Fungal metabolic plasticity and sexual development mediate induced resistance to arthropod fungivory

Prey organisms do not tolerate predator attack passively but react with a multitude of inducible defensive strategies. Although inducible defence strategies are well known in plants attacked by herbivorous insects, induced resistance of fungi against fungivorous animals is largely unknown. Resistance to fungivory is thought to be mediated by chemical properties of fungal tissue, i.e. by production of toxic secondary metabolites. However, whether fungi change their secondary metabolite composition to increase resistance against arthropod fungivory is unknown. We demonstrate that grazing by a soil arthropod, Folsomia candida, on the filamentous fungus Aspergillus nidulans induces a phenotype that repels future fungivores and retards fungivore growth. Arthropod-exposed colonies produced significantly higher amounts of toxic secondary metabolites and invested more in sexual reproduction relative to unchallenged fungi. Compared with vegetative tissue and asexual conidiospores, sexual fruiting bodies turned out to be highly resistant against fungivory in facultative sexual A. nidulans. This indicates that fungivore grazing triggers co-regulated allocation of resources to sexual reproduction and chemical defence in A. nidulans. Plastic investment in facultative sex and chemical defence may have evolved as a fungal strategy to escape from predation.     

Non‐trophic effects of oribatid mites on cord‐forming basidiomycetes in soil microcosms

1. Saprotrophic cord‐forming basidiomycetes are the primary agents of decomposition in forest ecosystems. Collembola and oribatid mites affect fungal growth and foraging, and therefore decomposition, through direct mycelial grazing. 2. Grazing on the fungal species Hypholoma fasciculare, Resinicium bicolor and Phanerochaete velutina by the collembola Folsomia candida, and the oribatid mites Steganacarus magnus, Euzetes globulus and Hermannia gibba was investigated in soil microcosms. 3. Folsomia candida grazed on all fungal species: radial extent of R. bicolor, hyphal coverage of all fungal species, and fractal dimension of R. bicolor and P. velutina were all reduced. Oribatid mites did not graze the fungi but did affect mycelial morphology. Steganacarus magnus caused a reduction in the radial extent of H. fasciculare, and the hyphal coverage and fractal dimension in both H. fasciculare and R. bicolor. Euzetes globulus and H. gibba reduced the hyphal coverage of P. velutina. 4. Oribatid mites are associated with a cornucopia of chemical secretions with possible anti‐fungal properties. Chemical analysis of H. gibba opisthonotal secretions revealed four main compounds, all of which are new to the known spectrum of opisthonotal components. The most abundant was (E)‐β‐farnesene. 5. Treatment effects were species‐specific in terms of both fungal and invertebrate species. This study provides the first evidence of non‐grazing effects of oribatid mites on fungal growth and morphology. This could potentially influence the spatial organisation of mycelium in forest soils and therefore the ability of fungi to locate, colonise and decompose dead organic matter.     

Specificity and stability of the Acromyrmex–Pseudonocardia symbiosis

The stability of mutualistic interactions is likely to be affected by the genetic diversity of symbionts that compete for the same functional niche. Fungus‐growing (attine) ants have multiple complex symbioses and thus provide ample opportunities to address questions of symbiont specificity and diversity. Among the partners are Actinobacteria of the genus Pseudonocardia that are maintained on the ant cuticle to produce antibiotics, primarily against a fungal parasite of the mutualistic gardens. The symbiosis has been assumed to be a hallmark of evolutionary stability, but this notion has been challenged by culturing and sequencing data indicating an unpredictably high diversity. We used 454 pyrosequencing of 16S rRNA to estimate the diversity of the cuticular bacterial community of the leaf‐cutting ant Acromyrmex echinatior and other fungus‐growing ants from Gamboa, Panama. Both field and laboratory samples of the same colonies were collected, the latter after colonies had been kept under laboratory conditions for up to 10 years. We show that bacterial communities are highly colony‐specific and stable over time. The majority of colonies (25/26) had a single dominant Pseudonocardia strain, and only two strains were found in the Gamboa population across 17 years, confirming an earlier study. The microbial community on newly hatched ants consisted almost exclusively of a single strain of Pseudonocardia while other Actinobacteria were identified on older, foraging ants in varying but usually much lower abundances. These findings are consistent with recent theory predicting that mixtures of antibiotic‐producing bacteria can remain mutualistic when dominated by a single vertically transmitted and resource‐demanding strain.     

Fruit,flies and filamentous fungi – experimental analysis of animal–microbe competition using Drosophila melanogaster and Aspergillus mould as a model system

In addition to their fundamental role in nutrient recycling, saprobiotic microorganisms may be considered as typical consumers of food‐limited ephemeral resource patches. As such, they may be engaged in inter‐specific competition with saprophagous animals feeding from the same resource. Bacteria and filamentous fungi are known to synthesise secondary metabolites, some of which are toxic and have been proposed to deter or harm animals. The microorganisms may, however, also be negatively affected if saprophagous animals do not avoid microbe‐laden resources but feed in the presence of microbial competitors. We hypothesised that filamentous fungi compete with saprophagous insects, whereby secondary metabolites provide a chemical shield against the insect competitors. For testing this, we developed a new ecological model system representing a case of animal–microbe competition between saprobiotic organisms, comprising Drosophila melanogaster and species of the fungus Aspergillus (A. nidulans, A. fumigatus, A. flavus). Infestation of Drosophila breeding substrate with proliferating fungal colonies caused graduated larval mortality that strongly depended on mould species and colony age. Confrontation with conidiospores only, did not result in significant changes in larval survival, suggesting that insect death may not be ascribed to pathogenic effects. When confronted with colonies of transgenic fungi that lack the ability to express the global secondary metabolite regulator LaeA (ΔlaeA), larval mortality was significantly reduced compared to the impact of the wild type strains. Yet, also in the ΔlaeA strains, inter‐specific variation in the influence on insect growth occurred. Competition with Drosophila larvae impaired fungal growth, however, wild type colonies of A. nidulans and A. flavus recovered more rapidly from insect competition than the corresponding ΔlaeA mutants (not in A. fumigatus). Our findings provide genetic evidence that toxic secondary metabolites synthesised by saprotrophic fungi may serve as a means to combat insect competitors. Variation in the ability of LaeA to control expression of various secondary metabolite gene clusters might explain the observed species‐specific variation in Drosophila–Aspergillus competition.     

Colony foraging allocation is finely tuned to food distance and sweetness even close to a bee colony

Social bee colonies can allocate their foraging resources over a large spatial scale, but how they allocate foraging on a small scale near the colony is unclear and can have implications for understanding colony decision‐making and the pollination services provided. Using a mass‐foraging stingless bee, Scaptotrigona pectoralis (Dalla Torre) (Hymenoptera: Apidae: Meliponini), we show that colonies will forage near their nests and allocate their foraging labor on a very fine spatial scale at an array of food sources placed close to the colony. We counted the foragers that a colony allocated to each of nine feeders containing 1.0, 1.5, or 2.0 M sucrose solution [31, 43, and 55% sucrose (wt/wt), respectively] at distances of 10, 15, and 20 m from the nest. A significantly greater number of foragers (2.6–5.3 fold greater) visited feeders placed 10 vs. 20 m away from the colony. Foraging allocation also corresponded to food quality. At the 10‐m feeders, 4.9‐fold more foragers visited 2.0 M as compared to 1.0 M sucrose feeders. Colony forager allocation thus responded to both differences in food distance and quality even when the travel cost was negligible compared to normal colony foraging distances (10 m vs. an estimated 800–1 710 m). For a nearby floral patch, this could result in unequal floral visitation and pollination.     

Synergistic effects of temperature,diet and colony size on the competitive ability of two ant species

Multiple biotic and abiotic factors influence species coexistence and co‐occurrence patterns. In a competitive environment, for example, temperature and diet variation may modify both foraging behaviour and aggression, thereby changing competitive interactions and species co‐occurrence patterns. In New Zealand, two endemic ant species (Prolasius advenus and Monomorium antarcticum) often form allopatric distributions; though also periodically do co‐occur in the same habitat. Here, we performed a long‐term laboratory experiment in an attempt to understand how diet, colony size and environmental conditions may influence these co‐occurrence patterns. The consequences of temperature and diet variation differed between P. advenus and M. antarcticum. Colonies of P. advenus exhibited increased aggression and foraging activities at higher temperatures. In addition, P. advenus colonies augmented their foraging activities when deprived of a carbohydrate‐rich food source. Conversely, small M. antarcticum colonies exhibited higher aggression than when in large colonies, and increased their foraging activities at lower temperatures. The modulation of aggression and foraging behaviour may influence the likelihood of small P. advenus and M. antarcticum colonies persisting in the long term. Our results are compatible with the hypothesis that the environment is likely to be a strong filter for the negative co‐occurrence patterns we observe between P. advenus and M. antarcticum in New Zealand. Furthermore, this study provides a mechanistic explanation for potential impacts of climate warming on community structure. Environmental modification of aggression and foraging behaviour could potentially alter competitive interactions and influence community assembly.     

Temporal variation in foraging activity and efficiency and the role of hitchhiking behaviour in the leaf-cutting ant, Atta cephalotes

Two phenomena are integral to the foraging behaviour of leaf‐cutting ants in the genus Atta: hitchhiking (where small ants ride on leaf fragments carried by larger workers) and rhythmic foraging (where foraging activity shows marked fluctuations over time). While parasitism by phorid flies has been implicated in eliciting both behaviours, recent research suggests fungal contaminants and the need to procure sap also play a key role in eliciting hitchhiking. For wild colonies of Atta cephalotes L. (Hymenoptera: Formicidae), we investigated the extent to which hitchhiking frequency varied in space and time and the foraging performance of day‐time and night‐time workers. Day‐time foragers were considerably smaller than nocturnal foragers, a trend previously described as a response to diurnal phorids. Despite their smaller size, day‐time foragers had higher foraging performance, perhaps as a consequence of decreased trail congestion. Larger leaf‐carriers were more likely to carry hitchhikers and hitchhiking frequency was higher at night, an observation that conflicts with the parasitoid defence hypothesis, but not with the leaf sap and fungal defence hypotheses. Hitchhikers constitute a major proportion (typically 12%) of the loads carried by workers, and have three times the effect of leaf fragment mass on forager velocity. However, they reduced energetic efficiency by only 2.6% and provisioning rate by 5.9%. Our results provide partial support for the parasitoid defence hypothesis, but suggest that both the risks of parasitism and the opportunity‐cost to foraging associated with carrying hitchhikers may be low.     

Plasticity in Forest Tent Caterpillar Collective Foraging Schedules

Self‐organization can generate synchronized group activity without external triggering cues, and schedules of self‐organized collective activity can vary with environmental conditions. This plasticity can improve group members’ ability to meet their requirements in different environments. In colonial caterpillars, synchronized colony foraging schedules have been postulated to depend either on avoidance of visual predators or on temperature effects on ectotherm physiology. We examine the foraging schedule of forest tent caterpillars (Malacosoma disstria) under different constant conditions to distinguish between these hypotheses. Plasticity in the foraging schedule was tested by keeping colonies under different constant regimes of light and temperature. Digital video and tracking software were used to record the colony's alternation between quiescent and active bouts. The duration and frequency of bouts was compared between treatments. The schedule of synchronized colony activity was not affected by lighting, but it accelerated at higher temperature, because of a decrease in the duration of both active and quiescent bouts. Forest tent caterpillars’ foraging schedule thus depends on the time required to accomplish the tasks of food finding (active bouts) and food processing (quiescent bouts). As caterpillars are ectotherms, locomotion and digestion rates increase at higher temperature and both tasks are accomplished faster. The forest tent caterpillar and the congeneric eastern tent caterpillar (M. americanum) both exhibit self‐organized synchronized collective foraging, but environmental modulation of foraging schedule differs between these species, according to differences in social organization and thermal ecology. Eastern tent caterpillars maintain a fixed foraging schedule under varying temperatures and use the tent to maintain high metabolic rates. In the forest tent caterpillar, flexibility of the foraging schedule in accordance with changes in metabolism lessens the constraints imposed by collective foraging. Synchronous foraging, where entire social groups travel together to and from feeding sites, is thought to have several fitness advantages including improved food finding, recruitment to profitable food sources, anti‐predator defense and group thermoregulation between foraging expeditions.     

Spread and change in stress resistance of Shiga toxin-producing Escherichia coli?O157 on fungal colonies

To elucidate the effect of fungal hyphae on the behaviour of Shiga toxin-producing Escherichia coli (STEC) O157, the spread and change in stress resistance of the bacterium were evaluated after coculture with 11 species of food-related fungi including fermentation starters. Spread distances of STEC O157 varied depending on the co-cultured fungal species, and the motile bacterial strain spread for longer distances than the non-motile strain. The population of STEC O157 increased when co-cultured on colonies of nine fungal species but decreased on colonies of Emericella nidulans and Aspergillus ochraceus. Confocal scanning microscopy visualization of green fluorescent protein-tagged STEC O157 on fungal hyphae revealed that the bacterium colonized in the water film that existed on and between hyphae. To investigate the physiological changes in STEC O157 caused by co-culturing with fungi, the bacterium was harvested after 7 days of co-culturing and tested for acid resistance. After co-culture with eight fungal species, STEC O157 showed greater acid resistance compared to those cultured without fungi. Our results indicate that fungal hyphae can spread the contamination of STEC O157 and can also enhance the stress resistance of the bacteria.     

Colony‐level behavioural variation correlates with differences in expression of the foraging gene in red imported fire ants

Among social insects, colony‐level variation is likely to be widespread and has significant ecological consequences. Very few studies, however, have documented how genetic factors relate to behaviour at the colony level. Differences in expression of the foraging gene have been associated with differences in foraging and activity of a wide variety of organisms. We quantified expression of the red imported fire ant foraging gene (sifor) in workers from 21 colonies collected across the natural range of Texas fire ant populations, but maintained under standardized, environmentally controlled conditions. Colonies varied significantly in their behaviour. The most active colonies had up to 10 times more active foragers than the least active colony and more than 16 times as many workers outside the nest. Expression differences among colonies correlated with this colony‐level behavioural variation. Colonies with higher sifor expression in foragers had, on average, significantly higher foraging activity, exploratory activity and recruitment to nectar than colonies with lower expression. Expression of sifor was also strongly correlated with worker task (foraging vs. working in the interior of the nest). These results provide insight into the genetic and physiological processes underlying collective differences in social behaviour. Quantifying variation in expression of the foraging gene may provide an important tool for understanding and predicting the ecological consequences of colony‐level behavioural variation.     

The farming ant Sericomyrmex amabilis nutritionally manages its fungal symbiont and its social parasite

1. When parasites exploit mutualisms involving food exchange, they can destabilise the partnership with costs to interacting partners. For instance, the ant Sericomyrmex amabilis farms fungal symbionts to produce food, but, in so doing, attracts parasitic Megalomyrmex symmetochus guest ants that infiltrate fungus‐farming ant societies and live with their hosts their entire lives. 2. The present study examined whether host foraging in parasitised colonies shifts towards nutritional requirements of the parasitic guest ants as inferred from the parasite's elemental content (%C, %N, and C:N). 3. Laboratory feeding experiments with nutritionally defined diets indicated that S. amabilis ants harvest protein‐biased substrate, and more total substrate when hosting M. symmetochus relative to when provisioning their fungus gardens and nestmates. 4. Field surveys further showed that parasitised colonies incur reductions in fungus garden nutritional quality and quantity, brood mass, and host worker body condition. And yet these costs appear manageable across growing seasons, as parasitised fungal cultivars appear to provide sufficient nutrition for stable populations of host ants. 5. The approach developed here shows how behavioural strategies for nutrient regulation can extend beyond the needs of the individual to entire fungus‐farming systems, and implies that S. amabilis dynamically adjusts collective foraging strategies when parasitised to enhance long‐term symbiotic stability.     

Turbidity amplifies the non‐lethal effects of predation and affects the foraging success of characid fish shoals

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Cost of exposure to trematode cercariae and learned recognition and avoidance of parasitism risk by fathead minnows Pimephales promelas

Fathead minnows Pimephales promelas exposed to cercariae of the trematode Ornithodiplostomum sp. incurred a significant mass loss 17 days after exposure to 20 or 120 cercariae. Parasite‐naïve P. promelas showed no evidence of innate recognition or avoidance of cercariae. After a single exposure to cercariae, however, fish responded to chemical and visual cues of dead (thawed) cercariae with a reduction in activity. Encounter rate with cercariae, and hence infection rate, increased with fish activity. The data indicated that experienced P. promelas associated parasitism risk with novel chemical and visual cues that later triggered avoidance behaviour. Parallels and interactions between antiparasite behaviour and antipredator behaviour open new avenues for behavioural ecological research in risk‐sensitive decision‐making.     

Diving and foraging behaviour of Adélie penguins in areas with and without fast sea-ice

The diving and foraging behaviours of Adélie penguins, Pygoscelis adeliae, rearing chiks at Hukuro Cove, Lützow-Holm Bay, where the fast sea-ice remained throughout summer, were compared to those of penguins at Magnetic Island, Prydz Bay, where the fast sea-ice disappeared in early January. Parent penguins at Hukuro Cove made shallower (7.1–11.3 m) but longer (90–111 s) dives than those at Magnetic Island (22.9 m and 62 s). Dive duration correlated with dive depth at both colonies (r ² = 0.001 ∼ 0.90), but the penguins atg Hukuro Cove made longer dives for a given depth. Parents at Hukuro Cove made shorter foraging trips (8.1–14.4 h) with proportionally longer walking/swimming (diving < 1 m) travel time (27–40% of trip duration) and returned with smaller meals (253–293 g) than those at Magnetic Island, which foraged on average for 57.2 h, spent 2% of time walking/swimming ( < 1 m) travel, and with meals averaging 525 g. Trip duration at both colonies correlated to the total time spent diving. Trip duration at Hukuro Cove, but not at Magnetic Island, increased as walking/swimming ( < 1 m) travel time increased. These differences in foraging behaviour between colonies probably reflected differences in sea-ice cover and the availability of foraging sites. Received: 3 November 1995/Accepted: 29 May 1996     

Multiple predator-avoidance behaviours of the freshwater snail Physella heterostropha pomila: responses vary with risk

• 1 We examined the predator‐avoidance behaviour, exhibited in response to chemical cues, of two populations of the snail Physella heterostropha pomila. Snails were subjected to four treatments simulating different degrees of predation risk: control water (low risk), or water from tanks containing nonforaging crayfish (intermediate risk), crushed conspecifics (high risk) or crayfish consuming conspecifics (high risk). Data were analysed using three‐way ANOVA models (population × predator chemicals × injured conspecific chemicals).
• 2 Physella increased its avoidance behaviour as risk increased. Crayfish cue elicited a significantly greater response than from controls. Cues from injured conspecifics elicited the strongest response.
• 3 Physella exhibited several types of avoidance behaviour, including burial into the substratum, moving to the water surface, and crawling out of the water. The type of cue present influenced response type. Cues from crayfish reduced burial and increased movement to the water surface or out of the water. Cues from injured‐conspecifics significantly increased crawling completely out of the water.
• 4 The two populations differed in the type and degree of response exhibited. One population exhibited significantly greater ‘reactivity’ (i.e. any avoidance behaviour) in response to foraging crayfish, and more burial and crawl‐out behaviours were exhibited in high‐risk treatments.

     

Why Do Dolphins Form Mixed‐Species Associations in the Azores?

Mixed‐species associations are temporary associations between individuals of different species that are often observed in birds, primates and cetaceans. They have been interpreted as a strategy to reduce predation risk, enhance foraging success and/or provide a social advantage. In the archipelago of the Azores, four species of dolphins are commonly involved in mixed‐species associations: the common dolphin, Delphinus delphis, the bottlenose dolphin, Tursiops truncatus, the striped dolphin, Stenella coeruleoalba, and the spotted dolphin, Stenella frontalis. In order to understand the reasons why dolphins associate, we analysed field data collected since 1999 by research scientists and trained observers placed onboard fishing vessels. In total, 113 mixed‐species groups were observed out of 5720 sightings. The temporal distribution, habitat (water depth, distance to the coast), behaviour (i.e. feeding, travelling, socializing), size and composition of mixed‐species groups were compared with those of single‐species groups. Results did not support the predation avoidance hypothesis and gave little support to the social advantage hypothesis. The foraging advantage hypothesis was the most convincing. However, the benefits of mixed‐species associations appeared to depend on the species. Associations were likely to be opportunistic in the larger bottlenose dolphin, while there seemed to be some evolutionary constraints favouring associations in the rarer striped dolphin. Comparison with previous studies suggests that the formation of mixed‐species groups depends on several environmental factors, and therefore may constitute an adaptive response.     

Predation ofApochthonius minimus (Pseudoscorpionida: Chthoniidae) onFolsomia canadida (Collembola: Isotomidae)

Summary We investigated the functional response of the predaceous pseudoscorpion,Apochthonius minimus, to density of the springtail,Folsomia candida, as well as the effects of temperature and prey size on handling time and attack rate. Temperature slightly altered the overall rise in response. Both the rise and shape of the response differed for two prey sizes. The changes in number of prey eaten over a 48-hour period were also examined, and the attack and feeding behaviour ofA. minimus was described and discussed in relation to the predation experiments. The pseudoscorpion preferred young adultF. candida, 0.8–1.2 mm in length, when offered prey in the range, 0.2–1.5 mm.     

Foraging strategy and predator avoidance behaviour: an intraspecific approach

Relationships between predator avoidance behaviour (scanning and flocking) and foraging were studied in Calidris alpina, to test predictions regarding the effect of foraging techniques on such behaviours. The scanning hypothesis predicts that individuals with a tactile hunting technique and individuals with a visual hunting technique (both continuous searchers) do not differ in any variable related to scanning behaviour. The flocking hypothesis predicts that visually hunting individuals witl tend to form smaller flocks than tactile-foraging individuals. The two continuous feeding strategies did not differ among individuals in vigilance rate, nor in vigilance time or mean scan duration. However, with respect to flocking behaviour, visual foragers differed from tactile foragers in foraging flock size. The relationships between flocking behaviour and foraging strategy are discussed. The pattern found at the intraspecific level are the same as those found at interspecific level.     

Foraging decisions of individual workers vary with colony size in the greenhead ant Rhytidoponera metallica (Formicidae, Ectatomminae)

Summary. The ability of worker ants to adapt their behaviour depending on the social environment of the colony is imperative for colony growth and survival. In this study we use the greenhead ant Rhytidoponera metallica to test for a relationship between colony size and foraging behaviour. We controlled for possible confounding ontogenetic and age effects by splitting large colonies into small and large colony fragments. Large and small colonies differed in worker number but not worker relatedness or worker/brood ratios. Differences in foraging activity were tested in the context of single foraging cycles with and without the opportunity to retrieve food. We found that workers from large colonies foraged for longer distances and spent more time outside the nest than foragers from small colonies. However, foragers from large and small colonies retrieved the first prey item they contacted, irrespective of prey size. Our results show that in R. metallica, foraging decisions made outside the nest by individual workers are related to the size of their colony.Received 23 March 2004; revised 3 June 2004; accepted 4 June 2004.     

Effects of life phase and schooling patterns on the foraging behaviour of coral‐reef fishes from the genus Haemulon

During this study (December 2009 to December 2010), underwater visual surveys using the focal animal method were performed in the coastal reefs of Tamandaré, north‐eastern Brazil. The aim was to analyse the effects of the life phase (juvenile and adult) and schooling patterns (school and solitary) on the feeding behaviour (foraging rates and substratum preferences) of four species of the genus Haemulon (Haemulon aurolineatum, Haemulon parra, Haemulon plumieri and Haemulon squamipinna). PERMANOVA analysis (P < 0·05) indicated that ontogenetic changes and schooling patterns directly influence foraging behaviour. Schooling individuals had low foraging rates (mean ± s.d . = 2·3 ± 2·1 bites 10 min^?1) and mobility, usually remaining near the bottom; however, solitary fishes had high foraging rates (mean ± s.d . = 12·5 ± 4·6 bites 10 min^?1). Juveniles preferred feeding in the water column (75% of the total number of bites), whereas adults foraged mainly in sand (80%) and bare rock (20%). All four Haemulon species displayed similar patterns of feeding behaviour as well as preferences for foraging sites and display competition for food resources. In contrast, little is known about their habitat use and foraging behaviour over the diel cycle, particularly the newly settled and early juvenile stages.