The trophic ecology of non-native ants on Round Island, Mauritius

Summary Non-native ants are implicated in the demise of native species around the world, though their trophic ecology remains poorly understood. Non-native ants have invaded Round Island, a globally significant site of biodiversity conservation located 21 km north-east of Mauritius in the Indian Ocean, but it is unclear how they are affecting the unique ecological community found there. To reveal their potential impact, I conducted a meta-analysis into the effects of non-native ants on animal community diversity in relatively undisturbed areas around the world, showing that non-native ants drive diversity declines in local animal communities by approximately 50 % on average (Chapter 2). I then examined the ecological role of non-native ants on Round Island specifically and first determined, using dietary DNA metabarcoding, whether an abundant native omnivore, Telfair’s skink, consumed non-native ants. Skinks do consume ants, though it was unclear to what degree these detections were deliberate or accidental (Chapter 3). I then identified the diet of the 12 most numerous non-native ant species on Round Island using dietary metabarcoding, revealing that all ant species showed unique generalist diet profiles and together consume over 150 species of animals and plants. The diet of the ant community was also driven by seasonal changes in food availability. This presents the first study to date detailing the diet of individual ants at the community level and that a community of generalist non-native species exhibit dietary niche separation (Chapter 4). I compared the diet of native skinks and centipedes with that of non-native ants, finding that skinks are not competing with ants for food, whilst centipedes are (Chapter 5). Overall, our results suggest, through five separate lines of evidence arising from the study, that non-native ants are having a significant impact on the Round Island ecosystem

Temporal variation in spider trophic interactions is explained by the influence of weather on prey communities, web building and prey choice

1. Generalist invertebrate predators are sensitive to weather conditions, but the relationship between their trophic interactions and weather is poorly understood. This study investigates how weather affects the identity and frequency of spider trophic interactions over time, alongside prey community structure, web characteristics and prey choice. 2. Spiders (Linyphiidae and Lycosidae) and their prey were collected from barley fields in Wales, UK from April to September 2017-2018. The gut contents of 300 spiders were screened using DNA metabarcoding, analysed via multivariate models, and compared against prey availability using null models. When linyphiids were collected from webs, the height and area of webs were recorded and compared against weather conditions. 3. Trophic interactions changed over time and with weather conditions, primarily related to concomitant changes in prey communities. Spiders did, however, appear to mitigate the effects of structural changes in prey communities through changing prey preferences according to prevailing weather conditions, possibly facilitated by adaptive web construction. 4. Using these findings, we demonstrate that prey choice data collected under different weather conditions can be used to refine inter-annual predictions of spider trophic interactions, although prey abundance was secondary to diversity in driving the diet of these spiders. By improving our understanding of the interaction between trophic interactions and weather, we can better predict how ecological networks are likely to change over time in response to variation in weather conditions and, more urgently, global climate change

Non‐native ants drive dramatic declines in animal community diversity: A meta‐analysis

Non‐native ants can cause ecosystem‐wide ecological change, and these changes are generally assumed to be negative. Despite this, the evidence base has never been holistically synthesised to quantify whether and to what degree non‐native ants impact native species diversity. In this study, we performed a meta‐analysis of the effects of ant invasion on animal communities. We extracted data from 46 published articles investigating abundance (156 effect sizes) and richness (53 effect sizes) responses of animal taxa to ant invasion in locations relatively unimpacted by other stressors (e.g. human disturbance, other non‐native species) to help isolate the effects of invasion. Overall, local animal diversity declined severely, with species abundance and richness lower by 42.79% and 53.56%, respectively, in areas with non‐native ants compared with intact uninvaded sites. We then combined responses of individual animal taxa extracted from an article into a single response to represent the ‘community’ abundance (40 effect sizes) or richness (28 effect sizes) response to non‐native ants represented in each article. Local communities decreased substantially in total abundance (52.67%) and species richness (53.47%) in invaded sites. These results highlight non‐native ants as the drivers, rather than passengers, of large net‐negative reductions to animal community diversity in relatively undisturbed systems around the world, approximately halving local species abundance and richness in invaded areas. Improved international prevention processes, early detection systems harnessing emerging technologies, and well‐designed control measures deployable by conservation practitioners are urgently needed if these effects are to be mitigated, prevented or reversed

Observational and metabarcoding approaches reveal the ecology, natural history and conservation status of Scolopendra abnormis, a threatened centipede endemic to Mauritius

The Serpent Island centipede Scolopendra abnormis is a threatened centipede species found on only 2 small islands in the Indian Ocean: Round Island, located 22.5 km northeast of Mauritius, and Serpent Island, 4 km northwest of Round Island. Current understanding of its ecology is based on limited direct observations from 30 yr ago. Round Island has since undergone significant habitat restoration. Hyperabundant non-native ants are also present, which may impact centipede nesting behaviour, ecology, and survival. Recent methodological advances, such as high-throughput sequencing of dietary DNA, can extend our understanding of invertebrate ecology and provide data complementary to direct observation. Using a combination of dietary metabarcoding and observational approaches, we provide new insights into the ecology and natural history of this threatened invertebrate predator. S. abnormis nest most consistently in the root network found beneath endemic Pandanus vandermeeschii trees. They are also found in areas with good soil cover, herbaceous growth, and areas of bare rock slab. Only 4 of 43 centipedes in this study were found near an ant foraging trail, which may have significant implications for S. abnormis nesting habits. These centipedes primarily consume insect prey (particularly taxa within Lepidoptera, Hymenoptera, Diptera), irrespective of centipede body size. A quarter of centipedes also consumed endemic lizards. We also found marked differences in diet composition between wet and dry seasons arising from the changing availability of prey. We provide additional natural history observations and conclude by suggesting conservation actions that would help better understand and safeguard S. abnormis populations

Overcoming the pitfalls of merging dietary metabarcoding into ecological networks

The construction of increasingly detailed species interaction networks is extending the potential applications of network ecology, providing an opportunity to understand complex eco-evolutionary interactions, ecosystem service provision and the impacts of environmental change on ecosystem functioning. Dietary metabarcoding is a rapidly growing tool increasingly used to construct ecological networks of trophic interactions, enabling the determination of individual animal diets including difficult-to-distinguish prey taxa and even for species where traditional dietary analyses are unsuitable (e.g. fluid feeders and small invertebrates). Several challenges, however, surround the use of dietary metabarcoding, especially when metabarcoding-based interactions are merged with observation-based species interaction data. We describe the difficulties surrounding the quantification of species interactions, sampling perspective discrepancy (i.e. zoocentric vs. phytocentric sampling), experimental biases, reference database omissions and assumptions regarding direct and indirect consumption events. These problems are not, however, insurmountable. Effective experimental design and data curation with appropriate attention paid to these problems renders the incorporation of dietary metabarcoding into ecological network analysis a powerful tool for the construction of highly resolved networks. Throughout, we discuss how these problems should be addressed when merging data to construct ecological networks

Prey nutrient content is associated with the trophic interactions of spiders and their prey selection under field conditions

Consumers are thought to select food resources based on their nutritional content. While laboratory experiments have explored this, the nutritional dynamics of invertebrate predators have been scarcely studied in the field given various methodological constraints. The intersection of these nutritional dynamics with predator traits is also poorly characterised, leading to many gaps in our understanding of how different predators forage and feed in natural systems. Here, we integrate dietary metabarcoding with prey macronutrient (protein, lipid and carbohydrate) content and abundance to assess how nutrients and predator traits (sex, life stage and taxonomy) interactively drive prey preferences in the field, using spider–prey interactions as a model system. Different spider genera, sexes and life stages had nutritionally distinct diets. Our analyses demonstrated disproportionate foraging (selection and avoidance) for prey rich in different macronutrients, with the nature of these relationships differing between spider taxa, life stages and sexes. This may be explained by niche differentiation among spider groups, driven by biases toward prey rich in different nutrients, or nutrient-specific foraging in which individual spiders vary their nutritional preferences to redress deficits, although further evidence is required to confirm this. This insight into the nutritional dynamics of generalist invertebrate predators extends our understanding beyond lab-based behavioural assays and provides a novel framework for other complex real-world systems

The predator problem and PCR primers in molecular dietary analysis: Swamped or silenced; depth or breadth?

Dietary metabarcoding has vastly improved our ability to analyse the diets of animals, but it is hampered by a plethora of technical limitations including potentially reduced data output due to the disproportionate amplification of the DNA of the focal predator, here termed “the predator problem”. We review the various methods commonly used to overcome this problem, from deeper sequencing to exclusion of predator DNA during PCR, and how they may interfere with increasingly common multipredator‐taxon studies. We suggest that multiprimer approaches with an emphasis on achieving both depth and breadth of prey detections may overcome the issue to some extent, although multitaxon studies require further consideration, as highlighted by an empirical example. We also review several alternative methods for reducing the prevalence of predator DNA that are conceptually promising but require additional empirical examination. The predator problem is a key constraint on molecular dietary analyses but, through this synthesis, we hope to guide researchers in overcoming this in an effective and pragmatic way

The predator problem and PCR primers in molecular dietary analysis: Swamped or silenced; depth or breadth?

Dietary metabarcoding has vastly improved our ability to analyse the diets of animals, but it is hampered by a plethora of technical limitations including potentially reduced data output due to the disproportionate amplification of the DNA of the focal predator, here termed “the predator problem”. We review the various methods commonly used to overcome this problem, from deeper sequencing to exclusion of predator DNA during PCR, and how they may interfere with increasingly common multipredator‐taxon studies. We suggest that multiprimer approaches with an emphasis on achieving both depth and breadth of prey detections may overcome the issue to some extent, although multitaxon studies require further consideration, as highlighted by an empirical example. We also review several alternative methods for reducing the prevalence of predator DNA that are conceptually promising but require additional empirical examination. The predator problem is a key constraint on molecular dietary analyses but, through this synthesis, we hope to guide researchers in overcoming this in an effective and pragmatic way

Density-independent prey choice, taxonomy, life history and web characteristics determine the diet and biocontrol potential of spiders (Linyphiidae and Lycosidae) in cereal crops

Spiders are among the dominant invertebrate predators in agricultural systems and are significant regulators of insect pests. The precise dynamics of biocontrol of pests in the field are, however, poorly understood. This study investigates how density-independent prey choice, taxonomy, life stage, sex, and web characteristics affect spider diet and biocontrol. We collected spiders in four genera of Linyphiidae (i.e., Bathyphantes, Erigone, Tenuiphantes, and Microlinyphia), and individuals from the Lycosidae genus Pardosa, and their proximate prey communities from barley fields in Wales, UK between April and September 2018. We analyzed the gut contents of 300 individual spiders using DNA metabarcoding. From the 300 spiders screened, 89 prey taxa were identified from 45 families, including a wide range of pests and predators. Thrips were the dominant prey, present in over a third of the spiders sampled, but a type IV functional response appears to reduce their predation at peak abundances. Spider diets significantly differed based on web characteristics, but this depended on the genus and sex of the spider and it was not the principal separating factor in the trophic niches of linyphiids and lycosids. Diets significantly differed between spider genera and life stages, reflected in different propensities for intraguild predation and pest predation. Adult spiders predated a greater diversity of other predators, and juveniles predated a greater diversity of pests. Overall, Tenuiphantes spp. and Bathyphantes spp. exhibited the greatest individual potential for biocontrol of the greatest diversity of pest genera. The greater trophic niche complementarity of Pardosa spp. and Erigone spp., however, suggests that their complementary predation of different pests might be of greater overall benefit to biocontrol. Sustainable agriculture should aim to optimize conditions throughout the cropping cycle for effective biocontrol, prioritizing provision for a diversity of spiders which predate a complementary diversity of pest species

Money spider dietary choice in pre- and post-harvest cereal crops using metabarcoding

Money spiders (Linyphiidae) are an important component of conservation biological control in cereal crops, but they rely on alternative prey when pests are not abundant, such as between cropping cycles. To optimally benefit from these generalist predators, prey choice dynamics must first be understood. Money spiders and their locally available prey were collected from cereal crops 2 weeks pre‐ and post‐harvest. Spider gut DNA was amplified with two novel metabarcoding primer pairs designed for spider dietary analysis, and sequenced. The combined general and spider‐exclusion primers successfully identified prey from 15 families in the guts of the 46 linyphiid spiders screened, whilst avoiding amplification of Erigone spp. The primers show promise for application to the diets of other spider families such as Agelenidae and Pholcidae. Distinct invertebrate communities were identified pre‐ and post‐harvest, and changes in spider diet and, to a lesser extent, prey choice reflected this. Spiders were found to consume one another more than expected, indicating their propensity towards intraguild predation, but also consumed common pest families. Changes in spider prey choice may redress prey community changes to maintain a consistent dietary intake. Consistent provision of alternative prey via permanent refugia should be considered to sustain effective conservation biocontrol