Spatial proximity loggers for recording animal social networks: consequences of inter-logger variation in performance

Social network analysis has become an increasingly popular method to link individual behaviour to population level patterns (and vice versa). Technological advances of recent years, such as the development of spatial proximity loggers, have enhanced our abilities to record contact patterns between animals. However, loggers are often deployed without calibration which may lead to sampling biases and spurious results. In particular, loggers may differ in their performance (i.e., some loggers may over-sample and other loggers may under-sample social associations). However, the consequences of inter-logger variation in logging performance has not been thoroughly considered or quantified. In this study, proximity loggers made by Sirtrack Ltd. were fitted to 20 dairy cows over a 3-week period. Contact records resulting from field deployment demonstrated variability in logger performance when recording contact duration, which was highly consistent for each logger over time. Testing loggers under standardised conditions suggested that inter-logger variation observed in the field was due to a combination of intrinsic variation in devices, and environmental/behavioural effects. We demonstrate the potential consequences that inter-logger variation in logging performance can have for social network analysis; particularly how measures of connectivity can be biased by logging performance. Finally, we suggest some approaches to correct data generated by proximity loggers with imperfect performance, that should be used to improve the robustness of future analyses.     

Spatial and temporal heterogeneities in the contact behaviour of rabbits

It is becoming increasingly evident that the social behaviour of many group-living species is more complex than previously assumed and that free mixing of individuals, even within social groups, is rare. This has important implications for ecological processes, such as disease transmission, which are dependent on interactions between individuals. European wild rabbits (Oryctolagus cuniculus) have been considered traditionally as highly sociable animals that mix freely within groups but interact less frequently between groups. We deployed proximity logging devices to quantify the intra- and inter-group contact behaviour of free-living wild rabbits in two populations in a temperate region of Australia. Altogether, 126 rabbits were fitted with proximity loggers at least once during the study. Radio-tracking was carried out alongside proximity data collection to determine the space use of rabbit social groups within the study sites. On average, a rabbit made only 1.54 ± 0.23 (SE) (median = 0.54) contacts per day with each other rabbit carrying a proximity logger in its social group, and the mean daily contact duration was 202 ± 38 s/day (SE) (median = 29 s). Despite the high degree of home range overlap between the neighbouring social groups, inter-group contacts were highly infrequent and brief. Our results demonstrated considerable spatial and temporal heterogeneities in the contact behaviour between individual rabbits, both between populations and between and within social groups in the same population. Such variations in the social organisation of rabbits are likely to create complex patterns of disease transmission through direct contact and may contribute towards observed heterogeneities in the effects of disease on wild rabbit populations.     

Rarefaction and nonrandom spatial dispersion patterns

Rarefaction estimates how many species are expected in a random sample of individuals from a larger collection and allows meaningful comparisons among collections of different sizes. It assumes random spatial dispersion. However, two common dispersion patterns, within-species clumping and segregation among species, can cause rarefaction to overestimate the species richness of a smaller continuous area. We use field studies and computer simulations to determine (1) how robust rarefaction is to nonrandom spatial dispersion and (2) whether simple measures of spatial autocorrelation can predict the bias in rarefaction estimates. Rarefaction does not estimate species richness accurately for many communities, especially at small sample sizes. Measures of spatial autocorrelation of the more abundant species do not reliably predict amount of bias. Survey sites should be standardized to equal-sized areas before sampling. When sites are of equal area but differ in number of individuals sampled, rarefaction can standardize collections. When communities are sampled from different-sized areas, the mean and confidence intervals of species accumulation curves allow more meaningful comparisons among sites. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.

GPS tracking a marine predator: the effects of precision,resolution and sampling rate on foraging tracks of African Penguins

We used a prototype GPS logger to track the movements of breeding African Penguins (Spheniscus demersus). The loggers also recorded temperature and water depth, which allowed us to reconstruct foraging tracks in three dimensions, although GPS signals are interrupted when the birds dive. Here we report the loggers performance in the field and assess the effects of GPS error, resolution and sampling rate on estimates of foraging track length and speed. There is a trade-off between sampling rate and battery lifespan. We tested loggers at sampling intervals of 1 s, 10 s, 1 min, 2 min and 10 min. Sampling less frequently increases the chance of tracking an entire foraging trip, but it slows uplink times, slightly decreases the accuracy of positional fixes, and significantly reduces the ability to measure fine-scale aspects of foraging behaviour. Compared with radio or satellite tracking, GPS loggers offer unprecedented detail about animal movements. The results of our analysis suggest that techniques that sample relatively infrequently, such as satellite tracking, underestimate actual track lengths by up to 50%. However, caution is needed when interpreting fine-scale sampling for relatively slow-moving organisms. Re-sampling 1-s tracks suggests that c. 35% of apparent movements at this scale are due to measurement error and, more importantly, the limited spatial resolution of GPS (1.85×1.54 m at the study area). We recommend that researchers use a 1-s sampling rate for fine-scale studies, but resample at less frequent intervals to remove spurious noise for slow-moving animals. At current levels of resolution, animals should move at least 4 m per sampling interval. We provide empirical correction factors to compare inferred track length sampled at different rates, but caution that these are idiosyncratic and strongly dependent on the animals behaviour. Overall, GPS loggers offer a significant advance for studies of fine-scale animal movement patterns.Communicated by O. Kinne, Oldendorf/Luhe     

The social network structure of a wild meerkat population: 2. Intragroup interactions

Knowledge of the structure of networks of social interactions is important for understanding the evolution of cooperation, transmission of disease, and patterns of social learning, yet little is known of how environmental, ecological, or behavioural factors relate to such structures within groups. We observed grooming, dominance, and foraging competition interactions in eight groups of wild meerkats (Suricata suricatta) and constructed interaction networks for each behaviour. We investigated relationships between networks for different social interactions and explored how group attributes (size and sex ratio), individual attributes (tenure of dominants), and ecological factors (ectoparasite load) are related to variation in network structure. Network structures varied within a group according to interaction type. Further, network structure varied predictably with group attributes, individual attributes, and ecological factors. Networks became less dense as group size increased suggesting that individuals were limited in their number of partners. Groups with more established dominant females were more egalitarian in their grooming and foraging competition interactions, but more despotic in their dominance interactions. The distribution of individuals receiving grooming became more skewed at higher parasite loads, but more equitable at low parasite loads. We conclude that the pattern of interactions between members of meerkat groups is not consistent between groups but instead depends on general attributes of the group, the influence of specific individuals within the group, and ecological factors acting on group members. We suggest that the variation observed in interaction patterns between members of meerkat groups may have fitness consequences both for individual group members and the group itself.     

Vigilance and aggregation in black howler monkeys (Alouatta pigra)

Animals are expected to reduce per capita vigilance with increasing group size. Widespread support for this expectation has been found in studies of birds and ungulates. Primate vigilance patterns appear to differ, but studies of primates may have sampled groups with too many members to detect intergroup differences in vigilance. We tested this idea by measuring individual vigilance rates in wild black howler monkeys (Alouatta pigra) living in stable groups of two to ten individuals. No group size effect on vigilance emerged. As in previous studies, inter-individual proximity explained variation in individual vigilance rates. Focal animals with associates within 2 m and with multiple associates in the same tree were less vigilant than isolated animals. Activity and class of focal animals as well as the presence of neonates influenced the average vigilance of adult and subadult black howler monkeys. We conclude that functional explanations must be considered for the general lack of a group size effect on primate vigilance.     

Inferring evolutionary signals from ecological data in a plant-pathogen metapopulation

We followed the dynamics of local epidemics in three populations of a natural plant-pathogen system for four sequential years. We characterize the overwintering process with spatial statistics and use a stochastic, spatially explicit, modeling approach with Bayesian parameter estimation to study the spread of the infection during the growing season. Our modeling approach allows us to infer coevolutionary signals from spatiotemporal data on pathogen prevalence. Most importantly, we are able to assess the distribution of resistant hosts within the distribution of all host plants. We show that resistant hosts occur in areas with high pathogen encounter rates, and that the occurrence of resistance correlates with overwintering probability of the pathogen. The estimates for essentially all model parameters are characterized by a large amount of variation over the years and the populations. While the variation in the fraction of resistant hosts and in the force of infection is to a large extent explained by the population, the other model parameters (two parameters describing the shape of the dispersal kernel) vary essentially in an unpredictable manner, suggesting that much of the variation may occur at very fine spatial and temporal scales.     

Estimating an homogeneous series of a population abundance indicator despite changes in data collection procedure: A hierarchical Bayesian modelling approach

Abundance indicators are required both to assess and to manage wild populations. As new techniques are developed and teams in charge of gathering the data change, data collection procedures (DCPs) can evolve in space and time. How to estimate an homogeneous series of abundance indicator despite changes in DCP? To tackle this question a hierarchical Bayesian modelling (HBM) approach is proposed. It integrates multiple DCPs in order to derive a single abundance indicator that can be compared over space and time irrespective of the DCP used. Compared to single DCP models, it takes further advantage for abundance estimation of the joint treatment of a larger set of spatio-temporal units. After presenting the general formulation of our HBM approach, it is applied to the juvenile Atlantic salmon (Salmo salar L.) population of the River Nivelle (France). Posterior model checking, using χ² discrepancy measure, do not reveal any inadequacy between the model and the data. Despite a change in the DCP used (successive removals to catch-per-unit of effort), a unique abundance indicator for the 425 spatio-temporal units (site × year) sampled over twenty-four years (1985-2008) is estimated. The HBM approach allows the assessment of precision of the abundance estimates and shows variation between DCPs: a reduction in precision is observed during the most recent years (2005-2008) when only the catch-per-unit of effort DCP was used. The merits and generality of our HBM approach are discussed. We contend it extends previous single DCP models or inter-calibration of two DCPs, and it could be applied to a wide range of specific situations (taxon and DCPs).     

An integrated model of regional and local residential sorting with application to air quality

We examine the interconnectedness of demand for regionally and locally varying public goods using a residential sorting model. We propose a version of the model that describes household choices at the city (MSA) level and, conditional on city, the neighborhood (census tract) level. We use a two-stage budgeting argument to develop an empirically feasible sorting model that allows us to estimate preferences for regionally varying air quality while accounting for sorting at the local level. Our conceptual and empirical approach nests previous sorting models as special cases, allowing us to assess the importance of accounting for multiple spatial scales in our predictions for the cost of air pollution. Furthermore our preferred specification connects the city and neighborhood sorting margins to the upper and lower elements of a nested logit model, thereby establishing a useful correspondence between two stage budgeting and nested logit estimation. Empirically we find that estimates from a conventional model of sorting across MSAs imply a smaller marginal willingness to pay for air quality than estimates from our proposed model. We discuss how the difference is attributable in part to the omitted variable problems arising when tract level sorting is ignored.     

Structure of the social network and its influence on transmission dynamics in a honeybee colony

Infectious processes in a social group are driven by a network of contacts that is generally structured by the organization arising from behavioral and spatial heterogeneities within the group. Although theoretical models of transmission dynamics have placed an overwhelming emphasis on the importance of understanding the network structure in a social group, empirical data regarding such contact structures are rare. In this paper, I analyze the network structure and the correlated transmission dynamics within a honeybee colony as determined by food transfer interactions and the changes produced in it by an experimental manipulation. The study demonstrates that widespread transmission in the colony is correlated to a lower clustering coefficient and higher robustness of the social network. I also show that the social network in the colony is determined by the spatial distribution of various age classes, and the resulting organizational structure provides some amount of immunity to the young individuals. The results of this study demonstrates how, using the honeybee colony as a model system, concepts in network theory can be combined with those in behavioral ecology to gain a better understanding of social transmission processes, especially those related to disease dynamics.     

Estimating parameters of neutral communities: from one single large to several small samples

The neutral theory of S. P. Hubbell postulates a two-scale hierarchical framework consisting of a metacommunity following the speciation-drift equilibrium characterized by the "biodiversity number" theta, and local communities following the migration-drift equilibrium characterized by the "migration rate" m (or the "fundamental dispersal number" I). While Etienne's sampling formula allows simultaneous estimation of theta and m from a single sample of a local community, its applicability to a network of (rather small) samples is questionable. We define here an alternative two-stage approach estimating theta from an adequate subset of the individuals sampled in the field (using Ewens' sampling formula) and m from community samples (using Etienne's sampling formula). We compare its results with the simultaneous estimation of theta and m (one-stage estimation), for simulated neutral samples and for 50 1-ha plots of evergreen forest in South India. The one-stage approach exhibits problems of bias and of poor differentiability between high-theta, low-m and low-theta, high-m solution domains. Conversely, the two-stage approach yielded reasonable estimates and is to be preferred when several small, scattered plots are available instead of a single large one.     

Evaluating the sampling pattern when detecting Zones of Abrupt Change

We present a method for detecting the zones where an irregularly sampled variable changes abruptly in the plane. Such zones are called Zones of Abrupt Change (ZACs). This method not only allows estimation of ZACs, but also testing of their statistical significance against the null hypothesis of a stationary correlated random field. The sampling pattern, in particular its local density, is crucial in the detection of potential ZACs. In this paper, we address the problem of evaluating the sampling pattern by assessing the power of the local test used for detecting ZACs. It is shown that mapping the power allows us to identify zones where ZACs may or may not be detected. The methodology is applied to a soil data set sampled at eight different dates in an agricultural field. Detecting ZACs for the soil water content allowed us to identify permanent structures in the agricultural field related to the boundaries between different soil types. Mapping the power for various sampling densities proved to be useful to determine the minimal sampling density necessary for detecting ZACs.

A Graph-Theory Framework for Evaluating Landscape Connectivity and Conservation Planning

Abstract:  Connectivity of habitat patches is thought to be important for movement of genes, individuals, populations, and species over multiple temporal and spatial scales. We used graph theory to characterize multiple aspects of landscape connectivity in a habitat network in the North Carolina Piedmont (U.S.A).^. We compared this landscape with simulated networks with known topology, resistance to disturbance, and rate of movement. We introduced graph measures such as compartmentalization and clustering, which can be used to identify locations on the landscape that may be especially resilient to human development or areas that may be most suitable for conservation. Our analyses indicated that for songbirds the Piedmont habitat network was well connected. Furthermore, the habitat network had commonalities with planar networks, which exhibit slow movement, and scale-free networks, which are resistant to random disturbances. These results suggest that connectivity in the habitat network was high enough to prevent the negative consequences of isolation but not so high as to allow rapid spread of disease. Our graph-theory framework provided insight into regional and emergent global network properties in an intuitive and visual way and allowed us to make inferences about rates and paths of species movements and vulnerability to disturbance. This approach can be applied easily to assessing habitat connectivity in any fragmented or patchy landscape.     

Nonparametric spatial regression of survival probability: visualization of population sinks in Eurasian woodcock

Both evolutionary ecologists and wildlife managers make inference based on how fitness and demography vary in space. Spatial variation in survival can be difficult to assess in the wild because (1) multisite study designs are not well suited to populations that are continuously distributed across a large area and (2) available statistical models accounting for detectability less than 1.0 do not easily cope with geographical coordinates. Here we use penalized splines within a Bayesian state-space modeling framework to estimate and visualize survival probability in two dimensions. The approach is flexible in that no parametric form for the relationship between survival and coordinates need be specified a priori. To illustrate our method, we study a game species, the Eurasian Woodcock Scolopax rusticola, based on band recovery data (5000 individuals) collected over a > 50 000-km2 area in west-central France with contrasted habitats and hunting pressures. We find that spatial variation in survival probability matches an index of hunting pressure and creates a mosaic of population sources and sinks. Such analyses could provide guidance concerning the spatial management of hunting intensity or could be used to identify pathways of spatial variation in fitness, for example, to study adaptation to changing landscape and climate.     

Kinships in a natural meadow vole population

Summary We have devised a radionuclide technique that allows the assessment of matrilineal kinship by the transfer of unique combinations of gamma-emitting radionuclides from pregnant and lactating female meadow voles (Microtus pennsylvanicus) to their offspring. A pool of prospective fathers can be established from field records of reproductively active males that were alive at the time of conception of the female's litter. Electrophoresis of 6 proteins allowed us to eliminate genetically incompatible males from the prospective pool of fathers. A log-likelihood statistic provided an estimate of the probability of paternity. In the case of numerical ties physical proximity of the males to the mother at the time of conception was used. With these techniques, we established 40 kinships in a field population of meadow voles.     

The ties that bind: Inter-clonal cooperation may help a fragile coral dominate shallow high-energy reefs

In Belize, shallow fore-reef buttresses are dominated byAgaricia tenuifolia Dana. The ecological importance of this fragile coral in such a high-energy environment may be explained in part by an unusual cooperative interaction between adjacent clones ofA. tenuifolia. The shallow buttresses are often composed primarily of many clones ofA. tenuifolia growing in close proximity. Surveys conducted at Carrie Bow Cay, Belize, in 1986 and 1987 showed that intraspecific contacts between different clones are common and occur far more frequently than interspecific encounters with other sessile taxa. In contrast to many other corals, contacts between non-clonemates ofA. tenuifolia do not result in competitive interactions, tissue bleaching or death, or significantly altered patterns of colony growth. Instead, inter-clonal contact stimulates localized morphological changes in the skeletons of both corals directly beneath the contact interface, which tend to anchor the two corals against each other, making them more resistant to breakage and detachment. By mechanically stabilizing clusters of otherwise fragile corals, these cooperative interactions potentially enhance the long-term survivorship and hence the fitness of interactingA. tenuifolia clones.The views expressed here are those of the author and do not necessarily reflect those of the Office of Technology Assessment     

Temporary alteration of local social structure in a threatened population of Cuban iguanas (Cyclura nubila)

In small, insular populations, behavioral patterns that lead to increased variance in individual reproductive success can accelerate loss of genetic variation. Over a 1-year period, we documented behavior and hormone levels in a breeding group of adult Cuban iguanas (Cyclura nubila) at Guantánamo Bay. Male dominance was associated with body and head size, display behavior, testosterone levels, home-range size, and proximity to females. Based on their success in agonistic encounters, we ranked males in a linear dominance hierarchy. During the subsequent breeding season, we conducted a removal experiment in which the five highest-ranking males were temporarily relocated from the study site. Although we were unable to assess reproductive success directly, previously lower-ranking males assumed control of vacated territories, won more fights, and increased their proximity to females in the absence of the dominant males. When it results in greater mating opportunities for otherwise socially suppressed individuals, temporary alteration of local social structure may help limit erosion of genetic variation in small, insular populations. Electronic Publication     

Genetic Variation and the Immune Response in Natural Populations of Pocket Gophers

It is thought that genetic variation can affect the persistence of a population through its influence on disease susceptibility. We assessed genome-wide genetic variation, variation at a locus involved in the immune system, and acceptance or rejection of skin grafts in three natural populations of the pocket gopher ( Thomomys bottae ). Multilocus DNA fingerprints confirmed previous allozyme data, revealing high levels of variation among Hastings Reserve pocket gophers and almost complete within-population identity for individuals from the two Patricks Point populations (Patricks J and Patricks F), although Patricks J animals were dissimilar to animals from Patricks F despite their proximity. Individuals from the high-variation population consistently rejected within-population reciprocal skin grafts, whereas Patricks J and Patricks F individuals accepted within-population grafts. Patricks J and Patricks F individuals were found to be immunocompetent, however, as revealed by the ability of all individuals to reject between-population grafts, including those that previously accepted within-population grafts. A DNA heteroduplex analysis was then used to directly characterize variability at DQα, a locus of the immune system's major histocompatability complex. Both populations low in genetic variation were fixed for unique DQα alleles, whereas observed heterozygosity in the Hastings population was 0.43, ascribable to at least three unique alleles. These data are in accord with previous cheetah skin-graft results and confirm that skin grafts can be used to assess genetic similarity. We suggest that although many animal populations can persist with extremely low levels of genetic variation in the wild, such populations may be at a greater risk of extinction from particular pathogens because of their genetic uniformity.