Non-Invasive Assessment of the Interrelationships of Diet, Pregnancy Rate, Group Composition, and Physiological and Nutritional Stress of Barren-Ground Caribou in Late Winter

RESEARCH ARTICLE Non-Invasive Assessment of the Interrelationships of Diet, Pregnancy Rate, Group Composition, and Physiological and Nutritional Stress of Barren-Ground Caribou in Late Winter Kyle Joly1,2*, Samuel K. Wasser3, Rebecca Booth3 1 Gates of the Arctic National Park & Preserve, National Park Service, Fairbanks, Alaska, United States of America, 2 Arctic Inventory and Monitoring Network, National Park Service, Fairbanks, Alaska, United States of America, 3 University of Washington, Center for Conservation Biology, Seattle, Washington, United States of America * Abstract OPEN ACCESS Citation: Joly K, Wasser SK, Booth R (2015) NonInvasive Assessment of the Interrelationships of Diet, Pregnancy Rate, Group Composition, and Physiological and Nutritional Stress of Barren-Ground Caribou in Late Winter. PLoS ONE 10(6): e0127586. doi:10.1371/journal.pone.0127586 Academic Editor: Cédric Sueur, Institut Pluridisciplinaire Hubert Curien, FRANCE Received: November 4, 2014 Accepted: April 16, 2015 Published: June 10, 2015 Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Data Availability Statement: All relevant data are available from the National Park Service's webpage dedicated to monitoring caribou. URL: http://science. nature.nps.gov/im/units/arcn/vitalsign.cfm?vsid=19. The winter diet of barren-ground caribou may affect adult survival, timing of parturition, neonatal survival, and postpartum mass. We used microhistological analyses and hormone levels in feces to determine sex-specific late-winter diets, pregnancy rates, group composition, and endocrine-based measures of physiological and nutritional stress. Lichens, which are highly digestible but contain little protein, dominated the diet (> 68%) but were less prevalent in the diets of pregnant females as compared to non-pregnant females and males. The amount of lichens in the diets of pregnant females decreased at higher latitudes and as winter progressed. Pregnancy rates (82.1%, 95% CI = 76.0 – 88.1%) of adult cows were within the expected range for a declining herd, while pregnancy status was not associated with lichen abundance in the diet. Most groups (80%) were of mixed sex. Male: female ratios (62:100) were not skewed enough to affect the decline. Levels of hormones indicating nutritional stress were detected in areas of low habitat quality and at higher latitudes. Levels of hormones indicated that physiological stress was greatest for pregnant cows, which faced the increasing demands of gestation in late winter. These fecal-based measures of diet and stress provided contextual information for the potential mechanisms of the ongoing decline. Non-invasive techniques, such as monitoring diets, pregnancy rates, sex ratios and stress levels from fecal samples, will become increasingly important as monitoring tools as the industrial footprint continues to expand in the Arctic. Funding: The National Park Service funded this study. Competing Interests: The authors have declared that no competing interests exist. PLOS ONE | DOI:10.1371/journal.pone.0127586 June 10, 2015 1 / 13 Late Winter Diets, Sex Ratios and Hormone Levels of Arctic Caribou Introduction The cumulative effects of industrial development are impacting caribou (Rangifer tarandus) populations, especially in the southern portions of their range. These impacts have been primarily documented in boreal caribou populations, while many barren-ground caribou herds in the arctic may be declining as well [1]. Industrial development is increasing in the Arctic and has the potential to have similarly negative consequences for barren-ground caribou as has been documented for boreal caribou [2–4]. Aside from habitat degradation and conversion, displacement of caribou from industrial development has received the most attention (e.g. [5]). However, industrial development may have numerous other indirect impacts on caribou populations, such as increasing nutritional stress and altering predator-prey dynamics [6,7]. Caribou, ranging from temperate rainforests to polar desert, are capable to adapting to a wide array of conditions that climate change may induce. Some potential changes, such as increased vegetative productivity in the Arctic, may actually prove beneficial for caribou. However, other changes, such as increased occurrence of icing events [8] and conversion of tundra to shrub habitats [9] may prove detrimental [10,11]. A warmer Arctic may lead to drier conditions and more wild fires which, in combination with competition from expanding shrub habitats, could lead to declines in lichen abundance [12]. Terricolous lichens are an important component of the winter diets of barren-ground caribou [13– 17]. Lichens are rich in digestible energy but low in protein [18]. The availability of lichens throughout the winter reduces the dependence of female caribou on body reserves that are important to survival [19] and reproduction [20]. Snow depth and hardness affects the availability of lichens for caribou [21]. Winter nutrition is linked with adult survival, timing of parturition, neonatal survival, and postpartum mass [22–27]. Low neonatal survival, resulting from poor winter nutrition during late gestation, could incorrectly be attributed to predation [27]. Predation on neonates could similarly obfuscate the effects of nutritional stress if high pregnancy rates exist [27]. Depressed postpartum mass could affect milk production and place cows at a disadvantage to reach an adequate nutritional plane to conceive in the fall [27,28]. Caribou may be able to compensate over the summer given favorable summer range conditions, however, Dale et al. [29] found that compensatory growth in smaller individuals occurred during winter months, not summer, for young caribou. The Western Arctic Herd, numbering 490,000 caribou in 2003, was the largest herd in Alaska and one of the largest in the world [30]. Rural residents from about 40 villages in northwest Alaska rely upon these caribou as a critical subsistence resource. Since 2003, the herd has rapidly declined [30] to 235,000 caribou in 2013 [31]. Coupled with the undetermined mechanism for the decline, the uncertain effects of a rapidly changing climate [10,32] and proposed industrial development in the region [4,33] are amplifying concerns about the population as well as the availability of caribou for subsistence-based communities in the region. Therefore, to establish a baseline for monitoring, we used a noninvasive fecal sampling approach and endocrine-based measures of stress to determine and evaluate the interrelationships of winter diets, sex, pregnancy status, group composition, and physiological and nutritional stress in overwintering caribou. While an analogous effort was completed f (...truncated)