How does inter-individual variation affect group level behaviour?

No two animals are the same. Individual differences in personality, memory or internal state may lead two different animals to make different choices or show different behavioural phenotypes. These inter-individual differences are key to understanding the life history strategies animals have adopted to adapt to their environments. However, despite the importance of inter-individual differences to our understanding of animal behaviour, there are still significant gaps in our knowledge of how inter-individual differences may affect group level behaviours. In this thesis I therefore aimed to determine how inter-individual differences in personality or memory may affect group level behaviour in social and subsocial invertebrates. In this thesis I describe lab-based behavioural trials on social and subsocial model systems (Temnothorax albipennis and Oniscus asellus respectively) to empirically test whether differences in inter-individual memories or personality affects group level decision-making and stability. I then further investigated the possible mechanisms behind our findings using agent-based modelling. The thesis shows that differences in both personality and memory played an important role in the emergence of group level behaviours and suggested that greater integration of the fields of animal personality and collective behaviour could greatly benefit our understanding of animal behaviour. I also explored the ethics and implications of carrying out animal behaviour studies. I suggested that research into invertebrate personality has many possible benefits both through tangible conservation interventions, as well as benefitting our theoretical understanding of animal interactions. However, I also highlighted the importance of continued re-evaluation of the ethics of the methods used in invertebrate research in light of shifting research into invertebrate cognition and public perception. I hope this work will spark further work into the role which inter-individual differences may play in group level behaviours as well as further interest in exploring the ethics and implications of this types of work

Keeping invertebrate research ethical in a landscape of shifting public opinion

(1) Invertebrate study systems are cornerstones of biological and biomedical research, providing key insights into fields from genetics to behavioural ecology. Despite the widespread use of invertebrates in research there are very few ethical guidelines surrounding their use. (2) Focussing on two ethical considerations faced during invertebrate studies – collecting methods and euthanasia - we make recommendations for integrating principles of vertebrate research into invertebrate research practice. (3) We argue, given emerging research on invertebrate cognition and shifting public perception on the use of invertebrates in research, it is vital that the scientific community revisits the ethics of invertebrate use in research. (4) Without careful consideration and development of the ethics surrounding the use of invertebrates by the scientific community, there is a danger of losing public support. It is imperative that the public understand the significance of research that uses invertebrates and that scientists demonstrate their ethical treatment of their experimental subjects

Leech blood-meal invertebrate-derived DNA reveals differences in Bornean mammal diversity across habitats.

The application of metabarcoding to environmental and invertebrate-derived DNA (eDNA and iDNA) is a new and increasingly applied method for monitoring biodiversity across a diverse range of habitats. This approach is particularly promising for sampling in the biodiverse humid tropics, where rapid land-use change for agriculture means there is a growing need to understand the conservation value of the remaining mosaic and degraded landscapes. Here we use iDNA from blood-feeding leeches (Haemadipsa picta) to assess differences in mammalian diversity across a gradient of forest degradation in Sabah, Malaysian Borneo. We screened 557 individual leeches for mammal DNA by targeting fragments of the 16S rRNA gene and detected 14 mammalian genera. We recorded lower mammal diversity in the most heavily degraded forest compared to higher quality twice logged forest. Although the accumulation curves of diversity estimates were comparable across these habitat types, diversity was higher in twice logged forest, with more taxa of conservation concern. In addition, our analysis revealed differences between the community recorded in the heavily logged forest and that of the twice logged forest. By revealing differences in mammal diversity across a human-modified tropical landscape, our study demonstrates the value of iDNA as a noninvasive biomonitoring approach in conservation assessments

A novel observation of food dunking in the Australian Magpie Gymnorhina tibicen

We document putative food-dunking behaviour in the Australian Magpie Gymnorhina tibicen. While conducting an experiment on the Mountain Katydid Acripeza reticulata, we presented one to a wild adult Magpie, which appeared to conduct 'dunking behaviour' while processing the insect. The Magpie carried the katydid to a puddle of water, dunked the katydid, and then dropped it. A nearby juvenile Magpie then retrieved the katydid and performed the same dunking behaviour before eating the katydid. To our knowledge, this is the frst reported instance of food dunking by Australian Magpies. We hope this observation will facilitate future investigations into behavioural adaptations to dietary choices of Magpies

The protective value of the colour and shape of the mountain katydid's antipredator defence

Deimatic behaviour is performed by prey when attacked by predators as part of an antipredator strategy. The behaviour is part of a sequence that consists of several defences, for example they can be preceded by camouflage and followed by a hidden putatively aposematic signal that is only revealed when the deimatic behaviour is performed. When displaying their hidden signal, mountain katydids (Acripeza reticulata) hold their wings vertically, exposing striking red and black stripes with blue spots and oozing an alkaloid-rich chemical defence derived from its Senecio diet. Understanding differences and interactions between deimatism and aposematism has proven problematic, so in this study we isolated the putative aposematic signal of the mountain katydid's antipredator strategy to measure its survival value in the absence of their deimatic behaviour. We manipulated two aspects of the mountain katydid's signal, colour pattern and whole body shape during display. We deployed five kinds of clay models, one negative control and four katydid-like treatments, in 15 grids across part of the mountain katydid's distribution to test the hypothesis that their hidden signal is aposematic. If this hypothesis holds true, we expected that the models, which most closely resembled real katydids would be attacked the least. Instead, we found that models that most closely resembled real katydids were the most likely to be attacked. We suggest several ideas to explain these results, including that the deimatic phase of the katydid's display, the change from a camouflaged state to exposing its hidden signal, may have important protective value

The protective value of a defensive display varies with the experience of wild predators

Predation has driven the evolution of diverse adaptations for defence among prey, and one striking example is the deimatic display. While such displays can resemble, or indeed co-occur with, aposematic ‘warning’ signals, theory suggests deimatic displays may function independently of predator learning. The survival value of deimatic displays against wild predators has not been tested before. Here we used the mountain katydid Acripeza reticulata to test the efficacy of a putative deimatic display in the wild. Mountain katydids have a complex defence strategy; they are camouflaged at rest, but reveal a striking red-, blue-, and black-banded abdomen when attacked. We presented live katydids to sympatric (experienced) and allopatric (naive) natural predators, the Australian magpie Cracticus tibicen, and observed bird reactions and katydid behaviors and survival during repeated interactions. The efficacy of the katydids’ defence differed with predator experience. Their survival was greatest when faced with naïve predators, which provided clear evidence of the protective value of the display. In contrast, katydid survival was consistently less likely when facing experienced predators. Our results suggest that sympatric predators have learned to attack and consume mountain katydids despite their complex defense, and that their post-attack display can be an effective deterrent, particularly against naïve predators. These results suggest that deimatism does not require predator learning to afford protection, but that a predator can learn to expect the display and subsequently avoid it or ignore it. That sympatric predators learn to ignore the defense is a possible explanation for the mountain katydid’s counter-intuitive behavior of revealing warning colors only after tactile stimuli from predator attack.peerReviewe

A synthesis of deimatic behaviour

Deimatic behaviours, also referred to as startle behaviours, are used against predators and rivals. Although many are spectacular, their proximate and ultimate causes remain unclear. In this review we aim to synthesise what is known about deimatic behaviour and identify knowledge gaps. We propose a working hypothesis for deimatic behaviour, and discuss the available evidence for the evolution, ontogeny, causation, and survival value of deimatic behaviour using Tinbergen's Four Questions as a framework. Our overarching aim is to direct future research by suggesting ways to address the most pressing questions in this field.peerReviewe

Leech blood-meal iDNA reveals differences in Bornean mammal diversity across habitats

Description: This data set includes the data used in Drinkwater et al. (2020) Leech blood-meal iDNA reveals differences in Bornean mammal diversity across habitats, submitted to Molecular Ecology. There are three sets of data based on the biomonitoring of mammals using iDNA extracted from leeches collected across the SAFE project (and DVCA) in 2016. At each site in the SAFE landscape 20 minute handsearches took place within the boundaries of fixed 25m2 vegetation plots. For these analyses we only used Haemadipsa picta individuals, as previous studies have revealed species differences between H. picta and H. zeylanica in the SAFE area. With metabarcoding techniques, first we extracted and amplified the 16S rRNA region of mammal DNA, from site-matched pools of leeches using PCR and specific mammal primers. NGS sequencing was used and the short fragments were then identified using in silico PCR with ecoPCR and OBITOOLS (metabarcoding packages) to assign taxonomy to the unknown sequences. We then analysed diversity in different habitats across the landscape and included microclimate data, from LiDAR scans of the landscape as variables which could impact the detection of mammals. Project: This dataset was collected as part of the following SAFE research project: The effects of rainforest fragmentation on mammal community assemblages using leech blood-meal analysisFunding: These data were collected as part of research funded by: NERC (Standard grant , NE/K016148/1)NERC (Independent research grant, NE/S01537X/1)This dataset is released under the CC-BY 4.0 licence, requiring that you cite the dataset in any outputs, but has the additional condition that you acknowledge the contribution of these funders in any outputs.Permits: These data were collected under permit from the following authorities:Sabah Biodiversity Council (Research licence JKM/MBS.1000 2/2 (34))Sabah Biodiversity Council (Research licence JKM/MBS.1000 2/3 JLD.2 (107))Sabah Biodiversity Council (Export licence JKM/MBS.1000 2/3 JLD.3 (44))Danum Valley Conservation Area (Research licence YS/DVMC/2016/253)XML metadata: GEMINI compliant metadata for this dataset is available hereFiles: This consists of 1 file: Drinkwater2020-iDNA_diversity3.xlsxDrinkwater2020-iDNA_diversity3.xlsxThis file contains dataset metadata and 3 data tables:UNFILTERED Taxonomic assignment of iDNA sequences (described in worksheet ecoTAG_output_raw)Description: UNFILTERED This dataset is the raw output of the in silico PCR using the programs ecoPCR and the OBITOOLS package. The exact primers are matched against all mammal sequences in GenBank (NCBI) using a minimum of three mismatches between primer and query sequence and a quality filter of a minimum identity of 0.95. This dataset was subsequently filtered for contaminant, geographically implausible mammals and collapsed by haplotype per poolNumber of fields: 15Number of data rows: 3454Fields: id: Unique sequence ID within leech pool (Field type: id)site: The site at the SAFE project from which the pool of leeches was collected (Field type: id)hab: The habitat type of the site at the SAFE project from which the pool of leeches was collected (Field type: id)count: Count of the times this sequence was found - UNFILTERED (Field type: numeric)best_identity: Percent identity match between query and database sequence - UNFILTERED (Field type: numeric)family: Family taxid - following GenBank (Field type: id)family_name: Family name (Field type: id)genus: Genus taxid - following GenBank (Field type: id)genus_name: Genus name (Field type: id)order: Order taxid - following GenBank (Field type: id)order_name: Order name (Field type: id)species: Species taxid - following GenBank (Field type: id)species_name: Species name (Field type: id)Assigned_name: Assigned taxonomic name (Field type: id)sequence: Query sequence (Field type: id)Mammal detections recorded in each pool (described in worksheet detections)Description: From the taxonomic assignment list, the unique sequences identfied in each pool are are recorded as detections. The value is a count of the numebr of time the unique sequence for that taxon was recorded in the pool. Geographically implausible mammals have been removed and taxa which agree per site have been collapsed. This give a detections by pool matrix. For analyses these counts were converted into presence/absence data. Number of fields: 19Number of data rows: 57Fields: pool: This is the pool name given to the leech pool for sequencing (Field type: id)site: The site at the SAFE project from which the pool of leeches was collected (Field type: id)leeches: This is the number of individual leeches which make up the pool (Field type: numeric)habitat: Habitat type - classification used in the paper to describe the quality of forest in the sites where the leeches were collected (Field type: id)Arctogalidia: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Elephas: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Felidae: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Helarctos: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Hemigalus: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Hystrix: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Macaca: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Manis: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Muntiacus: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Rusa: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Sus: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Paguma: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Tragulus: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Trichys: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Viverra: Occurrence of detections of this taxon in a leech pool, as determined from leech-based iDNA (Field type: abundance)Microclimate variables (described in worksheet microclimate)Description: Mean and maximum temperature and mean and maximum VPD extracted at each of the second order points used in the study. These values were extracted from microclimate surfaces generated in Jucker et al., (2018), using the coordinates from the centre of each of the 25m2 plots. For the values in Danum Valley Conservation Area (DVCA), these were extracted from the nearest river point (coordinates given).Number of fields: 6Number of data rows: 92Fields: Code: SAFE second order points including LOMBOK points at RLFE and three river sites at DVCA (Field type: location)site: The site at the SAFE project from which the pool of leeches was collected (Field type: id)T_max_raster: The maximum daily temperature at each second order point (Field type: numeric)T_mean_raster: The mean daily temperature at each second order point (Field type: numeric)VPD_max_raster: The maximum daily vapour pressure deficit (VPD) at each second order point (Field type: numeric)VPD_mean_raster: The mean daily vapour pressure deficit (VPD) at each second order point (Field type: numeric)Date range: 2016-01-01 to 2016-12-31Latitudinal extent: 4.5000 to 5.0700Longitudinal extent: 116.7500 to 117.8200Taxonomic coverage: All taxon names are validated against the GBIF backbone taxonomy. If a dataset uses a synonym, the accepted usage is shown followed by the dataset usage in brackets. Taxa that cannot be validated, including new species and other unknown taxa, morphospecies, functional groups and taxonomic levels not used in the GBIF backbone are shown in square brackets. -  Animalia  -  -  Chordata  -  -  -  Mammalia  -  -  -  -  Rodentia  -  -  -  -  -  Hystricidae  -  -  -  -  -  -  Hystrix  -  -  -  -  -  -  Trichys  -  -  -  -  -  -  -  Trichys fasciculata  -  -  -  -  Proboscidea  -  -  -  -  -  Elephantidae  -  -  -  -  -  -  Elephas  -  -  -  -  -  -  -  Elephas maximus  -  -  -  -  Primates  -  -  -  -  -  Cercopithecidae  -  -  -  -  -  -  Macaca  -  -  -  -  Carnivora  -  -  -  -  -  Felidae  -  -  -  -  -  Viverridae  -  -  -  -  -  -  Viverra  -  -  -  -  -  -  -  Viverra tangalunga  -  -  -  -  -  -  Paguma  -  -  -  -  -  -  -  Paguma larvata  -  -  -  -  -  -  Arctogalidia  -  -  -  -  -  -  -  Arctogalidia trivirgata  -  -  -  -  -  -  Hemigalus  -  -  -  -  -  -  -  Hemigalus derbyanus  -  -  -  -  -  Ursidae  -  -  -  -  -  -  Helarctos  -  -  -  -  -  -  -  Helarctos malayanus  -  -  -  -  Pholidota  -  -  -  -  -  Manidae  -  -  -  -  -  -  Manis  -  -  -  -  -  -  -  Manis javanica  -  -  -  -  Artiodactyla  -  -  -  -  -  Suidae  -  -  -  -  -  -  Sus  -  -  -  -  -  -  -  Sus barbatus  -  -  -  -  -  Tragulidae  -  -  -  -  -  -  Tragulus  -  -  -  -  -  Cervidae  -  -  -  -  -  -  Muntiacus  -  -  -  -  -  -  Rusa  -  -  -  -  -  -  -  Rusa unicolor</i