Erratum to: Using multistate capture–mark–recapture models to quantify effects of predation on age-specific survival and population growth in black-tailed deer

Effective species management and conservation relies on accurate estimates of vital rates and an understanding of their link to environmental variables. We used multistate capture–mark–recapture models to directly quantify effects of predation on age-specific survival of black-tailed deer Odocoileus hemionus columbianus in California, USA. Survival probabilities were derived from individual encounter histories of 136 fawns and 57 adults monitored over 4 years. Based on results from our survival analysis we parameterized a Lefkovitch matrix and used elasticity analyses to investigate contributions of mortality due to predation to changes in population growth. We found strong evidence for age-specific survival including senescence. Survival of females >1 year old was consistently low (0.56 ± 0.18 for yearlings, 0.77 ± 0.13 for prime-aged females, and 0.55 ± 0.08 for senescent individuals), primarily due to high puma Puma concolor predation during summer. Predation from black bears Ursus americanus and coyotes Canis latrans was the primary cause for low annual survival of fawns (0.24 ± 0.16). Resulting estimates of population growth rates were indicative of a strongly declining population (λ = 0.82 ± 0.13). Despite high sensitivity to changes in adult survival, results from a lower-level elasticity analysis suggested that predation on fawns was the most significant individual mortality component affecting population decline. Our results provide a rare, direct link between predation, age-specific survival and the predicted population decline of a common ungulate species. The magnitude of predation was unexpected and suggests that ungulates in multi-predator systems struggle to cope with simultaneous reductions in survival probabilities from predators targeting different age classes.     

An improved procedure to estimate wolf abundance using non-invasive genetic sampling and capture–recapture mixture models

Non-invasive genetic sampling (NGS) is increasingly used to estimate the abundance of rare or elusive species such as the wolf (Canis lupus), which cannot be directly counted in forested mountain habitats. Wolf individual and familial home ranges are wide, potentially connected by long-range dispersers, and their populations are intrinsically open. Appropriate demographic estimators are needed, because the assumptions of homogeneous detection probability and demographic closeness are violated. We compiled the capture–recapture record of 418 individual wolf genotypes identified from ca. 4,900 non-invasive samples, collected in the northern Italian Apennines from January 2002 to June 2009. We analysed this dataset using novel capture–recapture multievent models for open populations that explicitly account for individual detection heterogeneity (IDH). Overall, the detection probability of the weakly detectable individuals, probably pups, juveniles and migrants (P = 0.08), was ca. six times lower than that of the highly detectable wolves (P = 0.44), probably adults and dominants. The apparent annual survival rate of weakly detectable individuals was lower (Φ = 0.66) than those of highly detectable wolves (Φ = 0.75). The population mean annual finite rate of increase was λ = 1.05 ± 0.11, and the mean annual size ranged from N = 117 wolves in 2003 to N = 233 wolves in 2007. This procedure, combining large-scale NGS and multievent IDH demographic models, provides the first estimates of abundance, multi-annual trend and survival rates for an open large wolf population in the Apennines. These results contribute to deepen our understanding of wolf population ecology and dynamics, and provide new information to implement sound long-term conservation plans.     

Genetic mark–recapture population estimation in black bears and issues of scale

Abundance estimates for black bears (Ursus americanus) are important for effective management. Recently, DNA technology has resulted in widespread use of noninvasive, genetic capture–mark–recapture (CMR) approaches to estimate populations. Few studies have compared the genetic CMR methods to other estimation methods. We used genetic CMR to estimate the bear population at 2 study sites in northern New Hampshire (Pittsburg and Milan) in 2 consecutive years. We compared these estimates to those derived from traditional methods used by the New Hampshire Fish and Game Department (NHFG) using hunter harvest and mortality data. Density estimates produced with genetic CMR methods were similar both years and were comparable to those derived from traditional methods. In 2006, the estimated number of bears in Pittsburg was 79 (95% CI = 60–98) corresponding to a density of 15–24 (95% CI) bears/100 km²; the 2007 estimate was 83 (95% CI = 67–99; density = 16–24 bears/100 km²). In 2006, the estimated number of bears in Milan was 95 (95% CI = 74–117; density = 16–25 bears/100 km²); the 2007 estimate was 96 (95% CI = 77–114; density = 17–25 bears/100 km²). We found that genetic CMR methods were able to identify demographic variation at a local scale, including a strongly skewed sex ratio (2 M:1 F) in the Milan population. Genetic CMR is a useful tool for wildlife managers to monitor populations of local concern, where abundance or demographic characteristics may deviate from regional estimates. Future monitoring of the Milan population with genetic CMR is recommended to determine if the sex ratio bias continues, possibly warranting a change in local harvest regimes. © 2011 The Wildlife Society.     

Detecting femur–insert collisions to improve precision of fluoroscopic knee arthroplasty analysis

Fluoroscopic analysis is an important tool for assessing in vivo kinematics of knee prostheses. Most commonly, a single-plane fluoroscopic setup is used to capture the motion of prostheses during a particular task. Unfortunately, single-plane fluoroscopic analysis is imprecise in the out-of-plane direction. This can result in reconstructing physically impossible poses, in which—for example—the femoral component intersects with the insert, as the normal pose estimation process does not take into account the relation between the components. In the proposed method, the poses of both components are estimated simultaneously, while preventing femur–insert collisions. In a phantom study, the accuracy and precision of the new method in estimating the relative pose of the femoral component were compared to those of the original method. With reverse engineered models, the errors in estimating the out-of-plane position decreased from 2.0±0.7 to 0.1±0.1 mm, without effects on the errors in rotations and the in-plane positions. With CAD models, the errors in estimating the out-of-plane position decreased from 5.3±0.7 mm (mean±SD) to 0.0±0.4 mm, at the expense of a decreased precision for the other position or orientation parameters. In conclusion, collision detection can prevent reconstructing impossible poses and it improves the position and motion estimation in the out-of-plane direction.     

Bayesian latent class models for capture–recapture in the presence of missing data

We propose a method for estimating the size of a population in a multiple record system in the presence of missing data. The method is based on a latent class model where the parameters and the latent structure are estimated using a Gibbs sampler. The proposed approach is illustrated through the analysis of a data set already known in the literature, which consists of five registrations of neural tube defects.     

Estimating multiple years,tributary-specific,and overall Atlantic salmon smolt abundance in a large Canadian catchment using capture–mark–recapture experiments

Population monitoring of Atlantic salmon (Salmo salar L.) abundance is an essential element to understand annual stock variability and inform fisheries management processes. Smolts are the life stage marking the transition from the freshwater to the marine phase of anadromous Atlantic salmon. Estimating smolt abundance allows for subsequent inferences on freshwater and marine survival rates. Annual abundances of out-migrating Atlantic salmon smolts were estimated using Bayesian models and an 18-year capture–mark–recapture time series from two to five trapping locations within the Restigouche River (Canada) catchment. Some of the trapping locations were at the outlet of large upstream tributaries, and these sampled a portion of the total out-migrating population of smolts for the watershed, whereas others were located just above the head of tide of the Restigouche River and sampled the entire run of salmon smolts. Due to logistic and environmental conditions, not all trapping locations were operational each year. Additionally, recapture rates were relatively low (<5%), and the absolute number of recaptures was relatively few (most often a few dozen), leading to incoherent and highly uncertain estimates of tributary-specific and whole catchment abundance estimates when the data were modeled independently among trapping locations and years. Several models of increasing complexity were tested using simulated data, and the best-performing model in terms of bias and precision incorporated a hierarchical structure among years on the catchability parameters and included an explicit spatial structure to account for the annual variations in the number of sampled locations within the watershed. When the best model was applied to the Restigouche River catchment dataset, the annual smolt abundance estimates varied from 250,000 to 1 million smolts, and the subbasin estimates of abundance were consistent with the spatial structure of the monitoring programme. Ultimately, increasing the probabilities of capture and the absolute number of recaptures at the different traps will be required to improve the precision and reduce the bias of the estimates of smolt abundance for the entire basin and within subbasins of the watershed. The model and approach provide a significant improvement in the models used to date based on independent estimates of abundance by trapping location and year. Total abundance and relative production in discrete spawning, nesting, or rearing areas provide critical information to appropriately understand and manage the threats to species that can occur at subpopulation spatial scales.     

Mapping the protein–protein and genetic interactions of cancer to guide precision medicine

Massive efforts to sequence cancer genomes have compiled an impressive catalogue of cancer mutations, revealing the recurrent exploitation of a handful of ‘hallmark cancer pathways’. However, unraveling how sets of mutated proteins in these and other pathways hijack pro-proliferative signaling networks and dictate therapeutic responsiveness remains challenging. Here, we show that cancer driver protein–protein interactions are enriched for additional cancer drivers, highlighting the power of physical interaction maps to explain known, as well as uncover new, disease-promoting pathway interrelationships. We hypothesize that by systematically mapping the protein–protein and genetic interactions in cancer—thereby creating Cancer Cell Maps—we will create resources against which to contextualize a patient’s mutations into perturbed pathways/complexes and thereby specify a matching targeted therapeutic cocktail.     

A comparison of mark–release–recapture methods for estimating colony size in the wood ant Formica lugubris

Colony size can be considered the analogue of the body size of a superorganism. Just as body size is important to the physiology of an individual animal, colony size correlates with the life-history and ecology of social insects. Although nest excavation and counting all individuals is the most accurate method for estimating colony size (or nest size), it has the major drawback of being destructive. Alternatively, mark–release–recapture (MRR) can be used repeatedly to measure the size of the same colony or nest. We compared the accuracy and feasibility of four MRR methods and a Mound-Volume method with complete counts from nest excavation for estimating the nest size of F. lugubris, a mound-building wood ant of the Formica rufa group, during the early spring in Scotland. We found that our After-Disturbing method, in which we performed marking and recapturing after gentle disturbance to the top of nest mound, has the best balance between accuracy, non-destructiveness, and time required. We also found that mound volume can be an index of ant nest size under certain conditions. Both non-destructive methods can be used on the same colony or nest repeatedly to monitor nest dynamics.     

Non-lethal method of DNA sampling in euglossine bees supported by mark–recapture experiments and microsatellite genotyping

Non-lethal sampling methods are of great interest for conservation genetic studies to prevent the death of individuals in populations that are threatened or in decline. With this aim, we tested a non-lethal method of partial antennae removal for DNA sampling in two euglossine bee species: Euglossa cordata and Eulaema nigrita. We validated the survival of the individuals through mark–recapture experiments during 16 months. The quality and quantity of the tissue for DNA analysis was verified through amplification and genotyping of nine and eleven microsatellite loci, respectively. Our results from the mark–recapture experiments showed equal recapture rates of individuals with intact and removed antennae (E. cordata χ² = 2.492, df = 1, p = 0.114; E. nigrita χ² = 1.683, df = 1, p = 0.194). Microsatellite loci were successfully genotyped in 97.1 and 97.6 % of the E. cordata and E. nigrita individuals, respectively. Our results validate the feasibility of using antennae tissue for DNA genetic analysis without compromising the survival of individual bees.     

Monitoring population size of mammals using a spotlight-count-based abundance index: How to relate the number of counts to the precision?

Abundance indices are widely used to study changes in population size in wildlife management. However, a truly appropriate measure of precision is often lacking in such studies. Statistically, the two crucial issues regarding the use of an abundance index are sampling and observability, which lead one to consider two kinds of errors, namely sampling and observation errors. The purpose of this methodological paper is to relate the number of counts to the precision of an abundance index by introducing the Hansen–Hurwitz–Bershad model which takes into account both sampling and observation errors. We illustrate this statistical approach in the case of a European rabbit (Oryctolagus cuniculus) abundance index based on spotlight counts, for two fixed spatial sampling units located in different ecological contexts. We show (i) that the usual sampling variance estimator is a downward-biased estimator of the total variance of the abundance index, (ii) that the bias of the usual variance estimator does not decrease when increasing the sampling size, (iii) that correlated observation errors may have a dramatic impact on the total variance, especially when the sampling size increases. The acknowledgement that the (pure) sampling variance underestimates the total variance because of observation errors is a statistical result that is neither widely known nor appreciated by most wildlife ecologists. The magnitude of this underestimation may be important and, therefore, observation errors cannot be always considered as a priori negligible in assessing the precision of a count-based abundance index.     

Estimating local population size of the European Nightjar Caprimulgus europaeus using territory capture–recapture models

Capsule The capture–recapture model M(o) is an efficient way to estimate local population size.

Aims To test if a single capture–recapture modelling approach, combined with a simple survey method, can produce estimates of local population size from a dataset involving large‐scale multi‐observer surveys

Methods We sampled the presence of Nightjars in three separate sessions at three forests. Territory numbers were estimated using conventional territory‐mapping criteria. We ran different capture–recapture models to analyse the detection histories of territories obtained across the three sampling sessions and in the three different forests, using either only registrations of churring birds or all contacts.

Results The capture–recapture model M(o), assuming a constant detection probability, was the most efficient one to produce estimates of local population size. Using only two of the three sampling sessions gave less precise, though quite similar, estimates of the number of territories, with standard deviations representing 5–10% of the estimate values. However, this was reduced to 0.7–3.5%, i.e. three to seven times lower, when using the three sessions.

Conclusion Repeated sampling sessions to map territories can be efficiently used within the capture–recapture model M(o) to estimate detection probability and produce precise estimates of local population size.     

Can measures of prey availability improve our ability to predict the abundance of large marine predators?

Apex marine predators can structure marine communities, so factors underlying their abundance are of broad interest. However, such data are almost completely lacking for large sharks. We assessed the relationship between tiger shark abundance, water temperature, and the availability of a variety of known prey over 5 years in Western Australia. Abundance of sharks in four size categories and the density of prey (cormorants, dugongs, sea snakes, sea turtles) were indexed using daily catch rates and transects, respectively. Across all sizes, thermal conditions were a determinant of abundance, with numerical peaks coinciding with periods of high water temperature. However, for sharks exceeding 300 cm total length, the inclusion of dugong density significantly improved temperature-based models, suggesting that use of particular areas by large tiger sharks is influenced by availability of this sirenian. We conclude that large marine predator population models may benefit from the inclusion of measures of prey availability, but only if such measures consider prey types separately and account for ontogenetic shifts in the diet of the predator in question. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Prediction of marine species distribution from presence–absence acoustic data: comparing the fitting efficiency and the predictive capacity of conventional and novel distribution models

The accurate representation of species distribution derived from sampled data is essential for management purposes and to underpin population modelling. Additionally, the prediction of species distribution for an expanded area, beyond the sampling area can reduce sampling costs. Here, several well-established and recently developed habitat modelling techniques are investigated in order to identify the most suitable approach to use with presence–absence acoustic data. The fitting efficiency of the modelling techniques are initially tested on the training dataset while their predictive capacity is evaluated using a verification set. For the comparison among models, Receiver Operating Characteristics (ROC), Kappa statistics, correlation and confusion matrices are used. Boosted Regression Trees (BRT) and Associative Neural Networks (ASNN), which are both within the machine learning category, outperformed the other modelling approaches tested.     

Integrating topics of sex and gender into medical curricula—lessons from the international community

In the era of individualized medicine, training future scientists and health-care providers in the principles of sex- and gender-based differences in health and disease is critical in order to optimize patient care. International successes to incorporate these concepts into medical curricula can provide a template for others to follow. Methodologies and resources are provided that can be adopted and adapted to specific needs of other institutions and learning situations.     

Parasitoid-mediated effects: apparent competition and the persistence of host–parasitoid assemblages

Indirect effects such as apparent competition (in which two hosts that do not compete for resources interact via a shared natural enemy) are increasingly being shown to be prevalent in the structure and function of ecological assemblages. Here, we review the empirical and theoretical evidence for these enemy-mediated effects in host–parasitoid assemblages. We first address questions about the design of experiments to test for apparent competition. Second, we consider factors likely to affect the coexistence of host species that share a parasitoid and are involved in apparent competition. We show that parasitoid aggregation, and the switching effect that this can generate when hosts occur in separate patches, not only promotes persistence but is also strongly stabilizing. The broader consequences of these effects are discussed. Received: November 6, 1998 / Accepted: January 13, 1999     

Influence of relative NK–DC abundance on placentation and its relation to epigenetic programming in the offspring

Normal placentation relies on an efficient maternal adaptation to pregnancy. Within the decidua, natural killer (NK) cells and dendritic cells (DC) have a critical role in modulating angiogenesis and decidualization associated with pregnancy. However, the contribution of these immune cells to the placentation process and subsequently fetal development remains largely elusive. Using two different mouse models, we here show that optimal placentation and fetal development is sensitive to disturbances in NK cell relative abundance at the fetal–maternal interface. Depletion of NK cells during early gestation compromises the placentation process by causing alteration in placental function and structure. Embryos derived from NK-depleted dams suffer from intrauterine growth restriction (IUGR), a phenomenon that continued to be evident in the offspring on post-natal day 4. Further, we demonstrate that IUGR was accompanied by an overall reduction of global DNA methylation levels and epigenetic changes in the methylation of specific hepatic gene promoters. Thus, temporary changes within the NK cell pool during early gestation influence placental development and function, subsequently affecting hepatic gene methylation and fetal metabolism.Maternal adaptations to pregnancy are critical during mammalian development. Cumulative evidence suggests that immune-competent cells in the developing decidua are important for placental development and embryo survival. For instance, the cross-talk between natural killer (NK) cells and dendritic cells (DC) during early pregnancy has emerged as a key regulator of angiogenesis and decidualization,^{1, 2} both of which are critical events for normal placentation. In this context, we have shown that NK cells prevent the development of alloimmunity during normal pregnancy by modulating the immune-regulatory functions of DC during early gestation.^{2, 3} Furthermore, unbalanced relative NK cell abundance (i.e., upon in vivo NK cell depletion following fms-like tyrosine kinase 3 ligand (FL)-mediated DC expansion) upregulated the expression of anti-angiogenic growth factors, suggesting that NK cells are required for early vascular responses associated with pregnancy. Indeed, NK cells regulate the remodeling of maternal spiral arteries, transforming them from low capacity high resistance into high capacity low resistance vessels.⁴ As for DC, these cells not only influence maternal immune tolerance to fetal alloantigens,³ but also coordinate pregnancy-associated vascular adaptations including vessel permeability and blood flow to the implantation site via the CXCL12/CXCR4 pathway.^{1, 5}The placenta is the key organ supporting the survival and growth of the fetus during gestation. It constitutes an interface between the maternal and fetal circulations, allowing nutrient uptake, waste elimination and metabolic/gas exchange.⁶ In mice, placental development begins early in the blastocyst (embryonic day E3.5) and continues to show dramatic changes throughout gestation. The mouse placenta consists of three layers: the labyrinth (comprising highly branched villi that maximize nutrient transport), the junction zone (containing trophoblast giant cells and spongiotrophoblast cells that invade the decidua and maternal vessels) and the maternal decidua (including immune and decidual cells and the maternal vasculature).⁷ Inadequate differentiation of these layers leads to detrimental changes in placental architecture, which affect the supply of nutrients or oxygen to the fetus. Faulty placental development has been implicated in the pathophysiology of several human pregnancy disorders, including preeclampsia, intrauterine growth restriction (IUGR) and preterm labor.⁷ In this context, it is likely that the fetus adapts to the pathological situation by modifying its energy metabolism in order to sustain development and continue pregnancy.Changes in fetal metabolism are thought to occur via epigenetic modification of mitochondrial gene expression patterns, causing changes in mitochondrial number or function.^{8, 9} Indeed, animal models of IUGR have shown a reduction in mitochondrial DNA (mtDNA) content, accompanied by reduced expression of mtDNA encoded genes and epigenetic changes in fetal growth factors (e.g., insulin-like growth factor I (IgfI) and IgfII). In addition, many studies have suggested a role for nuclear receptors in the observed fetal metabolic adaptations toward adverse conditions in utero. These include receptors and associated coactivators, such as the peroxisome proliferator-activated receptor alpha (Pparα), peroxisome proliferator-activated receptor gamma coactivator 1 alpha (Pgc1α), hepatocyte nuclear factor 4 alpha (Hnf4α) and the glucocorticoid receptor (Nr3c1).⁸ During adaptation to restricted fetal development, modifications to nuclear receptors act to optimize growth and differentiation. In a process called fetal programming, these modifications can persist through adulthood possibly contributing to the observed increase in late-onset disorders at an adult age.^{10, 11}As the cross-talk between NK cells and DC influences both decidualization and angiogenesis, in this work we analyzed how in vivo manipulation of relative DC–NK cell abundance within the decidua impacts the placentation process and subsequently fetal development. We show that although manipulation of the relative abundance of DC and NK cells in early gestation does not seem to compromise fetal survival, both placental function and structure are specifically altered compared with control mice. Using a candidate gene approach, we demonstrate that these structural changes in the placenta are associated with epigenetic changes in the methylation of specific hepatic gene promoters in pups principally after NK cell depletion. The gene-specific changes were further accompanied by an overall reduction of global DNA methylation levels. Our data confirm that temporary changes within the NK and/or the DC pool during early gestation influence placental development and function, subsequently affecting hepatic gene methylation and fetal metabolism.