Quantifying telemetry collar bias when age is unknown: A simulation study with a long-lived ungulate

Radiotelemetry collars are frequently used to estimate demographic parameters of animals, such as annual survival and parturition rates. If animals are collared for multiple years and statistical adjustments are not made, these estimates can be biased by an unrepresentative age structure and individual variability of collared animals. To quantify the effects of different factors on the magnitude of these potential biases, we created a computer simulation of the female portion of a barren-ground caribou (Rangifer tarandus granti) herd and then randomly assigned collars to individuals within the simulated population. Under our default model, based on the Western Arctic Herd monitoring program, caribou were collared randomly from all females aged 2 years and over, and they remained collared for a mean of 7 years. Our simulations revealed that survival rates were underestimated by approximately 3.4% and parturition rates were overestimated by approximately 3.3%. The magnitude of these biases increased when individuals remained collared for longer periods. Increased individual variability in the population resulted in only small increases in survival and parturition rates. Because the magnitude of the bias increased steadily during the first years of the study, we found a substantial risk of incorrectly identifying a significant decline in survival in the first 7 years after marking. Including the number of years individual animals have been collared as a covariate in analyses can reduce the biases in demographic parameters and should be considered for inclusion in analyses when animal age is unknown. Actual survival rate estimates from telemetry data for the Western Arctic Herd were generally consistent with the results of these simulations. These potential biases should be considered when interpreting demographic parameters from multi-year collaring studies. © 2012 The Wildlife Society.     

A Burning Question: What are the Implications of Forest Fires for Woodland Caribou?

Canada's federal recovery strategy for boreal woodland caribou (Rangifer tarandus caribou) classifies areas burned by forest fire as disturbed habitat. This assignment of fire as a disturbance has potential economic and social implications across Canada, and influences plans and actions to achieve caribou conservation and recovery. Previous researchers have reported caribou avoid burned habitat, but these studies did not typically consider unburned residual patches within fire perimeters. Additionally, the implications of burned habitat on individual caribou survival is unclear. We examined resource selection by boreal woodland caribou of burns, and unburned residual patches, using global positioning system (GPS) locations for 201 caribou across 6 caribou populations in Alberta, Canada. We also examined if burned habitat affected the survival of adult female caribou. Caribou avoided burns and unburned residual patches. Increased use of burned habitats, however, did not lower the survival of adult caribou. Collectively, these results provide evidence to support current assertions that burns, and the embedded unburned residual patches are not preferred caribou habitat and increase our understanding of the implications of forest fire for caribou vital rates. Our investigation offers important information about the role of forest fire in caribou ecology and enhances the identification of disturbed habitat under recovery strategy guidelines to effectively address caribou population declines. © 2021 The Wildlife Society.     

Divergent estimates of herd‐wide caribou calf survival: Ecological factors and methodological biases

Population monitoring is a critical part of effective wildlife management, but methods are prone to biases that can hinder our ability to accurately track changes in populations through time. Calf survival plays an important role in ungulate population dynamics and can be monitored using telemetry and herd composition surveys. These methods, however, are susceptible to unrepresentative sampling and violations of the assumption of equal detectability, respectively. Here, we capitalized on 55 herd‐wide estimates of woodland caribou (Rangifer tarandus caribou) calf survival in Newfoundland, Canada, using telemetry (n = 1,175 calves) and 249 herd‐wide estimates of calf:cow ratios (C:C) using herd composition surveys to investigate these potential biases. These data included 17 herd‐wide estimates replicated from both methods concurrently (n = 448 calves and n = 17 surveys) which we used to understand which processes and sampling biases contributed to disagreement between estimates of herd‐wide calf survival. We used Cox proportional hazards models to determine whether estimates of calf mortality risk were biased by the date a calf was collared. We also used linear mixed‐effects models to determine whether estimates of C:C ratios were biased by survey date and herd size. We found that calves collared later in the calving season had a higher mortality risk and that C:C tended to be higher for surveys conducted later in the autumn. When we used these relationships to modify estimates of herd‐wide calf survival derived from telemetry and herd composition surveys concurrently, we found that formerly disparate estimates of woodland caribou calf survival now overlapped (within a 95% confidence interval) in a majority of cases. Our case study highlights the potential of under‐appreciated biases to impact our understanding of population dynamics and suggests ways that managers can limit the influence of these biases in the two widely applied methods for estimating herd‐wide survival.     

Dynamic selection for forage quality and quantity in response to phenology and insects in an Arctic ungulate

Spatiotemporal variation in forage is a primary driver of ungulate behavior, yet little is known about the nutritional components they select, and how selection varies across the growing season with changes in forage quality and quantity. We addressed these uncertainties in barren‐ground caribou (Rangifer tarandus), which experience their most important foraging opportunities during the short Arctic summer. Recent declines in Arctic caribou populations have raised concerns about the influence of climate change on summer foraging opportunities, given shifting vegetation conditions and insect harassment, and their potential effects on caribou body condition and demography. We examined Arctic caribou selection of summer forage by pairing locations from females in the Central Arctic Herd of Alaska with spatiotemporal predictions of biomass, digestible nitrogen (DN), and digestible energy (DE). We then assessed selection for these nutritional components across the growing season at landscape and patch scales, and determined whether foraging opportunities were constrained by insect harassment. During early summer, at the landscape scale, caribou selected for intermediate biomass and high DN and DE, following expectations of the forage maturation hypothesis. At the patch scale, however, caribou selected for high values of all forage components, particularly DN, suggesting that protein may be limiting. During late summer, after DN declined below the threshold for protein gain, caribou exhibited a switch at both spatial scales, selecting for higher biomass, likely enabling mass and fat deposition. Mosquito activity strongly altered caribou selection of forage and increased their movement rates, while oestrid fly activity had little influence. Our results demonstrate that early and late summer periods afford Arctic caribou distinct foraging opportunities, as they prioritize quality earlier in the summer and quantity later. Climate change may further constrain caribou access to DN as earlier, warmer Arctic summers may be associated with reduced DN and increased mosquito harassment.     

Woodland Caribou Extirpation and Anthropogenic Landscape Disturbance in Ontario

Abstract: The decline of woodland caribou (Rangifer tarandus caribou) has been attributed to anthropogenic landscape disturbances, but critical distance thresholds and time lags between disturbance and extirpation are unknown. Using a database of caribou presence and extirpation for northern Ontario, Canada, geo-coded to 10 times 10-km cells, we constructed logistic regression models to predict caribou extirpation based on distance to the nearest of each of 9 disturbance types: forest cutovers, fires, roads, utility corridors, mines, pits and quarries, lakes, trails, and rail lines. We used Akaike's Information Criterion to select parsimonious models and Receiver-Operating Characteristic curves to derive optimal thresholds. To deal with the effects of spatial autocorrelation on estimates of model significance, we used subsampling and restricted randomizations. Forest cutovers were the best predictor of caribou occupancy, with a tolerance threshold of 13 km to nearest cutover and a time lag of 2 decades between disturbance by cutting and caribou extirpation. Management of woodland caribou should incorporate buffers around habitat and requires long-term monitoring of range occupancy.     

Estimating Size and Trend of the North Interlake Woodland Caribou Population Using Fecal-DNA and Capture-Recapture Models

A critical step in recovery efforts for endangered and threatened species is the monitoring of population demographic parameters. As part of these efforts, we evaluated the use of fecal-DNA based capture–recapture methods to estimate population sizes and population rate of change for the North Interlake woodland caribou herd (Rangifer tarandus caribou), Manitoba, Canada. This herd is part of the boreal population of woodland caribou, listed as threatened under the federal Species at Risk Act (2003) and the provincial Manitoba Endangered Species Act (2006). Between 2004 and 2009 (9 surveys), we collected 1,080 fecal samples and identified 180 unique genotypes (102 females and 78 males). We used a robust design survey plan with 2 surveys in most years and analysed the data with Program MARK to estimate encounter rates (p), apparent survival rates (φ), rates of population change (λ), and population sizes (N). We estimated these demographic parameters for males and females and for 2 genetic clusters within the North Interlake. The population size estimates were larger for the Lower than the Upper North Interlake area and the proportion of males was lower in the Lower (33%) than the Upper North Interlake (49%). Population rate of change for the entire North Interlake area (2005–2009) using the robust design Pradel model was significantly <1.0 (λ = 0.90, 95% CI: 0.82–0.99) and varied between sex and area with the highest being for males in Lower North Interlake (λ = 0.98, 95% CI: 0.83–1.13) and the lowest being for females in Upper North Interlake (λ = 0.83, 95% CI: 0.69–0.97). The additivity of λ between sex and area is supported on the log scale and translates into males having a λ that is 0.09 greater than females and independent of sex, Lower North Interlake having a λ that is 0.06 greater than Upper North Interlake. Population estimates paralleled these declining trends, which correspond to trends observed in other fragmented populations of woodland caribou along the southern part of their range. The results of this study clearly demonstrate the applicability and success of non-invasive genetic sampling in monitoring populations of woodland caribou. © 2012 The Wildlife Society.     

Modeling the Western Arctic Caribou Herd During a Positive Growth Phase: Potential Effects of Wolves and Radiocollars

ABSTRACT Population modeling exercises can lead to both expected and unexpected results useful for wildlife research and management, even though inferences must often be qualitative, given underlying assumptions. Our main objective was to use empirical data on wolf (Canis lupus) kill rates and growth of the Western Arctic caribou (Rangifer tarandus) herd (WAH) of Alaska, USA, to assess the potential for predator regulation. We used available data and published literature to construct a deterministic density-dependent population model fitted to trends of the WAH from 1976 through 2003. By increasing wolf densities in the baseline model, we failed to reject the hypothesis that wolves at a density of 6.5 wolves per 1,000 km² could regulate a caribou herd at a density of 0.4 caribou per km². In addition, our model may be conservative by underestimating the regulatory potential of wolves. We suggest that this relatively simple predator-preysystem shows signs of a predation—food 2-state model. Elasticities from matrix models may be deceiving. Although herd growth is most sensitive to changes in adult female survival, survival of younger cohorts may be more easily influenced by natural conditions or management action. Management of the WAH near maximum sustained yield may not be attainable if desired, but modeling exercises such as this elucidate options. In conducting this research, we also discovered by Monte Carlo simulation that survival and productivity data from radiocollared females and calves were negatively biased and failed to predict herd growth. Thus, researchers should consider potential effects of neck collars on vital rates of female tundra caribou and concomitant offspring when using sample data to model population dynamics or test hypotheses.     

Impacts of spruce budworm defoliation on the habitat of woodland caribou,moose, and their main predators

Forest logging has contributed to the decline of several woodland caribou populations by causing the fragmentation of mature coniferous stands. Such habitat alterations could be worsened by spruce budworm (SBW) outbreaks. Using 6201 vegetation plots from provincial inventories conducted after the last SBW outbreak (1968–1992) in boreal forests of Québec (Canada), we investigated the influence of SBW‐caused tree defoliation and mortality on understory vegetation layers relevant to woodland caribou and its main predators. We found a positive association between severe outbreaks and the cover of most groups of understory plant species, especially in stands that were dominated by balsam fir before the outbreak, where a high canopy openness particularly benefited relatively fast‐growing deciduous plants. Such increases in early successional vegetation could provide high‐quality forage for moose, which is likely to promote higher wolf densities and increase predation pressure on caribou. SBW outbreaks may thus negatively affect woodland caribou by increasing predation risk, the main factor limiting caribou populations in managed forests. For the near future, we recommend updating the criteria used to define critical caribou habitat to consider the potential impacts of spruce budworm defoliation.     

Inferring parturition and neonate survival from movement patterns of female ungulates: a case study using woodland caribou

Analyses of animal movement data have primarily focused on understanding patterns of space use and the behavioural processes driving them. Here, we analyzed animal movement data to infer components of individual fitness, specifically parturition and neonate survival. We predicted that parturition and neonate loss events could be identified by sudden and marked changes in female movement patterns. Using GPS radio‐telemetry data from female woodland caribou (Rangifer tarandus caribou), we developed and tested two novel movement‐based methods for inferring parturition and neonate survival. The first method estimated movement thresholds indicative of parturition and neonate loss from population‐level data then applied these thresholds in a moving‐window analysis on individual time‐series data. The second method used an individual‐based approach that discriminated among three a priori models representing the movement patterns of non‐parturient females, females with surviving offspring, and females losing offspring. The models assumed that step lengths (the distance between successive GPS locations) were exponentially distributed and that abrupt changes in the scale parameter of the exponential distribution were indicative of parturition and offspring loss. Both methods predicted parturition with near certainty (>97% accuracy) and produced appropriate predictions of parturition dates. Prediction of neonate survival was affected by data quality for both methods; however, when using high quality data (i.e., with few missing GPS locations), the individual‐based method performed better, predicting neonate survival status with an accuracy rate of 87%. Understanding ungulate population dynamics often requires estimates of parturition and neonate survival rates. With GPS radio‐collars increasingly being used in research and management of ungulates, our movement‐based methods represent a viable approach for estimating rates of both parameters.     

Trapping oestrid parasites of reindeer: the relative age, fat body content and gonotrophic conditions of Cephenemyia trompeand Hypoderma tarandifemales caught in baited traps

Abstract. Dissection of flies caught in northern Norway revealed that only mated, gravid females of H.tarandi (L.) and larviparous C.trompe (Modeer) were caught in host-mimicking C0₂-baited traps. Trapped females had the same gonotrophic and fat body (FB) conditions as females caught on and around reindeer. Most trapped females of both species were of middle to old age, having only one-half to no FB reserves left and only a few to moderate numbers of eggs or larvae remaining. Most young females trapped also had previously oviposited or larviposited at least once, and some newly eclosed, mated females were present throughout the fly season. Based on the known location of reindeer herds, it was evident that trapped flies that had recently oviposited or larviposited had dispersed into the trapping area from 25–100 km away. Declining FB reserves sustained wild-caught C.trompe females (and in utero larvae) in the laboratory for 14 days and H.tarandi females for 18 days. Reserve FB also was depleted during long flights. Females of both species that flew for the longest times (5.1–11.7 h) on a laboratory flight mill had low FB reserves, but nearly maximum numbers of eggs or larvae. Conversely, most females that flew for less than 5 h on the flight mill had little or no FB remaining, and few eggs or larvae. The large FB reserves accumulated as larvae feed in the vertebrate host enable the non-feeding adults to survive and infect their hosts even after prolonged periods of flight-inhibiting climatic conditions.     

Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones

Bone development requires the recruitment of osteoclast precursors from surrounding mesenchyme, thereby allowing the key events of bone growth such as marrow cavity formation, capillary invasion, and matrix remodeling. We demonstrate that mice deficient in gelatinase B/matrix metalloproteinase (MMP)-9 exhibit a delay in osteoclast recruitment. Histological analysis and specialized invasion and bone resorption models show that MMP-9 is specifically required for the invasion of osteoclasts and endothelial cells into the discontinuously mineralized hypertrophic cartilage that fills the core of the diaphysis. However, MMPs other than MMP-9 are required for the passage of the cells through unmineralized type I collagen of the nascent bone collar, and play a role in resorption of mineralized matrix. MMP-9 stimulates the solubilization of unmineralized cartilage by MMP-13, a collagenase highly expressed in hypertrophic cartilage before osteoclast invasion. Hypertrophic cartilage also expresses vascular endothelial growth factor (VEGF), which binds to extracellular matrix and is made bioavailable by MMP-9 (Bergers, G., R. Brekken, G. McMahon, T.H. Vu, T. Itoh, K. Tamaki, K. Tanzawa, P. Thorpe, S. Itohara, Z. Werb, and D. Hanahan. 2000. Nat. Cell Biol. 2:737-744). We show that VEGF is a chemoattractant for osteoclasts. Moreover, invasion of osteoclasts into the hypertrophic cartilage requires VEGF because it is inhibited by blocking VEGF function. These observations identify specific actions of MMP-9 and VEGF that are critical for early bone development.