and evolution of species. In particular, the expansion of human infrastructure and the loss and fragmentation of natural habitats in cities is predicted to increase genetic drift and reduce gene flow by reducing the size and connectivity of populations. Alternatively, the 'urban facilitation model' suggests that some species will have greater gene flow into and within cities leading to higher diversity and lower differentiation in urban populations. These alternative hypotheses have not been contrasted across multiple cities. Here, we used the genomic data from the GLobal Urban Evolution project (GLUE), to study the effects of urbanisation on non-adaptive evolutionary processes of white clover (Trifolium repens) at a global scale. We found that white clover populations presented high genetic diversity and no evidence of reduced Ne linked to urbanisation. On the contrary, we found that urban populations were less likely to experience a recent decrease in effective population size than rural ones. In addition, we found little genetic structure among populations both globally and between urban and rural populations, which showed extensive gene flow between habitats. Interestingly, white clover displayed overall higher gene flow within urban areas than within rural habitats. Our study provides the largest comprehensive test of the demographic effects of urbanisation. Our results contrast with the common perception that heavily altered and fragmented urban environments will reduce the effective population size and genetic diversity of populations and contribute to their isolation.

Meta-Analysis Suggests Differing Indirect Effects of Viral, Bacterial, and Fungal Plant Pathogens on the Natural Enemies of Insect Herbivores.

Indirect effects are ubiquitous in nature, and have received much attention in terrestrial plant-insect herbivore-enemy systems. In such tritrophic systems, changes in plant quality can have consequential effects on the behavior and abundance of insect predators and parasitoids. Plant quality as perceived by insect herbivores may vary for a range of reasons, including because of infection by plant pathogens. However, plant diseases vary in their origin (viral, bacterial or fungal) and as a result may have differing effects on plant physiology. To investigate if the main groups of plant pathogens differ in their indirect effects on higher trophic levels, we performed a meta-analysis using 216 measured responses from 29 primary studies. There was no overall effect of plant pathogens on natural enemy traits as differences between pathogen types masked their effects. Infection by fungal plant pathogens showed indirect negative effects on the performance and preference of natural enemies via both chewing and piercing-sucking insect herbivore feeding guilds. Infection by bacterial plant pathogens had a positive effect on the natural enemies (parasitoids) of chewing herbivores. Infection by viral plant pathogens showed no clear effect, although parasitoid preference may be positively affected by their presence. It is important to note that given the limited volume of studies to date on such systems, this work should be considered exploratory. Plant pathogens are very common in nature, and tritrophic systems provide an elegant means to examine the consequences of indirect interactions in ecology. We suggest that further studies examining how plant pathogens affect higher trophic levels would be of considerable value.

Map-A-Mole: Greenspace Area Influences the Presence and Abundance of the European Mole Talpa europaea in Urban Habitats.

The European mole Talpa europaea is common across much of Britain. It has a unique fossorial lifestyle, and evidence of its presence is readily identified through the presence of characteristic molehills. Although molehills are often a common sight in urban greenspaces, moles are remarkably understudied, with very few studies to date exploring the urban ecology of moles. Here, we investigate if factors such as greenspace (largely urban parks and playing fields) area, intensity of management, distance to nearest patch, amount of time the patch had been isolated from other green patches, and the amount of urbanization (constructed surfaces) surrounding the patch, influence the distribution and abundance of urban moles. Mole signs (hills and surface runs) were counted in all discrete urban greenspaces (excluding domestic gardens and one private golf course) within an 89.5 km2 area in the UK town of Reading. We found that 17 out of 59 surveyed sites contained moles, with their presence being recorded in greenspaces with a minimum patch area of approximately 0.1 km2 (10 ha). Where present, the abundance of mole territories in the greenspaces was associated with both the area of greenspace and degree of urbanization within 150 m of the patch boundary. While the former was not surprising, the latter outcome may be a consequence of sites with an increased risk of flooding being home to fewer moles, and the surrounding area is also less likely to be built upon. This case study highlights how choices made in designing urban green infrastructure will determine which species survive in urban areas long into the future.

Urbanisation alters ecological interactions: Ant mutualists increase and specialist insect predators decrease on an urban gradient.

The modification of habitats in urban areas is thought to alter patterns of species interactions, by filtering specialist species and those at higher trophic levels. However, empirical studies addressing these hypotheses remain limited in scope and number. This work investigates (1) how main urban land uses affect predator-prey and mutualistic interactions, and (2) how specialist and generalist predators respond to size and availability of urban green spaces. In a large town in the UK, experimental colonies of ant-attended Black bean aphid Aphis fabae and non-ant-attended Pea aphid Acyrthosiphon pisum were monitored over two years. Ants were more frequently found in highly urbanised sites; however mutualistic ants were also more often encountered when the habitat was more plant diverse. Aphids were not affected by urban land uses, but A. fabae numbers were positively related to the presence of mutualists, and so indirectly affected by urbanisation. Predators were the only group negatively affected by increased urbanisation, and specialist species were positively related to increased proportion of urban green areas within the habitats. While this work supports the hypothesis that specialist predators are negatively affected by urbanisation, we also show that a fundamental ecological interaction, mutualism, is affected by urbanisation.

Asymptomatic Host Plant Infection by the Widespread Pathogen Botrytis cinerea Alters the Life Histories, Behaviors, and Interactions of an Aphid and Its Natural Enemies.

Plant pathogens can profoundly affect host plant quality as perceived by their insect herbivores, with potentially far-reaching implications for the ecology and structure of insect communities. Changes in host plants may have direct effects on the life-histories of their insect herbivores, which can then influence their value as prey to their natural enemies. While there have been many studies that have explored the effects of infection when plants show symptoms of disease, little is understood about how unexpressed infection may affect interactions at higher trophic levels. We examined how systemic, asymptomatic, and seed-borne infection by the ubiquitous plant pathogen Botrytis cinerea, infecting two varieties of the lettuce Lactuca sativa, affected aphids (the green peach aphid, Myzus persicae) and two widely used biocontrol agents (the parasitoid Aphidius colemani and the ladybird predator Adalia bipunctata). Lettuce varieties differed in host plant quality. Asymptomatic infection reduced chlorophyll content and dry weight of host plants, irrespective of plant variety. Aphids reared on asymptomatic plants were smaller, had reduced off-plant survival time and were less fecund than aphids reared on uninfected plants. Parasitoids showed reduced attack rates on asymptomatically infected plants, and wasps emerging from hosts reared on such plants were smaller and showed reduced starvation resistance. When given a choice in an olfactometer, aphids preferentially chose uninfected plants of one variety (Tom Thumb) but showed no preference with the second (Little Gem) variety. Parasitoids preferentially chose aphids on uninfected plants, irrespective of host plant variety, but ladybirds did not show any such preference. These results suggest that the reduced quality of plants asymptomatically infected by Botrytis cinerea negatively affects the life history of aphids and their parasitoids, and alters the behaviors of aphids and parasitoids, but not of ladybirds. Fungal pathogens are ubiquitous in nature, and this work shows that even when host plants are yet to show symptoms, pathogens can affect interactions between insect herbivores and their natural enemies. This is likely to have important implications for the success of biological control programs.

Increasing game prices may alter farmers' behaviours towards leopards (Panthera pardus) and other carnivores in South Africa.

Human-carnivore conflict occurs globally, particularly in regions where large carnivores predate livestock. Retaliatory killings do occur, and although predation of livestock by carnivores happens, losses from other factors such as disease or injury can be misattributed because of landowner perceptions. Game farming for both trophy hunting and eco-tourism is becoming increasingly common in South Africa, and there has been a rapid increase in the cost of game animals (in some species as much as five-fold) between 2010 and 2015. This could result in an increase in conflict between commercial game farmers and carnivores. We conducted two questionnaire surveys of farmers in 2010 and 2015 to investigate this. We asked if there had been changes in farming practices, perceived predator activity, perceived amount of livestock and commercial game losses, and actions taken towards carnivores in a South African farming community. We found no significant change in farming types in the area or losses of livestock between the years. However, there was a significant increase in perceived commercial game losses reported, even though protection of game had increased. Actions taken towards carnivores by livestock/game farmers were also significantly more negative in 2015 compared to farmers growing crops, but there was no such difference in 2010. We suggest that these changes could be a result of the increase in game prices over that period, leading to greater financial losses when an animal is predated, which in turn could increase the likelihood of retaliatory killings of carnivores.

The Curious Case of the Camelthorn: Competition, Coexistence, and Nest-Site Limitation in a Multispecies Mutualism.

Myrmecophyte plants house ants within domatia in exchange for protection against herbivores. Ant-myrmecophyte mutualisms exhibit two general patterns due to competition between ants for plant occupancy: (i) domatia nest sites are a limiting resource and (ii) each individual plant hosts one ant species at a time. However, individual camelthorn trees (Vachellia erioloba) typically host two to four ant species simultaneously, often coexisting in adjacent domatia on the same branch. Such fine-grain spatial coexistence brings into question the conventional wisdom on ant-myrmecophyte mutualisms. Camelthorn ants appear not to be nest-site limited, despite low abundance of suitable domatia, and have random distributions of nest sites within and across trees. These patterns suggest a lack of competition between ants for domatia and contrast strongly with other ant-myrmecophyte systems. Comparison of this unusual case with others suggests that spatial scale is crucial to coexistence or competitive exclusion involving multiple ant species. Furthermore, coexistence may be facilitated when co-occurring ant species diverge strongly on at least one niche axis. Our conclusions provide recommendations for future ant-myrmecophyte research, particularly in utilizing multispecies systems to further our understanding of mutualism biology.

Supplementary feeding of wild birds indirectly affects ground beetle populations in suburban gardens.

Supplementary feeding of wild birds by domestic garden-holders is a globally widespread and popular form of human-wildlife interaction, particularly in urban areas. Vast amounts of energy are thus being added to garden ecosystems. However, the potential indirect effects of this activity on non-avian species have been little studied to date, with the only two previous studies taking place under experimentally manipulated conditions. Here we present the first evidence of a localised depletive effect of wild bird feeding on ground beetles (Coleoptera: Carabidae) in suburban gardens under the usual feeding patterns of the garden-holders. We trapped significantly fewer ground beetles directly under bird-feeding stations than in matched areas of habitat away from feeders. Video analysis also revealed significantly higher activity by ground-foraging birds under the feeding stations than in the control areas. Small mammal trapping revealed no evidence that these species differ in abundance between gardens with and without bird feeders. We therefore suggest that local increases in ground-foraging activity by bird species whose diets encompass arthropods as well as seed material are responsible for the reduction in ground beetle numbers. Our work therefore illustrates that providing food for wild birds can have indirect negative effects on palatable prey species under typical conditions.

Widespread supplementary feeding in domestic gardens explains the return of reintroduced Red Kites Milvus milvus to an urban area.

Reintroductions are commonly used to mitigate biodiversity loss. One prominent example is that of the Red Kite Milvus milvus, a charismatic raptor of conservation concern. This species has been reintroduced across the UK over the last 25 years following its near extinction after centuries of persecution. The species was not expected to recolonize urban areas; its historical association with human settlements is attributed to scavenging on human waste and refuse, a resource now greatly reduced on the streets of modern European cities. However, the species has become a common daytime visitor to a large conurbation centred on the town of Reading, southern England, approximately 20 km from the first English reintroduction site. Given a near-absence of breeding and roost sites, we investigated foraging opportunities and habitat associations that might explain use by Red Kites of this urban area. Surveys of discarded human foods and road-kill suggested that these could support at most 13-29 Kites per day. Face-to-face surveys of a cross-section of residents revealed that 4.5% (equivalent to 4349 households) provided supplementary food for Red Kites in their gardens. Using estimates of per-household resource provision from another study, we calculated that this is potentially sufficient to feed 142-320 Kites, a substantial proportion of the total estimated to visit the conurbation each day (between 140 and 440). Road transects found positive associations between Red Kites and residential areas. We suggest that the decision made by thousands of householders to provide supplementary food for Red Kites in their gardens is the primary factor explaining their daytime abundance in this urban area.

Spatio-temporal variation in predation by urban domestic cats (Felis catus) and the acceptability of possible management actions in the UK.

Urban domestic cat (Felis catus) populations can attain exceedingly high densities and are not limited by natural prey availability. This has generated concerns that they may negatively affect prey populations, leading to calls for management. We enlisted cat-owners to record prey returned home to estimate patterns of predation by free-roaming pets in different localities within the town of Reading, UK and questionnaire surveys were used to quantify attitudes to different possible management strategies. Prey return rates were highly variable: only 20% of cats returned ≥4 dead prey annually. Consequently, approximately 65% of owners received no prey in a given season, but this declined to 22% after eight seasons. The estimated mean predation rate was 18.3 prey cat⁻¹ year⁻¹ but this varied markedly both spatially and temporally: per capita predation rates declined with increasing cat density. Comparisons with estimates of the density of six common bird prey species indicated that cats killed numbers equivalent to adult density on c. 39% of occasions. Population modeling studies suggest that such predation rates could significantly reduce the size of local bird populations for common urban species. Conversely, most urban residents did not consider cat predation to be a significant problem. Collar-mounted anti-predation devices were the only management action acceptable to the majority of urban residents (65%), but were less acceptable to cat-owners because of perceived risks to their pets; only 24% of cats were fitted with such devices. Overall, cat predation did appear to be of sufficient magnitude to affect some prey populations, although further investigation of some key aspects of cat predation is warranted. Management of the predation behavior of urban cat populations in the UK is likely to be challenging and achieving this would require considerable engagement with cat owners.

Clonal variation in acetylcholinesterase biomarkers and life history traits following OP exposure in Daphnia magna.

Two clones of Daphnia magna (Standard and Ruth) were exposed for 7 days to sub-lethal concentrations of acephate (5.0 and 10.0 mg/L). Survivorship, individual growth, reproduction and the population growth rate (lambda) were evaluated over three weeks. Acetylcholinesterase (AChE) activity was measured on days 2, 7 and 21. Acephate exposure inhibited AChE activity but had no direct effect on life history (LH) traits. There was also no effect of clone on AChE activity, LH and lambda. However, a significant interaction between clone and acephate concentration was found on both fecundity and lambda. AChE inhibition at 48 h was associated with a decrease in lambda in the Standard clone and an increase in lambda in clone Ruth. Therefore, our findings show that genotypic variation will influence the link between AChE activity and toxic effects at higher levels of biological organisation in D. magna.

Relative importance of fertiliser addition to plants and exclusion of predators for aphid growth in the field.

Herbivore dynamics and community structure are influenced both by plant quality and the actions of natural enemies. A factorial experiment manipulating both higher and lower trophic levels was designed to explore the determinants of colony growth of the aphid Aphis jacobaeae, a specialist herbivore on ragwort Senecio jacobaea. Potential plant quality was manipulated by regular addition of NPK-fertiliser and predator pressure was reduced by interception traps; the experiment was carried out at two sites. The size and persistence of aphid colonies were measured. Fertiliser addition affected plant growth in only one site, but never had a measurable effect on aphid colony growth. In both habitats the action of insect predators dominated, imposing strong and negative effects on aphid colony performance. Ants were left unmanipulated in both sites and their performance on the aphid colonies did not significantly differ between sites or between treatments. Our results suggest that, at least for aphid herbivores on S. jacobaea, the action of generalist insect predators appears to be the dominant factor affecting colony performance and can under certain conditions even improve plant productivity.