Space use by giant anteaters in a protected area within human‐modified landscape

Blog written by Alessandra Bertassoni. Read the full article here.

Shaggy, toothless, great snout and slow… These are common adjectives applied to the Giant Anteater – the largest anteater species in the Neotropic. This is a species that attracts curiosity, as well as having gaps in our knowledge of its ecology. Despite its large distribution (from Honduras to southern South America), it can be locally rare or very threatened in some areas (e.g. Central America and at the south of its distribution).

Numerous risks threaten the persistence of populations, such as wildfires, poaching, conflicts with dogs, road-kills, fragmentation, and habitat loss – these last two are the major threat to populations. To try to preserve natural habitats, countries have adopted the creation and maintenance of protected areas. On one hand, this is a good conservation strategy in times of huge changes to global systems – mostly driven by intensive human activities. On the other hand, some protected areas and their communities are immersed and isolated in human-modified landscapes. Large mammals require extended space, and the borders of the protected area are often bypassed.

This is the background of our study – “Space use by giant anteaters (Myrmecophaga tridactyla) in a protected area within the human‐modified landscape”. Our work took place in the Santa Bárbara Ecological Station (SBES), a protected Cerrado biome remnant (27 km²) surrounded by human-modified landscape in the State of São Paulo, Southeastern Brazil (Figure 1).

Figure 1: Santa Barbara Ecological Station (SBES, black polygon) and its surroundings in Southeastern Brazil. The green polygon is a Pinus sp. Plantation, the red traces are roads and Aguas de Santa Barbara municipality is represented as a light orange diamond.

This area is considered to have high biological importance due to its typical Cerrado vegetation. However, it is surrounded by pasture, sugarcane, exotic timber plantations (green dash line, Figure 1), and urban zones. It is also divided by a road network (red dash line, Figure 1). There is a resident population of giant anteaters within the SBES. We hypothesized that they would be highly dependent on the natural features of the protected Cerrado remnant because of their extreme specializations and habitat requirements. We also predicted that their home ranges will be primarily located within the SBES and the resources inside will be more used than the surroundings. Finally, we predicted that home ranges will overlap by more than 50% due to the small size of the protected area. This was a pioneer study of giant anteaters in a highly human-modified area.

To pursue these ideas it was necessary to track giant anteaters in the SBES and surrounding area. This species needs to be captured actively, as methods such as cage traps or baits are ineffective. Therefore, the team has to be in the field to search, find and catch giant anteaters.

In 2015, we spent three months in the SBES and its surrounding area. We covered approx. 12,000 km (three field campaigns) and we succeeded in capturing eight giant anteaters; four females (F) and four males (M). We fitted them with GPS-harnesses (see Figure 2).

Figure 2. A tracked giant anteater with GPS harness in the Santa Barbara Ecological Station, Southeastern Brazil.

For a few months (10 – 147 days, 91 on average), we were able to record 13,170 locations of the tracked individuals (Figure 3). This enabled us to record a great deal of interesting ecological data. Five giant anteaters (2 F and 3 M) remained almost exclusively inside the SBES and the other three (F1, M2, and M4) had more than 20% of their locations recorded outside of it. This gives us some indication that the SBES area and its requirements are not enough alone to accommodate this population. Residing outside of the protected area could be the best choice for individuals that require more space or are searching for specific resources which are too many exploited or limited within the SBES.

Another clue was the increasing trend in the home-range area of the two males (M2 and M4) to leave the SBES. From a conservation genetic perspective, individuals that leave a population to reach another can be considered propagules that contribute to the genetic pool. But, in a human-modified landscape, leaving protected areas is too risky, especially in a place that has more than one road.

In the two years that we spent in the study area, we found giant anteaters, deer and other animals killed by collisions with traffic. We predicted a great deal of overlap between individuals due to the SBES size, and we reported that dyads of opposite sex presented larger area-overlap than same-sex dyads, using two space-sharing indexes. However, this is not breaking news. Much more elucidative data came from the analysis of combined trajectories. This revealed proximity events in five dyads of opposite sexes and a male-dyad.

Figure 3. Giant anteaters locations inside the SBES and surroundings, Southeastern Brazil. M = male and F = female.

.What does this mean? Proximity events could indicate higher levels of coexistence than previously reported for this species, or that the study site is too small, meaning the anteaters interact more often. In addition, proximity analysis highlights that low home-range overlap cannot be strongly interpreted as a lack of individual interaction. Proximity events could indicate reproductive behaviour.

However, we still do not know if there is reproductive seasonality for the species, and this needs further study to advance our knowledge of this species’ natural history. Despite giant anteaters being most well-studied anteater species, we still lack the basic knowledge to to ask the right questions. We need to apply much more effort to studies on human-modified areas, to reach the minimal information needed to understand population trends and to move conservation forward.

Denning in brown bears

Blog written by Enrique González-Bernardo. Read the full article here.

Hibernation represents an adaptation for coping with unfavorable environmental conditions. For brown bears (Ursus arctos), hibernation coincides with winter in seasonal environments generally associated with low temperatures and low food abundance during which pronounced temporal reductions in several physiological functions occur. It is a critical period because at that time: (a) pregnant females give birth and undergo lactation while in dens; (b) energy savings during hibernation can be substantial; and (c) premature exit can negatively affect energy conservation and cub survival.

Brown bears are widely distributed around the northern hemisphere, with populations of different characteristics inhabiting very diverse habitats. Thus, the management and conservation of this species requires detailed knowledge about denning ecology of different populations, identifying patterns or gradients of denning behavior throughout the distribution range of the species and highlighting possible differences between populations. It is reasonable to expect that: (1) den chronology may vary by sex and bear reproductive status; (2) the duration of hibernation also depends on environmental factors, i.e. snow, temperature and food availability; (3) a relationship may exist between denning period and latitude, longitude and altitude; and (4) although the choice of a den and den surroundings may be variable, some differences may still exist by class, age and sex.

There are differences between sexes and ages in relation to denning chronology, with pregnant females enter the den earlier and exit later than other bear classes to take care of new-born and males and subadults generally having shorter denning periods. Hibernation in brown bears is mostly governed by a trade-off between environmental conditions metabolic dietary-related and energy conservation needs, with the exception of pregnant females which ultimate reasons are reproductive needs. As a general rule, the duration of hibernation in different brown bear populations seems to be conditioned by both snowfall/snow depth and snowmelt in spring. Snowfall can act as a major impetus to begin hibernation, as well as the ambient temperature. Warmer winters seems to be associated with a decrease in the length of the hibernation period and the postponement of den entry, while low autumn temperatures may cause early den entry. Den emergence seems to be regulated in some way with an increase in temperature, but not depending on the exact ambient temperature on the day of emergence (probably because den emergence is a longer process), but by the temperature the previous weeks. However, the hibernation period is primarily affected by a decrease in food availability due to the snow cover, which guides den entry and exit. Continuous availability of food and mild climates may prompt individuals to spend the winter outside dens, with bears in more northern areas spending more time hibernating than bears in the southernmost latitudes. There is an evident gradient between den chronology and latitude, but it seems to affect primarily to adult bears. Similarly, altitude has been described as influencing denning dates, with bears denning at lower altitudes emerging earlier than those hibernating at higher altitudes. Den abandonment occurs naturally, but human activities, such as industrial and forestry activity, hunting, transit of people or even research activity have been reported as the main cause. It may have negative consequences for populations, such as increases in cub mortality. In some populations where there are natural food sources during the winter, part of the population may not hibernate. This phenomenon is especially intense where supplementary food is provided during winter, which may alter the chronology of hibernation or winter.

The choice of a den and its surroundings may affect individual fitness, for example, loss of offspring and excessive energy consumption. Den selection is the result of broad- and fine-scale habitat selection, mainly linked to den insulation, remoteness, and availability of food in the surroundings of the den location. The most common den types are those excavated in the ground or located inside natural caves, but other types of dens such as depressions under rock shelters, nest dens and tree cavities have been reported. The typical conformation of a den consists of an entrance, a tunnel and the chamber where the bear builds the nest. Brown bears select sunny slopes and sites with deeper snowpack, which have insulating properties that help maintain a constant temperature protection. Other selected features are the slope of the hillside (simpler digging, stability, solar radiation and protection) and the distance and altitude (more permanent snow cover and further from human disturbances). Differences have been described in terms of sex, with pregnant females hibernating higher because they have a longer hibernation and need more isolation, while adult males hibernate in lower areas, which would provide them with greater food availability at den emergence, rapidly increase body mass and thus improve breeding success.

Brown bears hibernate for several months during which they do not eat, drink, defecate or urinate. This huge metabolic challenge has demanded a series of physiological adaptations in tissues and organs, many of them unique, enabling bears to survive under nutritional deprivation and to overcome anuria, hyperlipidaemia and immobilization, preserve muscles and bones avoiding osteoporosis or sarcopenia and prevent diseases such as metabolic syndrome, diabetes and cardiovascular pathologies. During hyperphagia, brown bears becoming temporary insensible to leptin which allows a constant appetite. Bears exhibit an increase in body mass of around 40% during the pre-hibernation hyperphagia, mainly fat. During hibernation, the mass loss could reach 4 kg per day. The metabolic rate drops to a quarter of the active state level and the temperature drop is about 3-5 °C, starting days before the den entrance. As a result, heart rate begins to decrease up to 80%. During hibernation, brown bears exhibit blood parameters that would be indicators of pathology in humans and as a consequence of fat-based metabolism, maintaining concentrations of phospholipids, cholesterol and free fatty acids much higher than healthy human values. However, atherosclerosis, fatty streaks, foam cell infiltration and inflammation have not been reported in hibernating bears. The bladder becomes permeable and both water and nitrogenous substances re-enter the blood. This and other adaptation, such as a reduction of urea synthesis and reincorporating urea into skeletal muscle and other proteins, allow recycling of nitrogenous substances and prevent renal complications or azotemia. Organs involved in digestive, metabolic and excretion processes, such as the liver and kidneys, have their activity decreased compared to the active period decrease in function. Brown bears do not appear to suffer from skeletal muscle and bone dysfunction or bone loss during hibernation, despite immobilization and lack of food. Brown bears are able to maintain both muscle and bone mass and function by reducing catabolic processes and maintaining a certain level of mechanical activity, such as shivering. Brown bears give birth during hibernation, around January-February, when there is no intake of food and water. Pregnant females appear to have delayed implantation of the embryo. In older females, as well as in females with high body fat content, den entry dates and birth dates tend to be earlier and the lactation period may be longer than in other females. In addition, in females with a higher percentage of fat and lean mass, implant embryos and cub birth occur earlier and the mortality of their cubs during the first summer is lower than in other females.

Concerning the hibernation of brown bears it is important to correctly distinguish between actual drivers of hibernation (temperature, snow, food availability) and their correlates (physiological changes). We suspect that the correlates of proximate factors might fluctuate according to current environmental variations. Predicted variations in air temperatures generally point towards an increase in temperature and precipitation variability has already affected biological systems by altering the phenology. Inter-annual fluctuations in hibernation chronology are expected to occur due to inter-annual variations in climate, extreme climatic events and temperature anomalies resulting from climate change. These fluctuations are probably unpredictable for many organisms, including bears. It has been reported how brown bears advance the den exit by increasing spring temperature, and how the total duration of hibernation is reduced. Brown bears have been reported showing a noticeable plasticity when hibernating, adapting their denning behavior to environmental factors, availability of food during hyperphagia or changing snow conditions during the winter. Despite this, energy demands of hibernating mammals would increase with higher winter temperature, and mismatches could be expected between the den exit dates and food resources, in addition to a reduction in their abundance or availability. Altering hibernation conditions could have a negative effect on reproductive success and cub survival. Such increased mismatches might also increase the likelihood of bear-human conflicts if bears emerge earlier. It is important to highlight here the potential effect of anthropogenic food, and especially supplementary feeding (provided with hunting, eco-tourism and the mitigation of human-bear conflicts purposes), on the chronology of hibernation, being able to halve the denning period or increase den abandonments. For all this, future research is important to know how changes in climatic factors might affect the ability of bears to face global climate change and the human-mediated changes in food availability. In addition to this, a better understanding of how hyperphagia, predenning and denning periods, including for those populations in which bears do not hibernate every year, and how to approach the study of bear denning merging insights from different perspectives, that is, physiology, ecology, and behavior.

Phylogenomics of endangered and threatened species of grasses reveal close phylogenetic relationships

Blog written by P. H. Pischl, S.V. Burke, E. M. Bach, and M. R. Duvall.  Read the full paper here.

Biodiversity is the variety of life forms on Earth, and includes the variation seen in animals, plants, fungi, and microorganisms.  A major cause for a decrease in biodiversity is loss of a species’ home or habitat.  Habitats are being lost by the conversion of natural areas to urban and agricultural lands by humans.  As habitats are lost, species and ecosystems (the community of living organisms and the place where they live) become threatened or endangered as their numbers and area decrease.

At The Nature Conservancy’s Nachusa Grasslands, grazing bison are partly obscured in the September tallgrass prairie.  Photo by P. H. Pischl.

One of the most endangered ecosystems in North America is the tallgrass prairie.  Illinois is nicknamed the “Prairie State” because it was once covered in tallgrass prairies.  However, since 1830 when European settlement began, 99.9% of Illinois’ original tallgrass prairies have been lost to agriculture, industry, and urbanization (Ellis, 2017).  The removal of the tallgrass prairie habitat has caused seventeen species of grasses to be listed as endangered and one species to be listed as threatened by the Illinois Environmental Species Protection Board.  Grasses provide many ecosystem services, such as erosion control, soil formation, habitat for wildlife and carbon storage.  Loss of these endangered and threatened species would result in a loss of ecosystem services as well as a loss of biodiversity.

Ecologists and conservation biologists work to preserve biodiversity by conserving the various species in a region or an ecosystem.  They not only look at the number of species, but also consider the phylogenetic diversity between the species in the ecosystem.  The phylogenetic diversity compares the DNA of the species in the ecosystem to better understand the variation in genetic background of the species.  This genetic variation is seen in the traits the species have or do not have in common.  Plant communities with greater genetic variation are considered to have higher phylogenetic diversity.  Plant communities with higher phylogenetic diversity have been shown to be more productive and resistant to invasion by nonnative species (Barak, 2017).  Plant communities that are more closely related and exhibit less phylogenetic diversity may share traits that make them more vulnerable to the same threat.  These species are considered to be at a higher risk of extirpation from the ecosystem by habitat loss or changes in environmental conditions.

Leaf tissue was obtained from preserved herbarium specimens for DNA extraction.  Photo by M. R. Duvall.

In our article in Ecology and Evolution, we study the phylogenetic diversity of the endangered and threatened species of grasses from Illinois.  However, in order to study phylogenetic diversity, it is necessary to extract DNA from the species of interest.  Since these species are endangered and threatened, we were able to refine our methods to use preserved grass tissue from herbarium specimens.  The use of herbarium specimens avoided the disturbance of living populations of the endangered or threatened grasses.  From the extracted DNA, we were able to use Next Generation Sequencing techniques to sequence the complete plastid genomes for the endangered and threatened species of grass.  Our use of the complete plastid genome in our analysis leads to phylogenetic trees with greater support than studies using gene coding sequences alone.  We then analyzed these phylogenetic trees with three phylogenetic diversity metrics to relate the evolutionary history of the species to their ecological characteristics.  All of these phylogenetic diversity metric values show that the endangered and threatened species are phylogenetically clustered at evolutionary points in both past and more recent events.  Phylogenetic clustering means that these species may be more closely related than expected by chance and share traits that make them vulnerable to the same threats.  Phylogenetic clustering is indicative of phylogenetic niche conservatism.  Should these species be lost from the landscape, several small groups of native grass diversity would be lost. 

In our study, we have shown how herbarium material is useful for ecological research, allowing the study of endangered and threatened species without disturbing the few remaining populations.  DNA extracted from the herbarium material was used to produce complete plastid genome sequences using Next Generation Sequencing techniques.  The complete plastomes from species of grasses known to grow in Illinois provided a robust and strongly supported phylogeny.  Communities of grasses in Illinois were evaluated using three phylogenetic diversity metrics.  The three phylogenetic diversity metrics all led to the same result; the endangered and threatened species are phylogenetically clustered, which can be interpreted as phylogenetic niche conservatism of these grasses.  The loss of the endangered and threatened species and the genetic biodiversity they supply would also lead to changes in ecosystem services and protection from invasive species.  The niches occupied by the endangered and threatened grasses should be considered as priority conservation sites to protect these species, the biodiversity, and ecosystem services they provide.  Maintaining healthy native plant communities is essential.  Not only for organisms that share these habitats and rely on these plants for shelter and forage, but for humans and the ecosystem services that are provided to maintain a healthy environment.

Barak, R. S., Williams, E. W., Hipp, A. L., Bowles, M. L., Carr, G. M., Sherman, R., & Larkin, D. J. (2017). Restored tallgrass prairies have reduced phylogenetic diversity compared with remnants. Journal of Applied Ecology, 54(4), 1080-1090.

Ellis, J. L. (2017). Ecosystem Conservation and Management in an Era of Global Climate Change. Science & Ecological Policy Paper. Retrieved January 7, 2018, from

Barriers facing early career researchers from minority groups

Written by Klara M Wanelik, Joanne S Griffin, Megan L Head, Fiona C Ingleby and Zenobia Lewis.

Read the full article here.

Over the course of the past ten years, Science Technology Engineering and Maths (STEM) academia has recognised that it has a diversity problem. The ‘leaky pipeline’, as it is often called, represents the shrinking pool of women in academia through the career stages from undergraduate students, through tenured staff, and then into more senior positions. Although the numbers vary between fields and countries, the overall trend is similar. Figures from the UK show that while over half of postgraduate biosciences students are women, only 15% are at professorial level. Aside from the moral argument for careers in academia being accessible to all those who want a place at the table, studies from corporate sectors have shown that diversity is beneficial in terms of productivity, outputs, and financial gains.

National schemes to improve the representation of women in STEM academia, such as Athena SWAN in the UK and Australia, have made some progress. And yet, the picture for non-gender minority groups is even more stark. Black, Asian, and Minority Ethnic (BAME), disabled, and LGBT+ people are even more poorly represented in academia, compared to in the general population, and are more likely to experience institutional and cultural barriers to career progression.

Back in 2017, we held a symposium for graduate students and postdocs at the University of Liverpool, showcasing the experiences of staff from minority backgrounds. Feedback from respondents suggested there was an appetite for more open discussion regarding the challenges associated with being in a minority group in academia, and from this, the Breaking Barriers project was born.

We surveyed early career researchers in the ecology and evolution community. We asked respondents for data regarding their personal characteristics, for example, which gender they identified with, whether they identified as LGBT+, and whether they were from an ethnic minority background. We also asked whether they had come from a lower socioeconomic background, as we predicted that socioeconomic background could prove to be a barrier to career progression. We asked respondents to provide information on their career to date, and finally, we asked respondents for information on whether they had experienced any barriers to their career progression and, if so, whether they had overcome them.

Our results were upsetting to say the least. Of the 188 individuals that responded to the survey, 54% reported having faced a barrier or multiple barriers to their career progression. Of these, almost a third reported that they had not overcome stated barriers and/or had left academia as a result of them. If anything, we believe this could be an underestimate, since people who had since left academia would have been less likely to engage with a study on an academic issue. We also found that BAME and Latino-Hispanic respondents reported having few publications on finishing their PhD, and having fewer publications translated into having to apply for more positions before obtaining a job. Respondents from lower socioeconomic backgrounds were more likely to be in a research and teaching role, as opposed to a research only role. They were also more likely, along with women, and LGBT+ individuals, to report having experienced a barrier to their career progression.

What does all this mean? It seems that in the field of ecology and evolution there is a significant pool of the workforce who are struggling to access, retain, and succeed in an academic career. Our study suggests that multiple interacting individual characteristics should be considered in combination when we try to understand diversity issues in academia. In particular we would like to highlight that, while barriers related to sex were cited most frequently in the free-text questions, it was not significant in predicting the measures of career progression that we examined. This could suggest that gender is still viewed as an obstacle, despite efforts to improve female representation. Alternatively, the wider discourse with respect to gender diversity in recent years may have helped people feel more comfortable to voice these concerns (rather than concerns they may have about other diversity issues). Worryingly, the relative lack of discourse around other diversity issues, for instance with respect to ethnic minority groups or people from lower socioeconomic backgrounds, may mean that these issues are more likely to be overlooked and underestimated. Until we have more open discussion and understanding of diversity as an intersectional issue, we might not see as much improvement in the field as we’d like to.

But it’s not all doom and gloom. Over two thirds of individuals who said they had faced a barrier (or multiple barriers) to their career progression reported that they had overcome stated barriers. We were able to draw on these individuals’ rich experience, asking them about how they had done this. Two main themes emerged in these individuals’ responses: the importance of people (including mentoring, networking and associating with senior allies) and opportunities (including taking up as well as actively asking for opportunities).

In light of this, we suggest some routes towards improvement in our paper, including more emphasis on mentoring schemes, as well as broadening accessibility of networking opportunities by creating more online spaces for this purpose (which might be something positive we could take forward from the current Covid-related working circumstances!). We also comment on the somewhat grander aim of overall institutional cultural change. This will be crucial in order to see major improvements, particularly with regards to ensuring that opportunities are made accessible to all early-career researchers. We hope that through further research into intersectional diversity issues in academia, we might open up the discussion a little more, and move towards creating a culture where diversity can be fully appreciated.

Seed consumption by rodents reflects the signature of top-down effects mediated by wolves

Blog written by Jennifer L. Chandler and John L. Orrock. Read the full paper here.

Because most plants die before becoming seedlings, the distribution and abundance of plants often depends upon the distribution and survival of plant seeds. Small mammals are ubiquitous granivores with the potential to determine the distribution and regeneration of plants and trees in forests. Despite their importance, patterns of rodent granivory can also be highly variable, making it difficult to predict how granivory will affect plant recruitment at large scales. While variation in productivity, seasonality, or latitude have been identified as important for predicting patterns of seed predation, often considerable variation in seed predation exists even after these factors are considered.

Since rodents are common prey of carnivores, knowledge of activity patterns of rodent predators may play a part in predicting hotspots and coldspots of seed consumption by rodents. Large carnivores can have effects that cascade down the food chain, altering ecosystem dynamics both when they are removed and reintroduced to a system. Top carnivores can affect abundance and behavior of mesocarnivores, which in turn affect abundance and behavior of their prey, usually herbivores, which can alter plant abundance and community composition. We hypothesized that distributions of apex predators can create large-scale variation in the distribution and abundance of mesopredators that consume small mammals, creating predictable areas of high and low seed survival.

The hypothesized effects of interactions among carnivores on rodent abundance and seed survival. Solid arrows represent direct effects and dashed arrows represent indirect effects. Pluses and minuses indicate positive and negative effects.

The natural recolonization of northern Wisconsin by gray wolves (Canis lupus) presented a unique opportunity to test the hypothesis that interactions among carnivores affect seed consumption by rodents. By comparing areas recolonized by wolves to areas that had been essentially wolf-free since 1960, we could test whether apex predator presence indicates areas of low seed predation by rodents. Gray wolves competitively exclude coyotes (C. latrans), but better tolerate foxes (Vulpes vulpes, Urocyon cinereoargentus) because foxes have less diet overlap with wolves and are therefore, are less competition. Thus, areas with high wolf activity, such as wolf territories, are areas of relatively lower coyote activity, and higher fox activity. Foxes are expected to consume a greater proportion of small mammals, such as rodents that eat seeds, compared to coyotes. Consequently, we hypothesized that wolf territories may be areas of lower seed consumption due to the higher abundance of rodent predators.

Using multi-year field trials at sites inside and outside of 11 wolf territories in northern Wisconsin, USA, we evaluated whether rodent abundance and seed consumption were lower in wolf territories. At each site, we conducted live trapping sessions to survey rodent abundance. To measure seed consumption, we placed seed depots (plastic containers with known numbers of seeds of four tree species scattered on top of a layer of sand) at study locations for two-week periods, after which, seeds depots were collected and remaining seeds were counted. To confirm that differences between areas inside and outside of wolf territories were a result of differing interactions among carnivores, we also investigated several alternate explanations for the patterns in rodent abundance and seed survival that we observed. We measured a variety of habitat characteristics across our site, such as tree canopy cover, shrub cover, and presence of woody debris (all factors that can influence rodent abundance and activity), to rule out other potential causes of low rodent abundance and seed consumption that may be inherent in habitat where wolves preferentially establish territories.

Acer saccharum and A. rubrum seeds consumed by small mammals inside a seed depot. Red circles indicate examples of consumed seeds.

Consistent with the hypothesized consequences of wolf occupancy, predation of seeds of three tree species was more than 25% lower inside wolf territories areas across two years. Rodent abundance was more than 40% lower in high-wolf areas during one of two study years: a result primarily driven by low southern red-backed vole (Myodes gapperi) abundance in wolf territories. The absence of significant habitat differences between high- and low-wolf areas that might affect rodent abundance or activity further supported these results. Together, our findings suggest that top-down effects of wolves on seed consumption by rodents and seed survival may occur inside wolf territories.

Accounting for the effects of interactions among carnivores on lower levels on the food chain may allow for more accurate predictions of large-scale patterns in seed survival and forest composition, as well as other important ecological processes. With the knowledge of the activity of relatively few individuals of an apex species (e.g., wolves), we were able to predict considerable variation in rodent abundance and seed survival. This finding has important practical applications in forest management; since the majority of U.S. forests rely upon natural regeneration of harvested forest stands (i.e., recruitment from seeds, as opposed to planting), understanding how top predators influence seed survival may allow forest managers to predict which stands are more likely to experience recruitment failure after harvest. Territory boundaries of apex predators may also predict patterns of ecological interactions that influence disease prevalence. For example, small mammals are important intermediate hosts of the bacteria that causes Lyme disease in humans. Areas between predator territories may be areas of high rodent abundance, and therefore, may indicate locations of increased Lyme disease risk to humans. Consideration of the top-down effects of carnivore interactions may shed new light on spatial patterns in many ecological processes with economic, human-health, and conservation consequences that may have otherwise been dismissed as anomalous.

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