Julian A. Drewe

Who infects whom? Social networks and tuberculosis transmission in wild meerkats

Transmission of infectious diseases is strongly influenced by who contacts whom. Despite the global distribution of tuberculosis (TB) in free-living wild mammal populations, little is known of the mechanisms of social transmission of Mycobacterium bovis between individuals. Here, I use a network approach to examine for correlations between five distinct types of intra- and intergroup social interaction and changes in TB status of 110 wild meerkats (Suricata suricatta) in five social groups over two years. Contrary to predictions, the most socially interactive animals were not at highest risk of acquiring infection, indicating that in addition to contact frequency, the type and direction of interactions must be considered when quantifying disease risk. Within social groups, meerkats that groomed others most were more likely to become infected than individuals who received high levels of grooming. Conversely, receiving, but not initiating, aggression was associated with M. bovis infection. Incidence of intergroup roving by male meerkats was correlated with the rovers themselves subsequently testing TB-positive, suggesting a possible route for transmission of infection between social groups. Exposure time was less important than these social interactions in influencing TB risk. This study represents a novel application of social network analysis using empirical data to elucidate the role of specific interactions in the transmission of an infectious disease in a free-living wild animal population.

Evaluation of animal and public health surveillance systems: a systematic review

Disease surveillance programmes ought to be evaluated regularly to ensure they provide valuable information in an efficient manner. Evaluation of human and animal health surveillance programmes around the world is currently not standardized and therefore inconsistent. The aim of this systematic review was to review surveillance system attributes and the methods used for their assessment, together with the strengths and weaknesses of existing frameworks for evaluating surveillance in animal health, public health and allied disciplines. Information from 99 articles describing the evaluation of 101 surveillance systems was examined. A wide range of approaches for assessing 23 different system attributes was identified although most evaluations addressed only one or two attributes and comprehensive evaluations were uncommon. Surveillance objectives were often not stated in the articles reviewed and so the reasons for choosing certain attributes for assessment were not always apparent. This has the potential to introduce misleading results in surveillance evaluation. Due to the wide range of system attributes that may be assessed, methods should be explored which collapse these down into a small number of grouped characteristics by focusing on the relationships between attributes and their links to the objectives of the surveillance system and the evaluation. A generic and comprehensive evaluation framework could then be developed consisting of a limited number of common attributes together with several sets of secondary attributes which could be selected depending on the disease or range of diseases under surveillance and the purpose of the surveillance. Economic evaluation should be an integral part of the surveillance evaluation process. This would provide a significant benefit to decision-makers who often need to make choices based on limited or diminishing resources.

Wildlife Population Structure and Parasite Transmission: Implications for Disease Management

The beginning stages of research often involve describing patterns (e.g. males tend to more heavily parasitized than females for a given subset of species). From those initial patterns, researchers then test hypothesised mechanisms that may create those patterns. As an emerging discipline, much of wildlife disease management is about detecting trends and associations, and currently there are few guiding principles that both explain the trends and are applicable across a broad range hosts and parasites. This chapter focuses on the associations between prevalence/transmission and host social structure, where host social structure includes within group factors (eg. sex, age, dominance) and among group factors (eg. group size and movement among groups). Although there are few general theories of how host social structure affects disease dynamics it is clear that a narrow focus on either the host or the pathogen is not as productive as a integrated approach that considers the host-parasite interaction, which is itself affected by the abiotic and biotic factors in the surrounding environment.

Recent advances in the analysis of behavioural organization and interpretation as indicators of animal welfare

While the incorporation of mathematical and engineering methods has greatly advanced in other areas of the life sciences, they have been under-utilized in the field of animal welfare. Exceptions are beginning to emerge and share a common motivation to quantify ‘hidden’ aspects in the structure of the behaviour of an individual, or group of animals. Such analyses have the potential to quantify behavioural markers of pain and stress and quantify abnormal behaviour objectively. This review seeks to explore the scope of such analytical methods as behavioural indicators of welfare. We outline four classes of analyses that can be used to quantify aspects of behavioural organization. The underlying principles, possible applications and limitations are described for: fractal analysis, temporal methods, social network analysis, and agent-based modelling and simulation. We hope to encourage further application of analyses of behavioural organization by highlighting potential applications in the assessment of animal welfare, and increasing awareness of the scope for the development of new mathematical methods in this area.

Novel Cause of Tuberculosis in Meerkats, South Africa

The organism that causes tuberculosis in meerkats (Suricata suricatta) has been poorly characterized. Our genetic analysis showed it to be a novel member of the Mycobacterium tuberculosis complex and closely related to the dassie bacillus. We have named this epidemiologically and genetically unique strain M. suricattae.

Performance of Proximity Loggers in Recording Intra and Inter-Species Interactions: A Laboratory and Field- Based Validation Study

Knowledge of the way in which animals interact through social networks can help to address questions surrounding the ecological and evolutionary consequences of social organisation, and to understand and manage the spread of infectious diseases. Automated proximity loggers are increasingly being used to record interactions between animals, but the accuracy and reliability of the collected data remain largely un-assessed. Here we use laboratory and observational field data to assess the performance of these devices fitted to a herd of 32 beef cattle (Bos taurus) and nine groups of badgers (Meles meles, n  = 77) living in the surrounding woods. The distances at which loggers detected each other were found to decrease over time, potentially related to diminishing battery power that may be a function of temperature. Loggers were highly accurate in recording the identification of contacted conspecifics, but less reliable at determining contact duration. There was a tendency for extended interactions to be recorded as a series of shorter contacts. We show how data can be manipulated to correct this discrepancy and accurately reflect observed interaction patterns by combining records between any two loggers that occur within a 1 to 2 minute amalgamation window, and then removing any remaining 1 second records. We make universally applicable recommendations for the effective use of proximity loggers, to improve the validity of data arising from future studies.

Spatial and temporal interactions between livestock and wildlife in South Central Spain assessed by camera traps.

The diversification of livestock farms into hunting estates in South Central Spain (SCS) may impede the success of Mycobacterium bovis eradication programmes by facilitating transmission between wildlife and livestock. In this observational study we aimed to provide information of relevance about the nature and frequency of interactions (observed visits to study points) between livestock (cattle and domestic pigs) and wildlife (wild boar and red deer). The study was conducted in an extensive cattle farm in SCS where the land is also used for game hunting. During a period of one year, camera traps (n=16) were placed at a priori risk points for interspecies interactions: water (natural and artificial troughs), food placed on the ground for baiting wildlife, and pasture. To define indirect interspecies interactions, a critical time window for M. bovis to survive in the environment was selected based on the literature. Results suggest that wildlife frequented food and pasture points more often than water points, and that the number of visits increased through the dry season, peaking during the acorn season (October-January) and the deer breeding season (June-July). Direct interactions were rare (n=10), as opposed to indirect interactions (n=8992). Wildlife-followed-by-livestock interactions (n=7714) occurred much more often than livestock-followed-by-wildlife (n=1278) and were frequent at water points (66% water points, 17% food, 17% pasture). Results also suggest that water points are a hotspot for indirect interactions and might therefore be a source of infection at the wildlife-livestock interface in the territory covered, particularly for M. bovis, as it is around water where the bacteria seem to survive the longest. Preventing aggregation and therefore reducing contact rates between domestic and wild animals especially at water points may be valuable for disease control in South Central Spain.

Integrating contact network structure into tuberculosis epidemiology in meerkats in South Africa: Implications for control

Empirical studies that integrate information on host contact patterns with infectious disease transmission over time are rare. The aims of this study were to determine the relative importance of intra-group social interactions in the transmission of tuberculosis (TB; Mycobacterium bovis infection) in a population of wild meerkats (Suricata suricatta) in South Africa, and to use this information to propose an evidence-based intervention strategy to manage this disease. Detailed behavioural observations of all members of eight meerkat groups (n=134 individuals) were made over 24 months from January 2006 to December 2007. Social network analysis of three types of interaction (aggression, foraging competitions and grooming) revealed social structure to be very stable over time. Clustering of interactions was positively correlated with group size for both aggression (r=0.73) and grooming interactions (r=0.71), suggesting that infections may spread locally within clusters of interacting individuals but be limited from infecting all members of large groups by an apparent threshold in connections between different clusters. Repeated biological sampling every three months of all members of one social group (n=37 meerkats) was undertaken to quantify individual changes in M. bovis infection status. These empirical data were used to construct a dynamic network model of TB transmission within a meerkat group. The results indicated that grooming (both giving and receiving) was more likely than aggression to be correlated with M. bovis transmission and that groomers were at higher risk of infection than groomees. Intervention strategies for managing TB in meerkats that focus on those individuals engaging in the highest amount of grooming are therefore proposed.

The social network structure of a wild meerkat population: 3. Position of individuals within networks

Individuals in social groups interact with numerous other group members in a polyadic network. Interactions can depend on the individuals own attributes (age, sex, status etc.), on their partners attributes, and the groups network of social interactions. Previous studies tend to look at a subset of dyadic interactions, focusing on particular classes of individuals. We used social network analysis to explore how an individual wild meerkats (Suricata suricatta) attributes related to their positions in three different interaction networks (grooming, dominance interactions, and foraging competitions) across eight groups. We asked whether individuals within groups associated assortatively and whether individuals with similar attributes occupied similar network positions. Differences in an individuals attributes did not consistently influence association patterns across different interaction network types. However, within network types, some attributes were especially influential across all groups. Grooming networks revealed negative assortativity by age and mass. Dominance networks revealed dominant–subordinate associations and high assortativity between males. Dominant individuals exhibited higher levels of dominance interactions and were aggressive to more different individuals than subordinates. Heavier individuals received higher levels of dominance interactions. Foraging competition networks revealed that younger and lighter individuals received higher overall levels of competitions and from more group members. Our observations were similar to focused studies on dyadic interactions but also revealed subtle differences. Future descriptions of social interactions should account for networks of social interactions occurring within a group and should be cautious about treating individuals with similar attributes as functionally similar with respect to their position within a social network.

Diagnostic Accuracy and Optimal Use of Three Tests for Tuberculosis in Live Badgers

Background Accurate diagnosis of tuberculosis (TB) due to infection with Mycobacterium bovis is notoriously difficult in live animals, yet important if we are to understand the epidemiology of TB and devise effective strategies to limit its spread. Currently available tests for diagnosing TB in live Eurasian badgers (Meles meles) remain unvalidated against a reliable gold standard. The aim of the present study was to evaluate the diagnostic accuracy and optimal use of three tests for TB in badgers in the absence of a gold standard. Methodology/Principal Findings A Bayesian approach was used to evaluate the diagnostic accuracy and optimal use of mycobacterial culture, gamma-interferon assay and a commercially available serological test using multiple samples collected from 305 live wild badgers. Although no single test was judged to be sufficiently sensitive and specific to be used as a sole diagnostic method, selective combined use of the three tests allowed guidelines to be formulated that allow a diagnosis to be made for individual animals with an estimated overall accuracy of 93% (range: 75% to 97%). Employing this approach in the study population of badgers resulted in approximately 13 out of 14 animals having their true infection status correctly classified from samples collected on a single capture. Conclusions/Significance This method of interpretation represents a marked improvement on the current procedure for diagnosing M. bovis infection in live badgers. The results should be of use to inform future test and intervention strategies with the aim of reducing the incidence of TB in free-living wild badger populations.