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.

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.

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.

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.

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.

Body size, age and paternity in common brushtail possums (Trichosurus vulpecula).

Sexual selection should produce sexual size dimorphism in species where larger members of one sex obtain disproportionately more matings. Recent theory suggests that the degree of sexual size dimorphism depends on physical and temporal constraints involving the operational sex ratio, the potential reproductive rate and the trade-off between current reproductive effort and residual reproductive value. As part of a large-scale experiment on dispersal, we investigated the mating system of common brushtail possums inhabiting old-growth Eucalyptus forest in Australia. Paternity was assigned to 20 of 28 pouch-young (maternity known) genotyped at six microsatellite loci. Male mating success was strongly related to body size and age; male body weight and age being highly correlated. Despite disproportionate mating success favouring larger males, sexual size dimorphism was only apparent among older animals. Trapping and telemetry indicated that the operational sex ratio was effectively 1 : 1 and the potential reproductive rate of males was at most four times that of females. Being larger appeared to entail significant survival costs because males 'died-off' at the age at which sexual size dimorphism became apparent (8-9 years). Male and female home ranges were the same size and males appeared to be as sedentary as females. Moreover, longevity appears to be only slightly less important to male reproductive success than it is to females. It is suggested that a sedentary lifestyle and longevity are the key elements constraining selection for greater sexual size dimorphism in this 'model' medium-sized Australian marsupial herbivore.

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.

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.

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.

Spatial structure of lemming populations (Dicrostonyx groenlandicus) fluctuating in density.

The pattern and scale of the genetic structure of populations provides valuable information for the understanding of the spatial ecology of populations, including the spatial aspects of density fluctuations. In the present paper, the genetic structure of periodically fluctuating lemmings (Dicrostonyx groenlandicus) in the Canadian Arctic was analysed using mitochondrial DNA (mtDNA) control region sequences and four nuclear microsatellite loci. Low genetic variability was found in mtDNA, while microsatellite loci were highly variable in all localities, including localities on isolated small islands. For both genetic markers the genetic differentiation was clear among geographical regions but weaker among localities within regions. Such a pattern implies gene flow within regions. Based on theoretical calculations and population census data from a snap-trapping survey, we argue that the observed genetic variability on small islands and the low level of differentiation among these islands cannot be explained without invoking long distance dispersal of lemmings over the sea ice. Such dispersal is unlikely to occur only during population density peaks.

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).

A membrane-associated progesterone-binding protein, 25-Dx, is regulated by progesterone in brain regions involved in female reproductive behaviors.

The ventromedial hypothalamus (VMH) plays a central role in the regulation of the female reproductive behavior lordosis, a behavior dependent upon the sequential activation of receptors for the ovarian steroid hormones estradiol (E) and progesterone (P). These receptors function as transcription factors to alter the expression of target genes. To discover behaviorally relevant genes targeted by E and P in the VMH, we used the differential display PCR to identify messenger RNAs that are differentially expressed in the hypothalamus of ovariectomized (ovx) rats treated with E alone compared with ovariectomized rats treated with E and P. We show here that one interesting mRNA within the hypothalamus that is repressed by P after E priming encodes the protein 25-Dx, the rat homolog of the human membrane-associated P-binding protein Hpr6.6. Neurons in the brain containing the highest levels of 25-Dx are located in several nuclei of the basal forebrain, including the VMH. 25-Dx expression is also higher in the hypothalamus of female P receptor "knockout" mice than in their wild-type littermates. These findings suggest a mechanism in which the activation of nuclear P receptor represses expression of a membrane P receptor, 25-Dx, during lordosis facilitation.

Phylogeography and mitochondrial DNA (mtDNA) diversity in North American collared lemmings (Dicrostonyx groenlandicus).

Variation in the nucleotide sequence of the mitochondrial control region (250 bp) and the cytochrome b region (870 bp) was examined in collared lemmings (Dicrostonyx groenlandicus) from 19 localities in northern Alaska and the Canadian Arctic. The division of D. groenlandicus in two phylogeographical groups with limited divergence across the Mackenzie River is consistent with the separation of this species in more than one refugial area located to the northwest of the Laurentide ice sheet during the last glaciation. Populations of D.groenlandicus from formerly glaciated areas are no less variable than those in nonglaciated areas. Instead, the low intrapopulation and intraregional diversity estimates in D. groenlandicus are probably a result of regional bottleneck events due to range contractions during Holocene warming events. These results are consistent with findings previously reported on collared lemmings (D. torquatus) from the Eurasian Arctic.

The prevalence of viral antibodies during a large population fluctuation of house mice in Australia.

We studied the seroprevalence of three viruses (mouse cytomegalovirus (MCMV), minute virus of mice (MVM), and mouse parvovirus (MPV)) in house mice (Mus domesticus) in 1995 7. In the first year average mouse density was less than 1 mouse/ha. From November 1995 to May 1996 the population increased at an average rate of 7% per week, a doubling time of about 10 weeks. From August 1996 to May 1997 the population increased at an average rate of 10% per week, a doubling time of about 7.5 weeks. From a peak around 250 mice/ha in May 1997, the mouse population fell 19% per week to 5 mice/ha in October 1997. The seroprevalence for all three viruses varied dramatically over time. MCMV had the highest seroprevalence (61.7%), followed by MVM (8.5%) and MPV (18.4%). Time series data indicated that MCMV spread rapidly through the population of mice once trap success was greater than 14% (40-100 mice/ha). By contrast MVM and MPV seroprevalence occurred with a 2-3 month and 3-4 month time lag, respectively. The current study supports the contention that MCMV would be a good carrier for an immunocontraceptive vaccine for controlling field populations of mice.

The 70-kDa heat shock cognate protein (Hsc73) gene is enhanced by ovarian hormones in the ventromedial hypothalamus.

Estrogen (E) and progesterone (P) orchestrate many cellular responses involved in female reproductive physiology, including reproductive behaviors. E- and P-binding neurons important for lordosis behavior have been located within the ventromedial hypothalamus (VMH), and several hormone-responsive genes have been observed there as well. In attempts to identify additional E- and P-responsive genes in the VMH that may contribute to sexual behaviors, we used the differential display mRNA screening technique. One of the genes identified encodes the 73-kDa heat shock cognate protein (Hsc73). Quantitative in situ hybridization analysis of brains from naturally cycling female rats revealed a significant increase in Hsc73 mRNA in the VMH and arcuate nucleus of animals during proestrus compared with those at diestrus-1. To confirm that these increases were steroid hormone dependent, we compared vehicle-treated ovariectomized females with ovariectomized females treated with estradiol benzoate and P. Northern analysis and in situ hybridizations showed that the Hsc73 gene is enhanced by E and P in the pituitary and subregions of the VMH. Incidentally, by examining the primary amino acid sequence of rat, human, and chicken progesterone receptors, we noticed that putative Hsc73 binding sites are conserved across species with similar sites existing in the androgen and glucocorticoid receptors. Together these findings suggest a possible mechanism through which E could influence the activities of progesterone, androgen, and glucocorticoid receptors, by enhancing the expression of Hsc73 in cells where these proteins colocalize.

From patterns to processes: phase and density dependencies in the Canadian lynx cycle.

Across the boreal forest of North America, lynx populations undergo 10-year cycles. Analysis of 21 time series from 1821 to the present demonstrates that these fluctuations are generated by nonlinear processes with regulatory delays. Trophic interactions between lynx and hares cause delayed density-dependent regulation of lynx population growth. The nonlinearity, in contrast, appears to arise from phase dependencies in hunting success by lynx through the cycle. Using a combined approach of empirical, statistical, and mathematical modeling, we highlight how shifts in trophic interactions between the lynx and the hare generate the nonlinear process primarily by shifting functional response curves during the increase and the decrease phases.

Population regulation in snowshoe hare and Canadian lynx: asymmetric food web configurations between hare and lynx.

The snowshoe hare and the Canadian lynx in the boreal forests of North America show 9- to 11-year density cycles. These are generally assumed to be linked to each other because lynx are specialist predators on hares. Based on time series data for hare and lynx, we show that the dominant dimensional structure of the hare series appears to be three whereas that of the lynx is two. The three-dimensional structure of the hare time series is hypothesized to be due to a three-trophic level model in which the hare may be seen as simultaneously regulated from below and above. The plant species in the hare diet appear compensatory to one another, and the predator species may, likewise, be seen as an internally compensatory guild. The lynx time series are, in contrast, consistent with a model of donor control in which their populations are regulated from below by prey availability. Thus our analysis suggests that the classic view of a symmetric hare-lynx interaction is too simplistic. Specifically, we argue that the classic food chain structure is inappropriate: the hare is influenced by many predators other than the lynx, and the lynx is primarily influenced by the snowshoe hare.

Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response.

Progressive tissue necrosis is a unique reaction to spinal cord trauma in which the site of injury is gradually transformed into a large, cavity-filled lesion. The earliest histopathological changes after injury include a widely disseminated extravasation of erythrocytes and neutrophils. To test whether such an inflammatory reaction might initiate progressive necrosis, we examined the effects of the following anti-inflammatory treatments: allopurinol (Ap) to inhibit injury-induced xanthine oxidase, indomethacin (I) or naproxen to inhibit constitutive and inducible cyclooxygenase, aminoguanidine (Ag) to inhibit inducible nitric oxide synthase, pregnenolone (P) as a precursor steroid, and a bacterial lipopolysaccharide (L) to stimulate secretory activities of glial cells and macrophages. The spinal cord of adult rats was crushed at T8 with jeweler's forceps and, after 3 or 21 days of treatment, the cords were studied quantitatively by light microscopical image analysis. Ag, Ag+I, or Ap significantly reduced the size of the primary lesion at 3 days postoperatively, while P+L+I did so only after 21 days of treatment. A secondary lesion developed in the dorsal column and gradually extended for many millimeters rostral and caudal from the primary lesion. The size of the dorsal column lesion was diminished by 3-day treatment with Ap and by 21-day treatment with Ap or P+L+I, but Ag or Ag+I had no effect. We conclude that (a) progressive necrosis is initiated and maintained by inflammatory mechanisms and (b) for this reason, treatment with specific anti-inflammatory agents selectively attenuates various components of the necrotizing process.

The cerebellum-enriched form of nuclear factor I is functionally different from ubiquitous nuclear factor I in glial-specific promoter regulation.

Nuclear factor I (NFI) binding sites are present in a wide range of brain-specific gene enhancer and promoter sequences and appear to play a role in establishing cell type-specific expression within the CNS. The precise mechanisms used by various members of the NFI family of proteins to confer brain-specific expression are unclear. We have addressed this issue by comparing the transactivating capabilities of two forms of NFI in directing gliotropic expression from two different JC virus (JCV) promoter configurations. The JCV is an opportunistic pathogen of humans that causes lytic destruction of the oligodendrocytes and thus demyelination in immunocompromised patients. Our results show that the cerebellum-enriched form of NFI (NFI-A1) transactivates two gliotropic JCV early promoters to a greater extent than the ubiquitous form of NFI (NFI-C1). Activation by NFI-A1 was dramatically greater in glial than in nonglial cells. These results suggest that NFI proteins direct brain-specific expression through combinatorial interactions with cell specific coactivators and/or transcription factors that recognize adjacent sites within brain specific promoters.