Who holds the reins? Context-dependent resource allocation in the mutualism between fig trees and their fig wasp pollinators.

Mutualisms are consumer-resource interactions, in which goods and services are exchanged. Biological market theory states that exchanges should be regulated by both partners. However, most studies on mutualisms are one-sided, focusing on the control exercised by host organisms on their symbionts. In the brood-site pollination mutualism between fig trees and their symbiont wasp pollinators, galled flowers are development sites for pollinator larvae and are exchanged for pollination services. We determined if pollinator galls influenced resource allocation to fig inflorescences called syconia and considered feedbacks from the host tree. We experimentally produced syconia containing only seeds (S), only pollinator galls (G) or seeds and galls (SG) with varying number of introduced female pollinator wasps, i.e., foundress wasps. Biomass allocation to syconia was affected by foundress numbers and treatment groups; SG treatments received highest biomass allocation at low foundress numbers, and both G and SG treatments at high foundress numbers. Seeds are important determinants of allocation at low foundress numbers; galls are likely more influential at high foundress numbers. Most allocation in the G and SG treatment was to the syconium wall, likely as protection from parasitoids and temperature/humidity fluctuations. Dry mass of individual seeds and wasps (except at low foundress numbers) was unchanged between treatment groups, indicating seeds and wasps regulate resource flow into them, with lower flow into galls containing the smaller males compared to females commensurate with sexual dimorphism. We demonstrate the importance of considering the direct role of symbionts in accessing resources and controlling exchanges within mutualisms.

Staying in the club: Exploring criteria governing metacommunity membership for obligate symbionts under host-symbiont feedback.

Metacommunity membership is influenced by habitat availability and trophic requirements. However, for multitrophic horizontally transmitted symbiont communities that are closely associated with hosts, symbiont-host interactions may affect membership criteria in novel ways. For example, failure of beneficial services from symbionts could influence the host, and in turn, the entire community. Understanding such host-symbiont feedback effects on symbiont community membership, symbiont community structure, and function is important for understanding if host-symbiont communities are fundamentally different from more traditional ecological communities. We investigate the membership criteria for a multitrophic insect symbiont community that colonizes host inflorescences at specific developmental stages termed colonization windows. The inflorescences serve as microcosm habitats. Symbionts exhibit a range of interactions from mutualism to parasitism. Hosts exhibit feedback by aborting inflorescences not pollinated by mutualistic symbionts. Habitats are consequently lost for all other symbiont species in such host-derived organs whose development is mutualist-dependent. Using empirical measurements to characterize inflorescence development, we simulate symbiont dispersal colonization across hosts. We vary host densities and lengths of symbiont colonization windows, and track the persistence of each symbiont species in the metacommunity based on its trophic requirements and resource availability within the microcosm. Since the persistence of the microcosm habitat is dictated by pollination performed by the mutualist, the mutualist fared better than all other symbionts. The length of symbiont colonization windows was positively related with colonization success and symbiont persistence. The cumulative length of the colonization windows of prey dictated predator success; diet breadth or prey colonization success did not influence predator persistence. Predators also had a greater host-plant density requirement than prey for persistence in the community. These results offer valuable insights into host densities required for maintaining symbionts, and have implications for multitrophic symbiont community stability. Special constraints can govern symbiont community membership, function and structure and symbiont persistence when host-symbiont feedback impacts host microcosm development.

Hopping on: Conspecific traveller density within a vehicle regulates parasitic hitchhiking between ephemeral microcosms.

Hitchhikers (phoretic organisms) identify their vehicles using species-specific visual, chemical and vibrational cues. However, what factors influence their choice between vehicles of the same species has rarely been investigated. Hitchhikers must not only avoid overcrowded vehicles but may also need to travel with conspecifics to ensure mates at their destination. Hence, a trade-off between overcrowding and presence of conspecifics likely determines the choice of a vehicle especially when destination sites are distant, ephemeral and unique. Here, we investigate whether a trade-off between the presence of conspecifics versus overcrowding by conspecifics or heterospecifics on a vehicle affects hitchhiker choice. We also investigate the sensory modality responsible for this choice. We experimentally examine these questions using a phoretic nematode community (containing plant- and animal-parasitic taxa) obligately associated with a brood-site pollination mutualism. In this model system, nematodes co-travel with conspecifics and heterospecifics on pollinators as vehicles, between ephemeral plant brood sites to complete their developmental life cycle. In this system, hitchhiker overcrowding has proven negative impacts on vehicle and plant fitness. We expected nematodes to respond to conspecifics and heterospecific density on offered vehicles when making their choice. We found that animal-parasitic nematodes preferred vehicles containing some conspecifics within a certain density range. However, plant-parasitic nematodes preferentially boarded vehicles that were devoid of conspecifics or had few conspecifics. Plant parasites that preferred empty vehicles likely hitchhiked in pairs. Both nematode types employed volatile cues to discriminate between vehicles with different conspecific nematode densities. Our results suggest that vehicle overcrowding by conspecifics, most likely, guaranteed access to mates at the destination determined hitchhiker choice. Surprisingly, and contrary to our expectations, plant- and animal-parasitic nematodes did not respond to heterospecific crowding on vehicles and did not discriminate between vehicles with different heterospecific nematode densities. The reason for this lack of response to heterospecific presence is unknown. This study not only shows that phoretic organisms use different strategies while choosing a vehicle but also confirms that density-dependent effects can ensure the stability and persistence of phoretic interactions in a mutualism by balancing overcrowding against reproductive assurance.

The Scent of Life: Phoretic Nematodes Use Wasp Volatiles and Carbon Dioxide to Choose Functional Vehicles for Dispersal.

Hitchhikers (phoretic organisms) need vehicles to disperse out of unsuitable habitats. Therefore, finding vehicles with the right functional attributes is essential for phoretic organisms. To locate these vehicles, phoretic organisms employ cues within modalities, ranging from visual to chemical senses. However, how hitchhikers discriminate between individual vehicles has rarely been investigated. Using a phoretic nematode community associated with an obligate fig-fig wasp pollination mutualism, we had earlier established that hitchhiking nematodes make decisions based on vehicle species identity and number of conspecific hitchhikers already present on the vehicle. Here we investigate if hitchhikers can differentiate between physiological states of vehicles. We asked whether phoretic nematodes choose between live or dead vehicles present in a chemically crowded environment and we investigated the basis for any discrimination. We conducted two-choice and single-choice behavioral assays using single nematodes and found that plant- and animal-parasitic nematodes preferred live over dead vehicles and used volatiles as a sensory cue to make this decision. However, in single-choice assays, animal-parasitic nematodes were also attracted towards naturally dead or freeze-killed wasps. The volatile profile of the wasps was dominated by terpenes and spiroketals. We examined the volatile blend emitted by the different wasp physiological states and determined a set of volatiles that the phoretic nematodes might use to discriminate between these states which is likely coupled with respired CO2. We determined that CO2 levels emitted by single wasps are sufficient to attract nematodes, demonstrating the high sensitivity of nematodes to this metabolic product.

Dynamic environments of fungus-farming termite mounds exert growth-modulating effects on fungal crop parasites.

This study investigated for the first time the impact of the internal mound environment of fungus-growing termites on the growth of fungal crop parasites. Mounds of the termite Odontotermes obesus acted as (i) temperature and relative humidity (RH) 'stabilisers' showing dampened daily variation and (ii) 'extreme environments' exhibiting elevated RH and CO2 levels, compared to the outside. Yet, internal temperatures exhibited seasonal dynamics as did daily and seasonal CO2 levels. During in situ experiments under termite-excluded conditions within the mound, the growth of the crop parasite Pseudoxylaria was greater inside than outside the mound, i.e., Pseudoxylaria is 'termitariophilic'. Also, ex situ experiments on parasite isolates differing in growth rates and examined under controlled conditions in the absence of termites revealed a variable effect with fungal growth decreasing only under high CO2 and low temperature conditions, reflecting the in situ parasite growth fluctuations. In essence, the parasite appears to be adapted to survive in the termite mound. Thus the mound microclimate does not inhibit the parasite but the dynamic environmental conditions of the mound affect its growth to varying extents. These results shed light on the impact of animal-engineered structures on parasite ecology, independent of any direct role of animal engineers.

Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco-evolutionary implications.

Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. We assessed the phenotypic integration of CCDs in a meta-analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules. Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs. We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals.

Resource dispersion influences dispersal evolution of highly insulated insect communities.

Communities in which species are obligately associated with a single host are ideal to test adaptive responses of community traits to host-imposed selection because such communities are often highly insulated. Fig species provide oviposition resources to co-evolved fig-wasp communities. Dispersing fig-wasp communities move from one host plant to another for oviposition. We compared the spatial dispersion of two fig species and the dispersal capacities of their multitrophic wasp communities. Dispersal capacities were assessed by measuring vital dispersal correlates, namely tethered flight durations, somatic lipid contents and resting metabolic rates. We suggest that dispersal-trait distributions of congeneric wasp species across the communities are an adaptive response to host plant dispersion. Larger dispersal capacities of the entire multitrophic community are related to more widely dispersed resources. Our results provide evidence and a novel perspective for understanding the potential role of adaptation in whole-community dispersal-trait distributions.

History Matters: Oviposition Resource Acceptance in an Exploiter of a Nursery Pollination Mutualism.

In the fig-fig wasp nursery pollination system, parasitic wasps, such as gallers and parasitoids that oviposit from the exterior into the fig syconium (globular, enclosed inflorescence) are expected to use a variety of chemical cues for successful location of their hidden hosts. Behavioral assays were performed with freshly eclosed naive galler wasps. Syconia with different oviposition histories, i.e. with or without prior oviposition, were presented to wasps in no-choice assays and the time taken to the first oviposition attempt was recorded. The wasps exhibited a preference for syconia previously exposed to conspecifics for oviposition over unexposed syconia. Additionally, syconia exposed to oviposition by heterospecific wasps were also preferred for oviposition over unexposed syconia indicating that wasps recognise and respond to interspecific cues. Wasps also aggregated for oviposition on syconia previously exposed to oviposition by conspecifics. We investigated chemical cues that wasps may employ in accepting an oviposition resource by analyzing syconial volatile profiles, chemical footprints left by wasps on syconia, and syconial surface hydrocarbons. The volatile profile of a syconium is influenced by the identity of wasps developing within and may be used to identify suitable host syconia at long range whereas close range preference seems to exploit wasp footprints that alter syconium surface hydrocarbon profiles. These cues act as indicators of the oviposition history of the syconium, thereby helping wasps in their oviposition decisions.

Dark Matters: Challenges of Nocturnal Communication Between Plants and Animals in Delivery of Pollination Services.

The night is a special niche characterized by dim light, lower temperatures, and higher humidity compared to the day. Several animals have made the transition from the day into the night and have acquired unique adaptations to cope with the challenges of performing nocturnal activities. Several plant species have opted to bloom at night, possibly as a response to aridity to prevent excessive water loss through evapotranspiration since flowering is often a water-demanding process, or to protect pollen from heat stress. Nocturnal pollinators have visual adaptations to function under dim light conditions but may also trade off vision against olfaction when they are dependent on nectar-rewarding and scented flowers. Nocturnal pollinators may use CO2 and humidity cues emanating from freshly-opened flowers as indicators of nectar-rich resources. Some endothermic nocturnal insect pollinators are attracted to thermogenic flowers within which they remain to obtain heat as a reward to increase their energy budget. This review focuses on mechanisms that pollinators use to find flowers at night, and the signals that nocturnally blooming flowers may employ to attract pollinators under dim light conditions. It also indicates gaps in our knowledge. While millions of years of evolutionary time have given pollinators and plants solutions to the delivery of pollination services and to the offering of appropriate rewards, this history of successful evolution is being threatened by artificial light at night. Excessive and inappropriate illumination associated with anthropogenic activities has resulted in significant light pollution which serves to undermine life processes governed by dim light.

The insect ovipositor as a volatile sensor within a closed microcosm.

We show that the insect ovipositor is an olfactory organ that responds to volatiles and CO2 in gaseous form. We demonstrate this phenomenon in parasitic wasps associated with Ficus racemosa where ovipositors, as slender as a human hair, drill through the syconium (enclosed inflorescences) and act as a guiding probe to locate highly specific egg-laying sites hidden inside. We hypothesize that olfaction will occur in the ovipositors of insects such as parasitic fig wasps where the hosts are concealed and volatile concentrations can build up locally. Relevant stimuli such as herbivore-induced fig volatiles and CO2 elicited electrophysiological responses from the ovipositors. Silver nitrate staining also revealed pores in ovipositor sensilla, indicating their olfactory nature. Insects could use volatile sensors on their ovipositors to evaluate ecologically relevant stimuli for oviposition. Further investigations on the sensory nature of ovipositors can provide designs for development of ovipositor-inspired micro-chemosensors.

Fungus-Farming Termites Selectively Bury Weedy Fungi that Smell Different from Crop Fungi.

Mutualistic associations such as the fungal farms of insects are prone to parasitism and are consequently vulnerable to attack by weeds and pests. Therefore, efficient farm management requires quick detection of weeds for their elimination. Furthermore, if the available weedicides are non-specific, then the ability of insects to discriminate between crop and weeds becomes essential for targeted application of such compounds. Here, we demonstrate for the first time in fungus-farming insects, that worker castes of the fungus-growing termite Odontotermes obesus discriminate between their crop (Termitomyces) and the weedy (Pseudoxylaria) fungi, even if exposed to only fungal scents. Termites respond to the presence of fungal mycelium or scent alone, by burying the weed with the offered material such as soil or agar, possibly anointing the weed with chemicals in the process. The scent profiles of crop and weedy fungi are distinct and the differences are likely exploited by termites to selectively mount their defences. Sesquiterpene compounds such as aristolene and viridiflorol, which are absent from crop odours, may constitute the "weedy scent". Our results provide a general mechanism of how other fungus-farming insects could avoid indiscriminate application of non-specific fungicides which could lead to poisoning their crops, and have bearing on the stability of the mutualism between termites and their crop fungus in the face of parasitism by weedy fungi.

Plant reproductive traits mediate tritrophic feedback effects within an obligate brood-site pollination mutualism.

Plants, herbivores and parasitoids affect each other directly and indirectly; however, feedback effects mediated by host plant traits have rarely been demonstrated in these tritrophic interactions. Brood-site pollination mutualisms (e.g. those involving figs and fig wasps) represent specialised tritrophic communities where the progeny of mutualistic pollinators and of non-mutualistic gallers (both herbivores) together with that of their parasitoids develop within enclosed inflorescences called syconia (hence termed brood-sites or microcosms). Plant reproductive phenology (which affects temporal brood-site availability) and inflorescence size (representing brood-site size) are plant traits that could affect reproductive resources, and hence relationships between trees, pollinators and non-pollinating wasps. Analysing wasp and seed contents of syconia, we examined direct, indirect, trophic and non-trophic relationships within the interaction web of the fig-fig wasp community of Ficus racemosa in the context of brood site size and availability. We demonstrate that in addition to direct resource competition and predator-prey (host-parasitoid) interactions, these communities display exploitative or apparent competition and trait-mediated indirect interactions. Inflorescence size and plant reproductive phenology impacted plant-herbivore and plant-parasitoid associations. These plant traits also influenced herbivore-herbivore and herbivore-parasitoid relationships via indirect effects. Most importantly, we found a reciprocal effect between within-tree reproductive asynchrony and fig wasp progeny abundances per syconium that drives a positive feedback cycle within the system. The impact of a multitrophic feedback cycle within a community built around a mutualistic core highlights the need for a holistic view of plant-herbivore-parasitoid interactions in the community ecology of mutualisms.

Solastalgia, our deteriorating environment, and Spirit of Place.

Climate anxiety is as newly recognised a phenomenon as is the neologism solastalgia. The word solastalgia was coined by the Australian environmental philosopher Glenn Albrecht; it is a composite of the concepts of solace and desolation, and the pain ('algia') derived from the immediate loss of or assault to one's place of residence (Albrecht 2005). It is different from nostalgia, which is the remembrance of times past, and it specifically refers to the mental distress caused by climate change of anthropogenic origin (Albrecht et al. 2007): ''Solastalgia, as opposed to atavistic nostalgia, can also be future orientated, as those who suffer from it might actively seek to create new things or engage in collective action that provides solace and communion in any given environment. Solastalgia has no necessary connection to the past, it may seek its alleviation in a future that has to be designed and created'' (Albrecht 2005).

Diel variation in fig volatiles across syconium development: making sense of scents.

Plants produce volatile organic compounds (VOCs) in a variety of contexts that include response to abiotic and biotic stresses, attraction of pollinators and parasitoids, and repulsion of herbivores. Some of these VOCs may also exhibit diel variation in emission. In Ficus racemosa, we examined variation in VOCs released by fig syconia throughout syconium development and between day and night. Syconia are globular enclosed inflorescences that serve as developing nurseries for pollinating and parasitic fig wasps. Syconia are attacked by gallers early in their development, serviced by pollinators in mid phase, and are attractive to parasitoids in response to the development of gallers at later stages. VOC bouquets of the different development phases of the syconium were distinctive, as were their day and night VOC profiles. VOCs such as α-muurolene were characteristic of the pollen-receptive diurnal phase, and may serve to attract the diurnally-active pollinating wasps. Diel patterns of release of volatiles could not be correlated with their predicted volatility as determined by Henry's law constants at ambient temperatures. Therefore, factors other than Henry's law constant such as stomatal conductance or VOC synthesis must explain diel variation in VOC emission. A novel use of weighted gene co-expression network analysis (WGCNA) on the volatilome resulted in seven distinct modules of co-emitted VOCs that could be interpreted on the basis of syconium ecology. Some modules were characterized by the response of fig syconia to early galling by parasitic wasps and consisted largely of green leaf volatiles (GLVs). Other modules, that could be characterized by a combination of syconia response to oviposition and tissue feeding by larvae of herbivorous galler pollinators as well as of parasitized wasps, consisted largely of putative herbivore-induced plant volatiles (HIPVs). We demonstrated the usefulness of WGCNA analysis of the volatilome in making sense of the scents produced by the syconia at different stages and diel phases of their development.

Understanding the chemical language of the natural pharmacopeia: Whose hallucinogen is it anyway?

Humans communicate aggression through words, gestures, guns, bombs, and missiles. Guns, bombs, and missiles are left out of expressions of affection, unless they are meant to impress a loved one or affirm a beloved ideology. Many organisms other than humans use gestures although they may not have words, and the vast majority of organisms also use the language of chemistry in offence and defence.

A Braver New World? Of chatbots and other cognoscenti.

The 1920s mark the rise of robots in the human lexicon. Karel Capek, a Czech playwright, wrote R. U. R., which stands for Rossumovi Univerzalni Roboti or Rossum's Universal Robots. The word for worker or labourer in Czech is robota; Karel was given the idea for this word by his artist brother Josef, and the word robot for a humanmanufactured humanoid entity was born in 1920. November 30, 2022, just over a century later, was when ChatGPT (Chat Generative Pre-trained Transformer), a chat robot, chatter bot or advanced chatbot, was made available by the company OpenAI for free download.

Composition of extrafloral nectar influences interactions between the myrmecophyte Humboldtia brunonis and its ant associates.

Ant-plant interactions often are mediated by extrafloral nectar (EFN) composition that may influence plant visitation by ants. Over a 300 km range in the Indian Western Ghats, we investigated the correlation between the EFN composition of the myrmecophytic ant-plant Humboldtia brunonis (Fabaceae) and the number and species of ants visiting EFN. EFN composition varied among H. brunonis populations and between plant organs (floral bud vs. young leaf EFN). In general, EFN was rich in sugars with small quantities of amino acids, especially essential amino acids, and had moderate invertase activity. In experiments at the study sites with sugar and amino acid solutions and with leaf or floral bud EFN mimics, dominant EFN-feeding ants differentiated between solutions as well as between mimics. The castration parasite Crematogaster dohrni (northern study site) was the least selective and did not exhibit any clear feeding preferences, while the largely trophobiont-tending non-protective Myrmicaria brunnea (middle study site) preferred higher sucrose concentrations and certain essential/non-essential amino acid mixtures. The mutualistic Technomyrmex albipes (southern study site) preferred sucrose over glucose or fructose solutions and consumed the leaf EFN mimic to a greater extent than the floral bud EFN mimic. This young leaf EFN mimic had low sugar concentrations, the lowest viscosity and sugar:amino acid ratio, was rich in essential amino acids, and appeared ideally suited to the digestive physiology of T. albipes. This preference for young leaf EFN may explain the greater protection afforded to young leaves than to floral buds by T. albipes, and may also help to resolve ant-pollinator conflicts. The differential response of dominant ants to sugar, amino acids, or solution viscosity suggests that plants can fine-tune their interactions with local ants via EFN composition. Thus, EFN can mediate local partner-choice mechanisms in ant-plant interactions.

Editorial : Reproducibility and replicability in science: A Sisyphean task.

The world received a confidence booster in the power of the scientific method, having witnessed and participated in the recent development of successful vaccines against SARS-COV-2. The world also got a peek into scientific controversies, the clamour for more transparency and data sharing, besides the requirement for rigorous testing, adequate sample sizes, false positives, false negatives, risk probabilities, and population variation. For an interested lay person, or even for a practising scientist, this was the equivalent of a crash course on the world stage on how science is done, warts and all, but where science triumphed in the end....

Moisture alone is sufficient to impart strength but not weathering resistance to termite mound soil.

Soil is used for the construction of structures by many animals, at times admixed with endogenous secretions. These additives, along with soil components, are suggested to have a role in biocementation. However, the relative contribution of endogenous and exogenous materials to soil strength has not been adequately established. Termite mounds are earthen structures with exceptional strength and durability including weathering resistance to wind and rain. With in situ and laboratory-based experiments, we demonstrate that the fungus-farming termite Odontotermes obesus which builds soil nest mounds, when given a choice, prefers soil close to its liquid limit for construction. At this moisture content, the soil-water mixture alone even in the absence of termite handling undergoes self-weight consolidation and upon drying attains a monolithic, densely packed structure with compressive strength comparable to the in situ strength of the mound soil; however, the soil-water mixture alone has lower resistance to water erosion than the in situ mound samples, suggesting that termite secretions impart weathering resistance and thereby long-term stability to the mound. Therefore, weathering resistance and compressive strength are conferred by different aspects of termite soil manipulation. Our work provides novel insights into termite mound construction and strength correlates for earthen structures built by animals.

Bi-layered architecture facilitates high strength and ventilation in nest mounds of fungus-farming termites.

Mass-energy transfer across the boundaries of living systems is crucial for the maintenance of homeostasis; however, it is scarcely known how structural strength and integrity is maintained in extended phenotypes while also achieving optimum heat-mass exchange. Here we present data on strength, stability, porosity and permeability of termite mounds of a fungus-farming species, Odontotermes obesus. We demonstrate that the termite mound is a bi-layered structure with a dense, strong core and a porous shell that is constantly remodelled. Its safety factor is extraordinarily high and is orders of magnitude higher than those of human constructions. The porous peripheries are analogous to the mulch layer used in agriculture and help in moisture retention crucial for the survival of fungus gardens, while also allowing adequate wind-induced ventilation of the mounds. We suggest that the architectural solutions offered by these termites have wider implications for natural and industrial building technologies.