Improving the assessment of predator functional responses by considering alternate prey and predator interactions.

To improve understanding of the complex and variable patterns of predator foraging behavior in natural systems, it is critical to determine how density-dependent predation and predator hunting success are mediated by alternate prey or predator interference. Despite considerable theory and debate seeking to place predator-prey interactions in a more realistic context, few empirical studies have quantified the role of alternate prey or intraspecific interactions on predator-prey dynamics. We assessed functional responses of two similarly sized, sympatric carnivores, lynx (Lynx canadensis) and coyotes (Canis latrans), foraging on common primary (snowshoe hares; Lepus americanus) and alternate (red squirrels; Tamiasciurus hudsonicus) prey in a natural system. Lynx exhibited a hyperbolic prey-dependent response to changes in hare density, which is characteristic of predators relying primarily on a single prey species. In contrast, the lynx-squirrel response was found to be linear ratio dependent, or inversely dependent on hare density. The coyote-hare and coyote-squirrel interactions also were linear and influenced by predator density. We explain these novel results by apparent use of spatial and temporal refuges by prey, and the likelihood that predators commonly experience interference and lack of satiation when foraging. Our study provides empirical support from a natural predator-prey system that (1) predation rate may not be limited at high prey densities when prey are small or rarely captured; (2) interference competition may influence the predator functional response; and (3) predator interference has a variable role across different prey types. Ultimately, distinct functional responses of predators to different prey types illustrates the complexity associated with predator-prey interactions in natural systems and highlights the need to investigate predator behavior and predation rate in relation to the broader ecological community.

Improved probability of detection of ecological "surprises".

Ecological "surprises" are defined as unexpected findings about the natural environment. They are critically important in ecology because they are catalysts for questioning and reformulating views of the natural world, help shape assessments of the veracity of a priori predictions about ecological trends and phenomena, and underpin questioning of effectiveness of resource management. Despite the importance of ecological surprises, major gaps in understanding remain about how studies might be done differently or done better to improve the ability to identify them. We outline the kinds of ecological surprises that have arisen from long-term research programs that we lead in markedly different ecosystems around the world. Based on these case studies, we identify important lessons to guide both existing studies and new investigations to detect ecological surprises more readily, better anticipate unusual ecological phenomena, and take proactive steps to plan for and alleviate "undesirable" ecological surprises. Some of these lessons include: (i) maintain existing, and instigate new, long-term studies; (ii) conduct a range of kinds of parallel and concurrent research in a given target area; (iii) better use past literature and conceptual models of the target ecosystem in posing good questions and developing hypotheses and alternative hypotheses; and (iv) increase the capacity for ecological research to take advantage of opportunities arising from major natural disturbances. We argue that the increased anticipatory capability resulting from these lessons is critical given that ecological surprises may become more prevalent because of climate change and multiple and interacting environmental stressors.

Disentangling trophic relationships in a High Arctic tundra ecosystem through food web modeling.

Determining the manner in which food webs will respond to environmental changes is difficult because the relative importance of top-down vs. bottom-up forces in controlling ecosystems is still debated. This is especially true in the Arctic tundra where, despite relatively simple food webs, it is still unclear which forces dominate in this ecosystem. Our primary goal was to assess the extent to which a tundra food web was dominated by plant-herbivore or predator-prey interactions. Based on a 17-year (1993-2009) study of terrestrial wildlife on Bylot Island, Nunavut, Canada, we developed trophic mass balance models to address this question. Snow Geese were the dominant herbivores in this ecosystem, followed by two sympatric lemming species (brown and collared lemmings). Arctic foxes, weasels, and several species of birds of prey were the dominant predators. Results of our trophic models encompassing 19 functional groups showed that <10% of the annual primary production was consumed by herbivores in most years despite the presence of a large Snow Goose colony, but that 20-100% of the annual herbivore production was consumed by predators. The impact of herbivores on vegetation has also weakened over time, probably due to an increase in primary production. The impact of predators was highest on lemmings, intermediate on passerines, and lowest on geese and shorebirds, but it varied with lemming abundance. Predation of collared lemmings exceeded production in most years and may explain why this species remained at low density. In contrast, the predation rate on brown lemmings varied with prey density and may have contributed to the high-amplitude, periodic fluctuations in the abundance of this species. Our analysis provided little evidence that herbivores are limited by primary production on Bylot Island. In contrast, we measured strong predator-prey interactions, which supports the hypothesis that this food web is primarily controlled by top-down forces. The presence of allochthonous resources subsidizing top predators and the absence of large herbivores may partly explain the predominant role of predation in this low-productivity ecosystem.

Impact of food and predation on the snowshoe hare cycle.

Snowshoe hare populations in the boreal forests of North America go through 10-year cycles. Supplemental food and mammalian predator abundance were manipulated in a factorial design on 1-square-kilometer areas for 8 years in the Yukon. Two blocks of forest were fertilized to test for nutrient effects. Predator exclosure doubled and food addition tripled hare density during the cyclic peak and decline. Predator exclosure combined with food addition increased density 11-fold. Added nutrients increased plant growth but not hare density. Food and predation together had a more than additive effect, which suggests that a three-trophic-level interaction generates hare cycles.

Ecosystem experiments.

Experimental manipulations of entire ecosystems have been conducted in lakes, catchments, streams, and open terrestrial and marine environments. Experiments have addressed applied problems of ecosystem management and complex responses of communities and ecosystems to perturbations. In the course of some experiments, environmental indicators and models have been developed and tested. Surprising results with implications for ecological understanding and management are common.

Population cycles in small rodents.

We conclude that population fluctuations in Microtus in southern Indiana are produced by a syndrome of changes in birth and death rates similar to that found in other species of voles and lemmings. The mechanisms which cause the changes in birth and death rates are demolished by fencing the population so that no dispersal can occur. Dispersal thus seems critical for population regulation in Microtus. Because most dispersal occurs during the increase phase of the population cycle and there is little dispersal during the decline phase, dispersal is not directly related to population density. Hence the quality of dispersing animals must be important, and we have found one case of increased dispersal tendency by one genotype. The failure of population regulation of Microtus in enclosed areas requires an explanation by any hypothesis attempting to explain population cycles in small rodents. It might be suggested that the fence changed the predation pressure on the enclosed populations. However, the fence was only 2 feet (0.6 meter) high and did not stop the entrance of foxes, weasels, shrews, or avian predators. A striking feature was that the habitat in the enclosures quickly recovered from complete devastation by the start of the spring growing season. Obviously the habitat and food quality were sufficient to support Microtus populations of abnormally high densities, and recovery of the habitat was sufficiently quick that the introduction of new animals to these enclosed areas resulted in another population explosion. Finally, hypotheses of population regulation by social stress must account for the finding that Microtus can exist at densities several times greater than normal without "stress" taking an obvious toll. We hypothesize that the prevention of dispersal changes the quality of the populations in the enclosures in comparison to those outside the fence. Voles forced to remain in an overcrowded fenced population do not suffer high mortality rates and continue to reproduce at abnormally high densities until starvation overtakes them. The initial behavioral interactions associated with crowding do not seem sufficient to cause voles to die in situ. What happens to animals during the population decline? Our studies have not answered this question. The animals did not appear to disperse, but it is possible that the method we used to measure dispersal (movement into a vacant habitat) missed a large segment of dispersing voles which did not remain in the vacant area but kept on moving. Perhaps the dispersal during the increase phase of the population cycle is a colonization type of dispersal, and the animals taking part in it are likely to stay in a new habitat, while during the population decline dispersal is a pathological response to high density, and the animals are not attracted to settling even in a vacant habitat. The alternative to this suggestion is that animals are dying in situ during the decline because of physiological or genetically determined behavioral stress. Thus the fencing of a population prevents the change in rates of survival and reproduction, from high rates in the increase phase to low rates in the decline phase, and the fenced populations resemble "mouse plagues." A possible explanation is that the differential dispersal of animals during the phase of increase causes the quality of the voles remaining at peak densities in wild populations to be different from the quality of voles at much higher densities in enclosures. Increased sensitivity to density in Microtus could cause the decline of wild populations at densities lower than those reached by fenced populations in which selection through dispersal has been prevented. Fencing might also alter the social interactions among Microtus in other ways that are not understood. The analysis of colonizing species by MacArthur and Wilson (27) can be applied to our studies of dispersal in populations of Microtus. Groups of organisms with good dispersal and colonizing ability are called r strategists because they have high reproductive potential and are able to exploit a new environment rapidly. Dispersing voles seem to be r strategists. Young females in breeding condition were over-represented in dispersing female Microtus (17). The Tf(C)/Tf(E) females, which were more common among dispersers during the phase of population increase (Fig. 6), also have a slight reproductive advantage over the other Tf genotypes (19). Thus in Microtus populations the animals with the highest reproductive potential, the r strategists, are dispersing. The segment of the population which remains behind after the selection-via-dispersal are those individuals which are less influenced by increasing population densities. These are the individuals which maximize use of the habitat, the K strategists in MacArthur and Wilson's terminology, or voles selected for spacing behavior. Thus we can describe population cycles in Microtus in the same theoretical framework as colonizing species on islands. Our work on Microtus is consistent with the hypothesis of genetic and behavioral effects proposed by Chitty (6) (Fig. 7) in that it shows both behavioral differences in males during the phases of population fluctuation and periods of strong genetic selection. The greatest gaps in our knowledge are in the area of genetic-behavioral interactions which are most difficult to measure. We have no information on the heritability of aggressive behavior in voles. The pathways by which behavioral events are translated into physiological changes which affect reproduction and growth have been carefully analyzed by Christian and his associates (28) for rodents in laboratory situations, but the application of these findings to the complex field events described above remains to be done. Several experiments are suggested by our work. First, other populations of other rodent species should increase to abnormal densities if enclosed in a large fenced area (29). We need to find situations in which this prediction is not fulfilled. Island populations may be an important source of material for such an experiment (30). Second, if one-way exit doors were provided from a fenced area, normal population regulation through dispersal should occur. This experiment would provide another method by which dispersers could be identified. Third, if dispersal were prevented after a population reached peak densities, a normal decline phase should occur. This prediction is based on the assumption that dispersal during the increase phase is sufficient to ensure the decline phase 1 or 2 years later. All these experiments are concerned with the dispersal factor, and our work on Microtus can be summarized by the admonition: study dispersal.

Lysyl oxidase copper-talon complex: a model.

The translated primary amino-acid sequences from human genomic and human, rat and mouse lysyl oxidase cDNAs were subjected to computer comparison. This revealed a highly-conserved primary structure and similar computer-predicted secondary structures. A prototypical lysyl oxidase structural model was reconciled with the known physical, chemical and biological properties. Analysis of the post-translationally-modified and proteolytically-processed mature enzyme model revealed a copper coordination complex that may be contained as part of the active site. This integral copper coordination complex resembles a talon. The proposed model should facilitate the elucidation of these and other structural and functional relationships within the lysyl oxidase molecule.

Mammalian cycles: internally defined periods and interaction-driven amplitudes.

The cause of mammalian cycles-the rise and fall of populations over a predictable period of time-has remained controversial since these patterns were first observed over a century ago. In spite of extensive work on observable mammalian cycles, the field has remained divided upon what the true cause is, with a majority of opinions attributing it to either predation or to intra-species mechanisms. Here we unite the eigenperiod hypothesis, which describes an internal, maternal effect-based mechanism to explain the cycles' periods with a recent generalization explaining the amplitude of snowshoe hare cycles in northwestern North America based on initial predator abundance. By explaining the period and the amplitude of the cycle with separate mechanisms, a unified and consistent view of the causation of cycles is reached. Based on our suggested theory, we forecast the next snowshoe hare cycle (predicted peak in 2016) to be of extraordinarily low amplitude.

Co-expression of estrogen and thyroid hormone receptors in individual hypothalamic neurons.

Estrogen receptors (ER) and thyroid hormone receptors (TR) are members of the nuclear receptor family of transcription factors that induce or repress the expression of target genes. Previous behavioral studies in female rodents have demonstrated that thyroid hormones can antagonize the effects of estrogen in the central nervous system (CNS), particularly by attenuating estrogen's ability to facilitate reproductive behaviors. Additional molecular studies have suggested a mechanism for this antagonism by showing that ligand-activated ER alpha and TRs have the potential to interact in their transcriptional controls. Although the expression patterns of ER alpha and TRs in the rodent brain appear to overlap in behaviorally relevant areas, it remained to be determined whether these two classes of proteins coexist in vivo at the level of single neurons. To address this possibility, we employed a highly sensitive double-label in situ hybridization technique using digoxigenin and (35)S-labeled cRNA probes to analyze, in detail, the expression of ER alpha mRNA with TR alpha 1 and TR alpha 2 mRNAs in the same neurons of the ovariectomized (OVX) adult mouse brain. Our results demonstrate that a large majority of the ER alpha-positive neurons also expresses TR alpha 1 and TR alpha 2 mRNAs. Quantitative examination of the cellular expression in the ventromedial and arcuate nuclei of the hypothalamus (VMH and Arc) showed that 81.5% and 80.5% of the neurons endowed with ER alpha mRNA also contain TR alpha 1 and TR alpha 2 mRNAs, respectively. In the amygdala, more than 60.5% and 67% of ER alpha-positive cells also contain TR alpha 1 and TR alpha 2 mRNAs, respectively. These findings provide the first anatomical evidence that ER and TR can be found in the same neurons, including hypothalamic neurons. This coexpression of ER alpha and TR provides the cellular basis for a new level of neuronal integration in a brain region where estrogens control female reproductive behaviors.

Reproductive changes in fluctuating house mouse populations in southeastern Australia.

House mice (Mus domesticus) in the Victorian mallee region of southeastern Australia show irregular outbreaks. Changes in reproductive output that could potentially drive changes in mouse numbers were assessed from 1982 to 2000. Litter size in females is positively correlated with body size. When standardized to an average size female, litter size changes seasonally from highest in spring to lowest in autumn and winter. Litter size is depressed throughout breeding seasons that begin when the abundance of mice is high, but is similar in breeding seasons over which the abundance of mice increases rapidly or remains low. Breeding begins early and is extended on average by about five weeks during seasons when mouse abundance increases rapidly. The size at which females begin to reproduce is larger during breeding seasons that begin when mouse abundance is high. An extended breeding season that begins early in spring is necessary for the generation of a house mouse plague, but it is not in itself sufficient. Reproductive changes in outbreaks of house mice in Australia are similar but not identical to reproductive changes that accompany rodent population increases in the Northern Hemisphere. We conclude that food quality, particularly protein, is a probable mechanism driving these reproductive changes, but experimental evidence for field populations is conflicting.

Adjustment of offspring sex ratios in relation to the availability of resources for philopatric offspring in the common brushtail possum.

The local-resource-competition hypothesis predicts that where philopatric offspring compete for resources with their mothers, offspring sex ratios will be biased in favour of the dispersing sex. This should produce variation in sex ratios between populations in relation to differences in the availability of resources for philopatric offspring. However, previous tests of local resource competition in mammals have used indirect measures of resource availability and have focused on sex-ratio variation between species or individuals rather than between local populations. Here, we show that the availability of den sites predicts the offspring sex ratio in populations of the common brushtail possum. Female possums defend access to dens, and daughters, but not sons, occupy dens within their mother's range. However, the abundances of possums in our study areas were determined principally by food availability. Consequently, in food-rich areas with a high population density, the per-capita availability of dens was low, and the cost of having a daughter should have been high. This cost was positively correlated with male bias in the sex ratio at birth. Low per capita availability of dens was correlated with male bias in the sex ratio at birth.

Expression of the SCAMP-4 gene, a new member of the secretory carrier membrane protein family, is repressed by progesterone in brain regions associated with female sexual behavior.

Rodent female reproductive behavior is facilitated by the genomic targets of estrogen (E) and progesterone (P) in neuroendocrine regions of the brain. Using the differential display-PCR technique to identify these targets we discovered a novel hormone-sensitive mRNA in the female rat brain that is substantially reduced in the ventromedial hypothalamus (VMH) after 3 h of P treatment, following 24 h of E priming. Northern blots show that it is a single transcript of approximately 1.7 kb. The sequence of the corresponding full-length cDNA indicates that this gene is the rat homolog of mouse SCAMP-4, the fourth member identified in a family of proteins known as secretory carrier membrane proteins (SCAMPs). In situ hybridization studies show that SCAMP-4 mRNA is relatively low throughout the rat forebrain, with the highest levels observed in the VMH, habenula and hippocampus. The SCAMP-4 message is also less abundant in the habenula and VMH during proestrus, when circulating levels of E and P are at their peak, than during diestrus-1 when circulating hormone levels are low. Amino acid sequence analysis indicates that SCAMP-4 lacks the putative calcium binding and leucine zipper structures, as well as protein-protein interacting NPF domains common among most SCAMP family members, but is the only member identified to date to contain a putative protein kinase C (PKC) phosphorylation site. Fluorescent microscopy of cells transfected with a SCAMP-4/GFP fusion construct reveals distinct fluorescence in subcellular aggregates that may contain secretory vesicles. In addition to our results in the VMH, the finding of high levels of SCAMP-4 message in the habenula, a brain area rich in mast cells, together with previous reports linking mast cell secretion with courtship behavior also suggest a possible role for SCAMP-4 in reproductive behaviors associated with mast cell activity in the central nervous system (CNS).

Effects of extra food on Peromyscus and Clethrionomys populations in the southern Yukon.

If food supply limits density in rodent populations, the addition of supplemental food ought to increase population size. From May to September we added food on 2-hectare areas of white spruce forest in the southern Yukon. In 1977, we used oats with no measurable impact. In 1978 and 1979 we used sunflower seeds and doubled or tripled the population densities of Peromyscus maniculatus and Clethrionomys rutilus. Supplemental feeding with sunflower seeds increased juvenile production in both species, probably by increasing early juvenile survival. The breeding season ended at the same time on experimental and control areas, and the onset of maturity in juveniles was not affected by feeding. Survival of adult rodents was not improved by feeding. Immigration into sunflower seed areas was very high, and was the major factor producing the increase in population density. Body weight was not changed by feeding. Food supply is thus one factor limiting population density in these subarctic small mammals, but we do not know why supplemental food produces no more than a 2- to 3-fold effect on densities.

Can predation cause the 10-year hare cycle?

We relate causes of mortality of snowshoe hares to density of hares over an 8-year period that included a peak in numbers. We then use simulation modeling to examine whether these density-dependent relationships could produce changes in hare density similar to those observed in our study are in Yukon, Canada.Predation during winter was the largest source of mortality for snowshoe hares at Kluane, Yukon during 1978-84. There was a one-year lag in the response of winter predation mortality rate to hare density. There was a two-year lag in the response of winter mortality not caused by predators to hare density.A simple simulation model with density-dependent predation produced 8-11 year cycles only within a narrow range of parameters that are inconsistent with data from the Kluane region. However, a simulation model that predicted winter mortality rates using a delayed density-dependent numerical response and a Type II functional response by predators, produced 8-11 year cycles within the range of parameter values measured in our study. Yet another simulation model that predicted both summer and winter mortality rates using a delayed density-dependent numerical response and a Type II functional response by predators, did not produce 8-11 year cycles within the range of parameter values measured in our study. Lack of data on juvenile mortality may be one reason for this result.

Monitoring coyote population dynamics by genotyping faeces.

Reliable population estimates are necessary for effective conservation and management, and faecal genotyping has been used successfully to estimate the population size of several elusive mammalian species. Information such as changes in population size over time and survival rates, however, are often more useful for conservation biology than single population estimates. We evaluated the use of faecal genotyping as a tool for monitoring long-term population dynamics, using coyotes (Canis latrans) in the Alaska Range as a case study. We obtained 544 genotypes from 56 coyotes over 3 years (2000-2002). Tissue samples from all 15 radio-collared coyotes in our study area had > or = 1 matching faecal genotypes. We used flexible maximum-likelihood models to study coyote population dynamics, and we tested model performance against radio telemetry data. The staple prey of coyotes, snowshoe hares (Lepus americanus), dramatically declined during this study, and the coyote population declined nearly two-fold with a 1(1/2)-year time lag. Survival rates declined the year after hares crashed but recovered the following year. We conclude that long-term monitoring of elusive species using faecal genotyping is feasible and can provide data that are useful for wildlife conservation and management. We highlight some drawbacks of standard open-population models, such as low precision and the requirement of discrete sampling intervals, and we suggest that the development of open models designed for continuously collected data would enhance the utility of faecal genotyping as a monitoring tool.

Are big mammals simply little mammals writ large?

Populations are regulated intrinsically (self-regulated) when the animals lower their rate of increase behaviorally or physiologically as a reaction to rising density. They are regulated extrinsically if the equilibrium is a mechanical consequence of interaction between the population and the organisms providing its food. We suggest that, at least for mammalian herbivores, self-regulation is unlikely to evolve unless the population's intrinsic rate of increase exceeds about 0.45 on a yearly basis. That value corresponds to a body weight of about 30 kg, the intrinsic rate being related inversely to body weight by r m=1.5 W(-0.36) with W in kg.The two dynamic strategies, self-regulation and extrinsic regulation, should enforce a bimodality of the frequency distribution of observed intrinsic rates of increase. This in turn might be reflected in a bimodality of body sizes, the smaller herbivores constituting the lower mode generally showing intrinsic regulation and the larger herbivores of the upper mode generally being regulated by extrinsic mechanisms. There is some empirical support for these predictions but it is by no means clearcut.Mechanisms of self-regulation can evolve either by individual or group selection. Individual selection may act in two ways. By inhibiting their neighbours with some form of interference, individuals may increase their relative fitness without increasing their reproductive rate. Alternatively, individual selection may raise the absolute fitness of individuals and thereby raise the populations's intrinsic rate of increase. The population is destabilized if that process continues beyond a certain threshold and the population is then at significant risk of extinction at the troughs of the consequent oscillations. Selection between such populations will favour those carrying the beginnings of a self-regulating mechanism, and with that mechanism strengthened and fixed by continuing group selection, individual selection is again freed of the dynamic restraints on raising further the intrinsic rate of increase.