Brood Parasites That Care: Alternative Nesting Tactics in a Subsocial Wasp.

AbstractHosts and brood parasites are a classic example of conflict. Parasites typically provide no offspring care after laying eggs, imposing costs on hosts. Female subsocial wasps (Ammophila pubescens) alternate between initiating their own nests and using an "intruder" tactic of replacing eggs in nests of unrelated conspecifics. Hosts can respond by substituting new eggs of their own, with up to eight reciprocal replacements. Remarkably, intruders usually provision offspring in host nests, often alongside hosts. We used field data to investigate why intruders provision and to understand the basis of interactions. We found that intruders could not increase their fitness payoffs by using the typical brood parasite tactic of not provisioning offspring. Intruders using the typical tactic would benefit when hosts provisioned in their stead, but their offspring would starve when hosts failed to provision. Although some hosts obtained positive payoffs when intruders mistakenly provisioned their offspring, on average utilizing a conspecific nest represents parasitism: hosts pay costs while intruders benefit. Hosts and intruders used the same tactic of egg replacement, but intruders more often laid the final egg. Selection should favor better discrimination of offspring, which could lead to repeated cycles of costly egg replacement.

Crozier's Effect and the Acceptance of Intraspecific Brood Parasites.

Organisms can often benefit by distinguishing between different classes of individuals. An example is kin recognition, whereby individuals preferentially associate with or aid genetic relatives that bear matching recognition cues but reject others. Despite its potential benefits, however, kin recognition using genetically based cues is often weak or absent [1-4]. A general explanation, termed "Crozier's effect," is that when individuals interact randomly, rarer cue alleles less often match cues of other individuals, and so are involved predominantly in "reject"-type interactions. If such interactions are more costly, positive frequency-dependent selection will erode the cue diversity upon which discrimination depends [4, 5]. Although widely cited [1, 2, 4, 6-9], this idea lacks rigorous testing in the field. Here, we show how Crozier's effect applies to interactions between hosts and conspecific parasites, and measure it using field data. In the wasp we studied, conspecific parasitism fits a key assumption of Crozier's model: the same females act as both hosts and parasites. By exchanging offspring between nests experimentally, we find no evidence that females respond to genetically based cues associated with foreign offspring. Through measuring costs and benefits, however, we demonstrate a strong Crozier effect: because more parental investment is wasted when foreign offspring are rejected, interactions involving rejection have substantially lower payoffs than interactions involving acceptance. Costly rejection can thus eliminate cue diversity by causing selection against rare cue alleles, consistent with the absence of genetically based recognition that we observe. Females instead appear to rely on non-genetic cues that enable them to detect less than half of parasitic offspring.

Simplifying understory complexity in oil palm plantations is associated with a reduction in the density of a cleptoparasitic spider, Argyrodes miniaceus (Araneae: Theridiidae), in host (Araneae: Nephilinae) webs.

Expansion of oil palm agriculture is currently one of the main drivers of habitat modification in Southeast Asia. Habitat modification can have significant effects on biodiversity, ecosystem function, and interactions between species by altering species abundances or the available resources in an ecosystem. Increasing complexity within modified habitats has the potential to maintain biodiversity and preserve species interactions. We investigated trophic interactions between Argyrodes miniaceus, a cleptoparasitic spider, and its Nephila spp. spider hosts in mature oil palm plantations in Sumatra, Indonesia. A. miniaceus co-occupy the webs of Nephila spp. females and survive by stealing prey items caught in the web. We examined the effects of experimentally manipulated understory vegetation complexity on the density and abundance of A. miniaceus in Nephila spp. webs. Experimental understory treatments included enhanced complexity, standard complexity, and reduced complexity understory vegetation, which had been established as part of the ongoing Biodiversity and Ecosystem Function in Tropical Agriculture (BEFTA) Project. A. miniaceus density ranged from 14.4 to 31.4 spiders per square meter of web, with significantly lower densities found in reduced vegetation complexity treatments compared with both enhanced and standard treatment plots. A. miniaceus abundance per plot was also significantly lower in reduced complexity than in standard and enhanced complexity plots. Synthesis and applications: Maintenance of understory vegetation complexity contributes to the preservation of spider host-cleptoparasite relationships in oil palm plantations. Understory structural complexity in these simplified agroecosystems therefore helps to support abundant spider populations, a functionally important taxon in agricultural landscapes. In addition, management for more structurally complex agricultural habitats can support more complex trophic interactions in tropical agroecosystems.

Ant mosaics in Bornean primary rain forest high canopy depend on spatial scale, time of day, and sampling method.

BACKGROUND: Competitive interactions in biological communities can be thought of as giving rise to "assembly rules" that dictate the species that are able to co-exist. Ant communities in tropical canopies often display a particular pattern, an "ant mosaic", in which competition between dominant ant species results in a patchwork of mutually exclusive territories. Although ant mosaics have been well-documented in plantation landscapes, their presence in pristine tropical forests remained contentious until recently. Here we assess presence of ant mosaics in a hitherto under-investigated forest stratum, the emergent trees of the high canopy in primary tropical rain forest, and explore how the strength of any ant mosaics is affected by spatial scale, time of day, and sampling method. METHODS: To test whether these factors might impact the detection of ant mosaics in pristine habitats, we sampled ant communities from emergent trees, which rise above the highest canopy layers in lowland dipterocarp rain forests in North Borneo (38.8-60.2 m), using both baiting and insecticide fogging. Critically, we restricted sampling to only the canopy of each focal tree. For baiting, we carried out sampling during both the day and the night. We used null models of species co-occurrence to assess patterns of segregation at within-tree and between-tree scales. RESULTS: The numerically dominant ant species on the emergent trees sampled formed a diverse community, with differences in the identity of dominant species between times of day and sampling methods. Between trees, we found patterns of ant species segregation consistent with the existence of ant mosaics using both methods. Within trees, fogged ants were segregated, while baited ants were segregated only at night. DISCUSSION: We conclude that ant mosaics are present within the emergent trees of the high canopy of tropical rain forest in Malaysian Borneo, and that sampling technique, spatial scale, and time of day interact to determine observed patterns of segregation. Restricting sampling to only emergent trees reveals segregatory patterns not observed in ground-based studies, confirming previous observations of stronger segregation with increasing height in the canopy.

The effects of catchment and riparian forest quality on stream environmental conditions across a tropical rainforest and oil palm landscape in Malaysian Borneo.

Freshwaters provide valuable habitat and important ecosystem services but are threatened worldwide by habitat loss and degradation. In Southeast Asia, rainforest streams are particularly threatened by logging and conversion to oil palm, but we lack information on the impacts of this on freshwater environmental conditions, and the relative importance of catchment versus riparian-scale disturbance. We studied 16 streams in Sabah, Borneo, including old-growth forest, logged forest, and oil palm sites. We assessed forest quality in riparian zones and across the whole catchment and compared it with stream environmental conditions including water quality, structural complexity, and organic inputs. We found that streams with the highest riparian forest quality were nearly 4 °C cooler, over 20 cm deeper, had over 40% less sand, greater canopy cover, more stored leaf litter, and wider channels than oil palm streams with the lowest riparian forest quality. Other variables were significantly related to catchment-scale forest quality, with streams in the highest quality forest catchments having 40% more bedrock and 20 times more dead wood, along with higher phosphorus, and lower nitrate-N levels compared to streams with the lowest catchment-scale forest quality. Although riparian buffer strips went some way to protecting waterways, they did not maintain fully forest-like stream conditions. In addition, logged forest streams still showed signs of disturbance 10-15 years after selective logging. Our results suggest that maintenance and restoration of buffer strips can help to protect healthy freshwater ecosystems but logging practices and catchment-scale forest management also need to be considered.

The effects of forest conversion to oil palm on ground-foraging ant communities depend on beta diversity and sampling grain.

Beta diversity - the variation in species composition among spatially discrete communities - and sampling grain - the size of samples being compared - may alter our perspectives of diversity within and between landscapes before and after agricultural conversion. Such assumptions are usually based on point comparisons, which do not accurately capture actual differences in total diversity. Beta diversity is often not rigorously examined. We investigated the beta diversity of ground-foraging ant communities in fragmented oil palm and forest landscapes in Sabah, Malaysia, using diversity metrics transformed from Hill number equivalents to remove dependences on alpha diversity. We compared the beta diversities of oil palm and forest, across three hierarchically nested sampling grains. We found that oil palm and forest communities had a greater percentage of total shared species when larger samples were compared. Across all grains and disregarding relative abundances, there was higher beta diversity of all species among forest communities. However, there were higher beta diversities of common and very abundant (dominant) species in oil palm as compared to forests. Differences in beta diversities between oil palm and forest were greatest at the largest sampling grain. Larger sampling grains in oil palm may generate bigger species pools, increasing the probability of shared species with forest samples. Greater beta diversity of all species in forest may be attributed to rare species. Oil palm communities may be more heterogeneous in common and dominant species because of variable community assembly events. Rare and also common species are better captured at larger grains, boosting differences in beta diversity between larger samples of forest and oil palm communities. Although agricultural landscapes support a lower total diversity than natural forests, diversity especially of abundant species is still important for maintaining ecosystem stability. Diversity in agricultural landscapes may be greater than expected when beta diversity is accounted for at large spatial scales.

Retaining biodiversity in intensive farmland: epiphyte removal in oil palm plantations does not affect yield.

The expansion of agriculture into tropical forest frontiers is one of the primary drivers of the global extinction crisis, resulting in calls to intensify tropical agriculture to reduce demand for more forest land and thus spare land for nature. Intensification is likely to reduce habitat complexity, with profound consequences for biodiversity within agricultural landscapes. Understanding which features of habitat complexity are essential for maintaining biodiversity and associated ecosystem services within agricultural landscapes without compromising productivity is therefore key to limiting the environmental damage associated with producing food intensively. Here, we focus on oil palm, a rapidly expanding crop in the tropics and subject to frequent calls for increased intensification. One promoted strategy is to remove epiphytes that cover the trunks of oil palms, and we ask whether this treatment affects either biodiversity or yield. We experimentally tested this by removing epiphytes from four-hectare plots and seeing if the biodiversity and production of fruit bunches 2 months and 16 months later differed from equivalent control plots where epiphytes were left uncut. We found a species-rich and taxonomically diverse epiphyte community of 58 species from 31 families. Epiphyte removal did not affect the production of fresh fruit bunches, or the species richness and community composition of birds and ants, although the impact on other components of biodiversity remains unknown. We conclude that as they do not adversely affect palm oil production, the diverse epiphyte flora should be left uncut. Our results underscore the importance of experimentally determining the effects of habitat complexity on yield before introducing intensive methods with no discernible benefits.

An ant-plant by-product mutualism is robust to selective logging of rain forest and conversion to oil palm plantation.

Anthropogenic disturbance and the spread of non-native species disrupt natural communities, but also create novel interactions between species. By-product mutualisms, in which benefits accrue as side effects of partner behaviour or morphology, are often non-specific and hence may persist in novel ecosystems. We tested this hypothesis for a two-way by-product mutualism between epiphytic ferns and their ant inhabitants in the Bornean rain forest, in which ants gain housing in root-masses while ferns gain protection from herbivores. Specifically, we assessed how the specificity (overlap between fern and ground-dwelling ants) and the benefits of this interaction are altered by selective logging and conversion to an oil palm plantation habitat. We found that despite the high turnover of ant species, ant protection against herbivores persisted in modified habitats. However, in ferns growing in the oil palm plantation, ant occupancy, abundance and species richness declined, potentially due to the harsher microclimate. The specificity of the fern-ant interactions was also lower in the oil palm plantation habitat than in the forest habitats. We found no correlations between colony size and fern size in modified habitats, and hence no evidence for partner fidelity feedbacks, in which ants are incentivised to protect fern hosts. Per species, non-native ant species in the oil palm plantation habitat (18 % of occurrences) were as important as native ones in terms of fern protection and contributed to an increase in ant abundance and species richness with fern size. We conclude that this by-product mutualism persists in logged forest and oil palm plantation habitats, with no detectable shift in partner benefits. Such persistence of generalist interactions in novel ecosystems may be important for driving ecosystem functioning.

Experimentally testing and assessing the predictive power of species assembly rules for tropical canopy ants.

Understanding how species assemble into communities is a key goal in ecology. However, assembly rules are rarely tested experimentally, and their ability to shape real communities is poorly known. We surveyed a diverse community of epiphyte-dwelling ants and found that similar-sized species co-occurred less often than expected. Laboratory experiments demonstrated that invasion was discouraged by the presence of similarly sized resident species. The size difference for which invasion was less likely was the same as that for which wild species exhibited reduced co-occurrence. Finally we explored whether our experimentally derived assembly rules could simulate realistic communities. Communities simulated using size-based species assembly exhibited diversities closer to wild communities than those simulated using size-independent assembly, with results being sensitive to the combination of rules employed. Hence, species segregation in the wild can be driven by competitive species assembly, and this process is sufficient to generate observed species abundance distributions for tropical epiphyte-dwelling ants.

The simulated hospital environment: a qualitative study applying space industry techniques.

Patterned after the integrated simulation approach utilized in the space industry, we report results of an innovative simulation in nursing, a 96-hour continuous simulated hospital environment. Training objectives for our study emphasized the integrative and critical thinking skills needed by new graduate nurses. The purpose of this study was to determine the process for development and the experience of participating in a simulated hospital environment. We sought to (a) translate space industry-integrated simulation techniques into development of a simulated hospital environment and (b) determine the experience of participating in an integrated simulation experience among undergraduate (UG) and graduate nursing students and nursing faculty. We used a qualitative mixed-methods design. Data were collected from participant focus groups, debriefing sessions, research team field notes, and electronic health record documentation. The sample, 72 student focus group participants, consisted of 12 baccalaureate-level soon-to-graduate students and 60 graduate nurse practitioner students as patient actors and providers. Important themes emerged from the project. We were able to design a simulated hospital environment that was true to life. Notably, student knowledge-practice gap was a major theme of the study, consistent with studies of employer concerns of new graduate nurses.

Biodiversity hanging by a thread: the importance of fungal litter-trapping systems in tropical rainforests.

The exceptionally high species richness of arthropods in tropical rainforests hinges on the complexity of the forest itself: that is, on features such as the high plant diversity, the layered nature of the canopy and the abundance and the diversity of epiphytes and litter. We here report on one important, but almost completely neglected, piece of this complex jigsaw-the intricate network of rhizomorph-forming fungi that ramify through the vegetation of the lower canopy and intercept falling leaf litter. We show that this litter-trapping network is abundant and intercepts substantial amounts of litter (257.3 kg ha(-1)): this exceeds the amount of material recorded in any other rainforest litter-trapping system. Experimental removal of this fungal network resulted in a dramatic reduction in both the abundance (decreased by 70.2 ± 4.1%) and morphospecies richness (decreased by 57.4 ± 5.1%) of arthropods. Since the lower canopy levels can contain the highest densities of arthropods, the proportion of the rainforest fauna dependent on the fungal networks is likely to be substantial. Fungal litter-trapping systems are therefore a crucial component of habitat complexity, providing a vital resource that contributes significantly to rainforest biodiversity.

Establishing the evidence base for maintaining biodiversity and ecosystem function in the oil palm landscapes of South East Asia.

The conversion of natural forest to oil palm plantation is a major current threat to the conservation of biodiversity in South East Asia. Most animal taxa decrease in both species richness and abundance on conversion of forest to oil palm, and there is usually a severe loss of forest species. The extent of loss varies significantly across both different taxa and different microhabitats within the oil palm habitat. The principal driver of this loss in diversity is probably the biological and physical simplification of the habitat, but there is little direct evidence for this. The conservation of forest species requires the preservation of large reserves of intact forest, but we must not lose sight of the importance of conserving biodiversity and ecosystem processes within the oil palm habitat itself. We urgently need to carry out research that will establish whether maintaining diversity supports economically and ecologically important processes. There is some evidence that both landscape and local complexity can have positive impacts on biodiversity in the oil palm habitat. By intelligent manipulation of habitat complexity, it could be possible to enhance not only the number of species that can live in oil palm plantations but also their contribution to the healthy functioning of this exceptionally important and widespread landscape.

Inclusive fitness theory and eusociality.

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

Behavioural ecology: the menopausal aphid glue-bomb.

A gall-forming aphid has an extended post-reproductive life in which adults become transformed into glue-packed warriors able to defend their colony. These aphids thus provide a novel example of late-life, post-reproductive helping behaviour.

Stochastic and deterministic processes jointly structure tropical arthropod communities.

The question of whether ecological assemblages are structured by stochastic and deterministic (e.g. interspecific competition) processes is controversial, but it is difficult to design sampling regimes and experiments that can dissect the relative importance of stochastic and deterministic processes in natural assemblages. Using null models, we tested communities of arthropod decomposers in tropical epiphytes for patterns of species co-occurrence, while controlling for habitat gradients, seasonal variations and ecological succession. When environmental conditions were controlled, our analysis showed that the communities were structured stochastically. However, analysing mixed sets of communities that were deliberately created either from two distinct heights or two successional stages revealed that communities were structured deterministically. These results confirm that habitat gradients and dispersal/competition trade-offs are capable of generating non-random patterns within decomposer arthropod communities, but reveal that when such effects are accounted for, species co-occurrence is fundamentally random.

Children's perceptions of rainforest biodiversity: which animals have the lion's share of environmental awareness?

Globally, natural ecosystems are being lost to agricultural land at an unprecedented rate. This land-use often results in significant reductions in abundance and diversity of the flora and fauna as well as alterations in their composition. Despite this, there is little public perception of which taxa are most important in terms of their total biomass, biodiversity or the ecosystem services they perform. Such awareness is important for conservation, as without appreciation of their value and conservation status, species are unlikely to receive adequate conservation protection. We investigated children's perceptions of rainforest biodiversity by asking primary-age children, visiting the University Museum of Zoology, Cambridge to draw their ideal rainforest. By recording the frequency at which children drew different climatic, structural, vegetative and faunal components of the rainforest, we were able to quantify children's understanding of a rainforest environment. We investigated children's perceptions of rainforest biodiversity by comparing the relative numbers of the taxa drawn with the actual contributions made by these taxa to total rainforest biomass and global biodiversity. We found that children have a sophisticated view of the rainforest, incorporating many habitat features and a diverse range of animals. However, some taxa were over-represented (particularly mammals, birds and reptiles) and others under-represented (particularly insects and annelids) relative to their contribution to total biomass and species richness. Scientists and naturalists must continue to emphasise the diversity and functional importance of lesser-known taxa through public communication and outdoor events to aid invertebrate conservation and to ensure that future generations are inspired to become naturalists themselves.

Duelling aphids: electrical penetration graphs reveal the value of fighting for a feeding site.

Horned aphids (Cerataphidini) fight each other for access to feeding sites on leaves. An attacker attempts to force another aphid to abandon its feeding site; the victor then appears to insert its stylets into the site relinquished by the loser. This study used electrical penetration graph (EPG) recordings of Astegopteryx pallida (Van der Goot) individuals to pinpoint the benefits of fighting. We show that victors take significantly less time to commence feeding in the phloem, measured from the start of probing with their stylets, compared with aphids that initiate a new or discover an abandoned site: 9.0 versus 22.9 min, respectively. We also recorded the behaviour of aphids unencumbered with the wire necessary for EPG recordings. Those adult aphids that acquired a feeding site through fighting commenced feeding on average 20 min earlier than those that did not, taking into account the time spent searching and fighting as well as probing. This study clearly establishes that horned aphids use the exact feeding site vacated by another individual and that the benefit they gain is rapid access to the phloem - more rapid, indeed, than has previously been recorded in any aphid.

Oil palm research in context: identifying the need for biodiversity assessment.

Oil palm cultivation is frequently cited as a major threat to tropical biodiversity as it is centered on some of the world's most biodiverse regions. In this report, Web of Science was used to find papers on oil palm published since 1970, which were assigned to different subject categories to visualize their research focus. Recent years have seen a broadening in the scope of research, with a slight growth in publications on the environment and a dramatic increase in those on biofuel. Despite this, less than 1% of publications are related to biodiversity and species conservation. In the context of global vegetable oil markets, palm oil and soyabean account for over 60% of production but are the subject of less than 10% of research. Much more work must be done to establish the impacts of habitat conversion to oil palm plantation on biodiversity. Results from such studies are crucial for informing conservation strategies and ensuring sustainable management of plantations.

Ecological correlates of sociality in Pemphigus aphids, with a partial phylogeny of the genus.

BACKGROUND: Because the systems of social organisation in the various species of Pemphigus aphids span the continuum from asociality through to advanced sociality (typified by the possession of morphologically specialised soldiers), the genus is an ideal model clade in which to study the influence of ecology on the origins of eusociality. We made detailed study of the ecology of three gall-dwelling species that show clear differences in their levels of social behaviour. To elucidate evolutionary relationships and to attempt to estimate the number of origins of sociality, we also created a phylogeny based on sequences spanning the mitochondrial genes Cytochrome Oxidase I and II for nine species of Pemphigus. RESULTS: P. spyrothecae, a highly social species with aggressive morphologically-specialised soldiers, has the longest galling phase, unsynchronised development of a large number of individuals in a densely-populated gall, and an extended period over which alates emerge. P. populi, a species with no soldiers, has the shortest galling phase, synchronised development of a small number of individuals in a sparsely-populated gall, and an extremely brief emergence period. The ecology of P. bursarius, which has behavioural soldiers that are not morphologically specialised, is intermediate between these two extremes. The galls of P. spyrothecae and P. bursarius form small openings during the course of the season and predation-related mortality is relatively high in these two species. Conversely, predation does not occur during the galling phase of P. populi, which has no soldiers but makes an entirely-sealed gall. The phylogeny allowed us to infer one likely point of origin of basic social defence and two independent origins of enhanced defence. Based on current knowledge of behaviour, the phylogeny also suggests that the defence trait may have been lost at least once. CONCLUSION: The life-history strategy of P. spyrothecae appears to be geared towards defending the colony against the constant threat of predation that faces the inhabitants of a long-lived, open gall. The life-history strategy of P. populi, on the other hand, is to avoid predation in the closed gall fortress and flee for the secondary host at the earliest opportunity. The life-history strategy of P. bursarius appears to represent a compromise between these strategies.

Costs of egg-laying and offspring provisioning: multifaceted parental investment in a digger wasp.

Nest-building Hymenoptera have been a major testing ground for theories of parental investment and sex allocation. Investment has usually been estimated by the likely costs of offspring provisioning, ignoring other aspects of parental care. Using three experimental treatments, we estimated the costs of egg-laying and provisioning separately under field conditions in a digger wasp Ammophila pubescens. In one treatment, we increased the provisioning effort required per offspring by removing alternate prey items as they were brought to the nest. In two other treatments, we reduced parental effort by either preventing females from provisioning alternate nests or preventing them from both ovipositing and provisioning. Our results indicate that both egg-laying and provisioning represent significant costs of reproduction, expressed as differences in productivity but not survival. A trade-off-based model suggests that other components of parental care such as nest initiation may also represent significant costs. Costs of egg production and nest initiation are probably similar for male and female offspring, so that taking them into account leads to a less male-biased expected sex ratio. Mothers compensated only partially for prey removal in terms of the total provisions they gave to individual offspring.