Changes in population structure and reproduction during a 3-yr population cycle of voles

Cyclic changes in population growth rate are caused by changes in survival and/or reproductive rate. To find out whether cyclic changes in reproduction are an important part of the mechanism causing cyclic fluctuations in small mammal populations, we studied changes in the population structure and reproduction of field voles ( Microtus agrestis ), sibling voles ( M. rossiaemeridionalis ), bank voles ( Clethrionomys glareolus ), and common shrews ( Sorex araneus ) in western Finland during 1984–1992, in an area with 3-yr vole cycles. We also modelled the population growth of voles using parameter values from this study. The animals studied were collected by snap trapping in April, May, June, August, September, and, during 1986–1990, also in October. We found several phase-related differences in the population structure (age structure, sex ratio, proportion of mature individuals) and reproduction (litter size, length of the breeding season) of voles. In non-cyclic common shrews, the only significant phase-related difference was a lower proportion of overwintered individuals in the increase phase. According to the analyses and the vole model, phase-related changes in litter size had only a minor impact on population growth rate. The same was true for winter breeding in the increase phase. The length and intensity of the summer breeding season had an effect on yearly population growth but this impact was relatively weak compared to the effect of cyclic changes in survival. The population increase rates of Microtus were delayed dependent on density (8–12-month time lag). Our results indicate that cyclic changes in reproduction are not an important part of the mechanism driving cyclic fluctuations in vole populations. Low survival of young individuals appeared to play an important role in the shift from the peak to the decline phase in late summer and early autumn.     

Spatial dynamics in fluctuating vole populations

Summary Patterns and consistency of distribution, spatial and temporal components, and the extent of spatial density-dependence were compared between semi-cyclic and cyclic populations of the vole species Clethrionomys glareolus and Microtus agrestis in south-central and north Sweden. Cyclic populations were less clumped and only C. glareolus showed a consistency in distribution between years. Spatial variation contributed little to the distributions in cyclic populations while the spatial and temporal variations were of the same magnitude in the semi-cyclic populations. The latter populations could be subdivided into areas with different spatial and temporal components. The spatial density-dependence increased from increase to decline years in C. glareolus but not in M. agrestis, which differed conspicuously between reregions in population development. The data imply that spatial dynamics should be considered as much as temporal ones for non-cyclic populations, that the same regulating or limiting factors may be at work in both spatial and temporal components and that, in addition, social behaviour may be important in explaining spatial dynamics. However, the latter effects may be fairly species-specific.     

Breeding of captive bank voles (Clethrionomys glareolus) related to dynamics of source populations

Proportionately fewer female bank voles from cyclic or dense populations bred than did females from sparse or non-cyclic populations when brought into a laboratory and kept as monogamous pairs for at least 1 year. Similarly, fewer litters were produced by females from cyclic or dense populations. Breeding frequency and litter production did not differ in the second laboratory generation. Large variance in litter numbers indicated further changes in reproduction in response to the laboratory environment. Certain differences between origins still persisted after long-term laboratory breeding. The regional variations between field-born animals are most parsimoniously explained by differences in sensitivity to density.     

Seed production and outbreaks of non-cyclic rodent populations in deciduous forests

Summary In a 10-year study period, outbreaks of the bank vole, Clethrionomys glareolus, Schreber only occurred in years following huge seed production of European beech, Fagus sylvatica. Intensive winter reprodution preceded the outbreaks, in contrast to a normal breeding season from April through September. No winter reproduction occurred in nearby populations from habitats without mast production. During the winter, the average weight of C. glareolus remained high in the mast forests and the age structure resembled that of a summer breeding population. Despite excess energy requirements of winter breeding, survival rates were similar to that of non-breeding winter populations. In mast years, rodent consumption in the beech forest was estimated as 1.0–10.3% of endosperm production available to postdispersal seed predators. Between mast years rodent consumption made up 30–100% of endosperm production available. Mast years occurred at irregular intervals and seed production seems to be synchronized between individual trees over large areas and induced by climatic events. These phenomena lead to seed predator satiation.     

Reproduction of the bank vole, Clethrionomys glareolus, in northern and southern Sweden during several seasons and in different phases of the vole population cycle

The breeding biology of the bank vole was studied in northern and southern populations in Sweden in the years 1973–76. Trapped specimens supplied organ weights and histological data, which were utilized to describe the breeding season, number and size of litters, reproductive losses, spermatogenesis, and sexual maturation. In the north the populations are cyclic. During the increase phase of the cycle the breeding season was long, litter sizes and gonad weights were large, and there was maturation of yearlings in the summer. During the peak phase reproduction was impaired in all these respects. In southern Sweden there was no cyclicity, and the reproductive events varied less, but in 1976 the litters were larger than usual and the season was much extended.
In the south the voles born during the early part of the season regularly became sexually mature during their first summer. The differences in reproductive biology are related to population dynamics and discussed in terms of different hypotheses concerning vole population cyclicity.     

Do intrinsic or extrinsic factors limit reproduction in cyclic populations of Clethrionomys glareolus and C. rufocanus?

Changes in reproduction and functional age structure of females in cyclic populations of Clethrionomys glareolus and C. rufocanus were studied by live-trapping individually marked voles during 1980 to 1984 in northern Sweden. A complete population cycle was observed in both species, with a synchronous 'summer-decline' in 1982. In both species, the length of the breeding season became successively shorter towards the peak, and it was extremely short at the decline. When the populations expanding, the density of breeding females increased in a sigmoid way, and thereafter it remained fairly constant throughout the summer. At the decline, the density of breeding females decreased successively from spring to autumn. Year-born females matured and bred in all years except at the decline. Intrinsic factors, such as spacing behaviour of breeding females, are thought to limit the density of breeders in general, but only when the populations are expanding. Other factors such as deteriorating food conditions are more likely to operate at the decline.     

From process to pattern: how fluctuating predation risk impacts the stress axis of snowshoe hares during the 10-year cycle

Predation is a central organizing process affecting populations and communities. Traditionally, ecologists have focused on the direct effects of predation—the killing of prey. However, predators also have significant sublethal effects on prey populations. We investigated how fluctuating predation risk affected the stress physiology of a cyclic population of snowshoe hares (Lepus americanus) in the Yukon, finding that they are extremely sensitive to the fluctuating risk of predation. In years of high predator numbers, hares had greater plasma cortisol levels at capture, greater fecal cortisol metabolite levels, a greater plasma cortisol response to a hormone challenge, a greater ability to mobilize energy and poorer body condition. These indices of stress had the same pattern within years, during the winter and over the breeding season when the hare:lynx ratio was lowest and the food availability the worst. Previously we have shown that predator-induced maternal stress lowers reproduction and compromises offspring’s stress axis. We propose that predator-induced changes in hare stress physiology affect their demography through negative impacts on reproduction and that the low phase of cyclic populations may be the result of predator-induced maternal stress reducing the fitness of progeny. The hare population cycle has far reaching ramifications on predators, alternate prey, and vegetation. Thus, predation is the predominant organizing process for much of the North American boreal forest community, with its indirect signature—stress in hares—producing a pattern of hormonal changes that provides a sensitive reflection of fluctuating predator pressure that may have long-term demographic consequences.     

Density-dependence in the survival and reproduction of Bald Eagles: Linkages to Chum Salmon

During the late 20th Century, due to decreases in both contamination and persecution, bald eagle (Haliaeetus leucocephalus) populations increased dramatically. Currently, mechanisms regulating eagle populations are not well understood. To examine potential regulating processes in the Pacific Northwest, where eagles are no longer primarily regulated by contaminants or direct persecution, we examined bald eagle reproductive success, breeding populations, winter populations, mortality, and salmon stream use. Wintering and breeding eagle populations in south-coastal British Columbia (BC) quadrupled between the early 1980s and the late 1990s, and have since stabilized. Density-dependent declines in reproduction occurred during 1986–2009, but not through changes in site quality. Mid-winter survival was crucial as most mortality occurred then, and models showed that density-dependent reductions in population growth rates were partially due to reduced survival. Wintering eagles in British Columbia fed heavily on chum salmon (Oncorhynchus keta) runs, and then switched to birds in late winter, when mortality was highest. Eagles tended to arrive after the peak in salmon availability at streams in BC as part of a migration associated with salmon streams from Alaska to northern Washington. Eagles were most abundant in southern BC during cold Alaskan winters and in years of high chum salmon availability. We suggest that eagle populations in the Pacific Northwest are currently partially limited by density on the breeding grounds and partially by adult mortality in late winter, likely due to reduced late winter salmon stocks forcing eagles to exploit more marginal prey supplies. Larger eagle populations have affected some local prey populations. © 2011 The Wildlife Society.     

Population dynamics of red-backed voles (<Emphasis Type="Italic">Myodes</Emphasis>) in North America

We review the population dynamics of red-backed voles (Myodes species) in North America, the main deciduous and coniferous forest-dwelling microtines on this continent, and compare and contrast their pattern with that of the same or similar species in Eurasia. We identify 7 long-term studies of population changes in Myodes in North America. Using autoregressive and spectral analysis, we found that only 2 of the 7 show 3- to 5-year cycles like those found in some Eurasian populations. There was no relationship between latitude and cycling. The general lack of cyclicity is associated with two key aspects of their demography that act in tandem: first, poor overwinter survival in most years; second, chronically low densities, with irregular outbreak years. Eight factors might explain why some Myodes populations fluctuate in cycles and others fluctuate irregularly, and we review the evidence for each factor: food supplies, nutrients, predation, interspecific competition, disease, weather, spacing behavior and interactive effects. Of these eight, only food supplies appear to be sufficient to explain the differences between cyclic and non-cyclic populations. Irregular fluctuations are the result of pulsed food supplies in the form of berry crops (M. rutilus) or tree seeds (M. gapperi) linked to weather patterns. We argue that, to understand the cause for the patterns in the respective hemispheres, we must know the mechanism(s) driving population change and this must be linked to rigorous field tests. We suggest that a large-scale, year-round feeding experiment should improve overwintering survival, increase standing densities, and flip non-cyclic Myodes populations into cyclic dynamics that would mimic the patterns seen in the cyclic populations found in parts of Eurasia.     

Density-dependent effects on physical condition and reproduction in North American elk: an experimental test

Density dependence plays a key role in life-history characteristics and population ecology of large, herbivorous mammals. We designed a manipulative experiment to test hypotheses relating effects of density-dependent mechanisms on physical condition and fecundity of North American elk (Cervus elaphus) by creating populations at low and high density. We hypothesized that if density-dependent effects were manifested principally through intraspecific competition, body condition and fecundity of females would be lower in an area of high population density than in a low-density area. Thus, we collected data on physical condition and rates of pregnancy in each experimental population. Our manipulative experiment indicated that density-dependent feedbacks affected physical condition and reproduction of adult female elk. Age-specific pregnancy rates were lower in the high-density area, although there were no differences in pregnancy of yearlings or in age at peak reproduction between areas. Age-specific rates of pregnancy began to diverge at 2 years of age between the two populations and peaked at 6 years old. Pregnancy rates were most affected by body condition and mass, although successful reproduction the previous year also reduced pregnancy rates during the current year. Our results indicated that while holding effects of winter constant, density-dependent mechanisms had a much greater effect on physical condition and fecundity than density-independent factors (e.g., precipitation and temperature). Moreover, our results demonstrated effects of differing nutrition resulting from population density during summer on body condition and reproduction. Thus, summer is a critical period for accumulation of body stores to buffer animals against winter; more emphasis should be placed on the role of spring and summer nutrition on population regulation in large, northern herbivores.     

Geographic variations in life-history traits of the intertidal ocypodid crab Macrophthalmus banzai

Reproductive traits of the mud crab Macrophthalmus banzai were compared in populations from Okinawa (26°13′ N) and Amakusa (32°32′ N). Crabs matured earlier and at a smaller size in Okinawa than in Amakusa, but growth rate did not differ between the two localities. Population density was much higher in Okinawa. Breeding occurred in winter in Okinawa and in summer in Amakusa. In Okinawa, females produced one brood at over 1 year of age and then died. In Amakusa, females produced one brood at over 1 year of age, and one or two broods at around 2 years of age, and then died. Egg weight in the Okinawa population was almost twice that of the Amakusa population. Furthermore, brood weight was larger in Okinawa than in Amakusa. Longevity was 16–19 months in Okinawa and 28–30 months in Amakusa. At high latitudes, the winter low temperature blocks reproduction of M. banzai. At low temperature blocks reproduction of M. banzai. At low latitudes, their short lifespan prevents iterative breeding. Thus, the difference in breeding season greatly affects other life-history traits.     

On the relationship between reproduction,age and survival in two carbid beetles:

Summary In this study the inverse relationship between the amount of reproduction in female carabid beetles and their survival until the next breeding season, suggested by Murdoch (1966), was examined in Pterostichus coerulescens L. and Calathus melanocephalus L. This was tested with individual and differently reproducing females, kept at the same temperature, as well as with groups of females kept at different temperatures, i.e. with very different overall levels of reproduction.No relationship was found between the numbers of eggs laid by individual females and their survival until the next breeding season.The numbers of eggs laid by individual females varies greatly, even under constant and optimal conditions,. In contrast to this, an individual female continues to lay a characteristic number of eggs over several succeeding weeks. The amount of reproduction is highly correlated with temperature when food is optimal. In P. coerulescens there was a positive correlation between the amount of reproduction of the same individuals in two succeeding years, whereas in C. melanocephalus no relationship could be found.Both in the field and in our experiments individuals of P. coerulescens generally live for 3 to 4 years, longer than C. melanocephalus which usually only lives for 2 years. The 3–4 year-old individuals of P. coerulescens die during the breeding season or shortly afterwards, but also during the winter, whereas the 2–3 year-old individuals of C. melanocephalus die during the winter. Males and females show a similar mortality after breeding. The level of reproduction of a population depends on the proportion of old beetles, since especially the very old ones die before the end of the breeding season.We reject the hypothesis of Murdoch because of these data. However, in a different way from that of Murdoch, we also suggest that old beetles are of great importance for the survival of a population, namely that this form of heterogeneity of a population may enhance its stability under varying environmental conditions.Communication No. 204 of the Biological Station, Wijster     

Advances in laying date and increasing population size suggest positive responses to climate change in Common Eiders Somateria mollissima in Iceland

Models of climate change predict that its effects on animal populations will not always be negative, but most studies indicate negative associations between changes in climate and the phenology of animal migration and reproduction. For some populations, however, climate change may render particular environments more favourable, with positive effects on population growth. We used a 30-year population dataset on over 2000 Common Eiders Somateria mollissima at a colony in southwest Iceland to examine the response of this species to climate fluctuations. Eiders are strongly dependent on suitable climatic conditions for successful reproduction and survival. Temperatures in southwest Iceland, in both winter and summer, have generally increased over the past 30 years but have shown considerable fluctuation. We show that females laid earlier following mild winters and that year-to-year variation in the number of nests was related to the temperature during the breeding season 2 years previously. Milder summers could have positive effects on breeding success and offspring survival, producing an increase in nest numbers 2 years later when most Eiders recruit into the breeding population. In this part of their range, Eiders could benefit from a general warming of the climate.     

Population-specific adjustment of the annual cycle in a super-swift trans-Saharan migrant

For migratory birds optimal timing of the onset of reproduction is vital, especially when suitable conditions for reproduction occur only for a short while during the year. With increasing latitude the suitable period becomes shorter and we expect the organization of annual cycle to be more synchronized to the local conditions across individuals of same population. This should result in low variation of arrival and departure date in breeding sites at higher latitudes. We quantify the temporal and geographical variation in pre- and post-breeding migration between individuals from four different populations of alpine swifts Tachymarptis melba along a latitudinal gradient. We tracked 215 individuals in three years with geolocators. The two western and two eastern populations showed separate migratory flyways and places of residence in Africa. Length of stay at the breeding sites was negatively correlated with latitude and differed by more than a month between populations. Duration of migration was similarly short in all populations (median 6.2 days in autumn and 8.7 days in spring). However, variation in timing of migration was unrelated to latitude and individuals everywhere arrived in the same asynchrony at the breeding site.     

Decline of a montane Mediterranean pied flycatcher Ficedula hypoleuca population in relation to climate

Certain populations of long‐distance migratory birds are suffering declines, which may be attributed to effects of climate change. In this article, we have analysed a long‐term (1991–2015) data set on a pied flycatcher Ficedula hypoleuca population breeding in nest‐boxes in a Mediterranean montane oak forest, exploring the trends in population size due to changes in nestling recruitment, female survival and female immigration. We have related these changes in population parameters to local climate, winter NAO index and to breeding density. During the last 25 yr the population has declined by half, mainly in association with a decrease in nestling mass and structural size which had repercussions on the probability of nestling recruitment to the population. Lower local nestling recruitment in certain years was linked to lower female immigration rate in the same years. On the other hand, the local survival of females remained stable throughout the study period. Laying date and breeding success were negatively affected by local temperatures while breeding, recruitment rate likewise by minimum temperature prior to breeding in April. As minimum April temperatures have increased across the study period, this may have affected recruitment and immigration rates negatively. On the other hand, tarsus length and body mass of nestlings were positively associated with winter NAO index, pointing to more global climatic links. Moreover, there was also a negative temporal trend in body mass of adults, implying increasingly difficult conditions for breeding. Declining recruit production in the study area could be attributed to a mismatch between the timing of arrival and breeding in the population, and the peak of food availability in this area.     

Gradients in density variations of small rodents: the importance of latitude and snow cover

Summary Microtine rodents are known to show extreme population variations (cycles) but non-cyclic populations have also been recognized during recent years. The cyclic populations have been widely thought to be regulated by intrinsic mechanisms. However, such predictions for cyclic populations are usually not applicable to non-cyclic ones and extrinsic factors may have to be included in any explanation.A hypothesis that the degree of fluctuations in small rodent numbers is related to the sustainable number of generalist predators was tested on mainly literature data by computing indices of cyclicity for local populations. These indices were related to latitude and snow cover (two measures) as these variables will affect the amount of alternative prey available for these generalists. Within Fennoscandia such indices for Clethrionomys glareolus and Microtus agrestis were clearly positively related to latitude and snow cover. The fraction of populations with summer declines in numbers, characterizing highly cyclic populations, increased in the same way. Cyclicity indices in Great Britain were similar to those in southern Fennoscandia, both areas being poor in snow, but were higher at the same latitudes in eastern Europe with more snow. Indices of density variations were generally low in North American Clethrionomys species and very variable in Microtus species.The gradients observed and differences between continents are interpreted as due to microtine-vegetation interactions in northern European areas poor in generalist predators but with important small mustelid predation, and to similar snowshoe hare-vegetation interactions in mainly Canada-Alaska, where small rodents may serve as alternative prey for numerically fluctuating hare predators, at least in the forests. Western European microtine populations, and probably many others, seem to be regulated by generalist predators.     

Effects of winter food provisioning on the phenotypes of breeding blue tits

Throughout the Western World, huge numbers of people regularly supply food for wild birds. However, evidence of negative impacts of winter feeding on future reproduction has highlighted a need to improve understanding of the underlying mechanisms shaping avian responses to supplementary food. Here, we test the possibility that carry‐over effects are mediated via their impact on the phenotypes of breeding birds, either by influencing the phenotypic structure of populations through changes in winter survival and/or by more direct effects on the condition of breeding birds. Using a landscape‐scale 3‐year study of blue tits (Cyanistes caeruleus), we demonstrate the importance of nutritional composition of supplementary food in determining carry‐over effect outcomes. We show that breeding populations which had access to vitamin E‐rich foods during the previous winter were comprised of individuals with reduced feather carotenoid concentrations, indicative of lower pre‐feeding phenotypic condition, compared to fat‐fed and unfed populations. This suggests that supplementary feeding in winter can result in altered population phenotypic structure at the time of breeding, perhaps by enhancing survival and recruitment of lower quality individuals. However, supplementation of a fat‐rich diet during winter was detrimental to the oxidative state of breeding birds, with these phenotypic differences ultimately found to impact upon reproductive success. Our findings demonstrate the complex nature by which supplementary feeding can influence wild bird populations.     

Population dynamics of the collared lemming and the tundra vole at Pearce Point,Northwest Territories,Canada

From 1987 to 1989 we monitored population changes during summer of the collared lemming (Dicrostonyx groenlandicus) and the tundra vole (Microtus oeconomus) at Pearce Point, Northwest Territories, Canada (69° 48 N, 122° 40 W). Populations on four study areas did not cycle but remained at low density (<3/ha) each year and continued at low numbers for the following 3 years (Reid et al. 1995). Lemming numbers often declined throghout the summer in spite of continous reproduction, and population recovery occurred overwinter. Heavy predation losses of radio-collared lemmings occurred each summer and this lemming population may be trapped in a predator-pit. Collared lemmings breed in winter and only because of winter population growth do these populations persist. Tundra vole numbers increased rapidly in most summers but usually declined overwinter. Tundra voles do not seem able to sustain winter reproduction in this extreme environment and this prevents them from reaching high density because of the short summer. Population growth in both these rodents could be prevented by poor food or by predation losses, and landscape patchiness may also help to prevent population growth. For lemmings we do not think that a shortage of shelter or intrinsic limitations could be restricting population increase at Pearce Point. This is the first detailed study of a non-cyclic collared lemming population.     

Genetic diversity in water frog hybrids (Pelophylax esculentus) varies with population structure and geographic location

Pelophylax esculentus is a hybridogenetic frog originating from matings between P. ridibundus (RR) and P. lessonae (LL). Typically, diploid hybrids (LR) live in sympatry with one of their parental species, upon which they depend for successful reproduction. In parts of their range, however, pure hybrid populations can be found. These hybrid populations have achieved reproductive independence from their parental species by using triploid hybrids (LLR, LRR) rather than LL and RR as their sexual hosts. These different breeding systems also entail differences in reproduction (clonal versus sexual) and hence offer the opportunity to study how genetic diversity is affected by reproductive mode, population structure and geographic location. We investigated 33 populations in the Scania region (South Sweden) and 18 additional populations from Northern and Central Europe. Within both genomes (L, R), genetic variability increases with the potential for recombination and declines from the main species distribution area southeast of the Baltic Sea to the fringe populations northwest of the Baltic Sea. Within the main study area in Scania, genetic diversity is low and decreases from a core area to the periphery. Genetic differentiation between Scania populations is small but significant and best explained by ‘isolation by distance’. Despite the low genetic variability within the discrete genomes, all‐hybrid P. esculentus populations in southern Sweden are apparently not suffering from direct negative fitness effects. This is probably because of its somatic hybrid status, which increases diversity through the combination of genomes from two species.     

Trade-off between reproduction and moult – a comparison of three Fennoscandian pied flycatcher populations

Organisms that reproduce at high latitudes are assumed to have evolved several adaptations to the short summer. For birds, and especially for long-distance migrants, there is a time constraint because both reproduction and moult must be completed before autumn migration. It has therefore been assumed that birds at northern latitudes must initiate their moult during reproduction more often than birds at low latitudes. To investigate how passerine birds breeding at different latitudes allocate their time between reproduction and moult, we compared timing of these activities during three consecutive breeding seasons in three widely separated populations of the pied flycatcher Ficedula hypoleuca. Our results show that the frequency of individuals with moult-breeding overlap, and moult initiation in relation to breeding stage, varied considerably among populations and years. In all three populations, female moult initiation was restricted to the late nestling period. The males had a more pronounced moult-breeding overlap than the females, but its duration was similar in all three study areas. Thus, there was no evidence for a more pronounced moult-breeding overlap at high compared with low latitudes. These results suggest that pied flycatchers sometimes accept a moult-breeding overlap, but that the time gained by having too extensive an overlap between reproduction and moult does not outweigh the associated costs. Long-distance migrants breeding at northern latitudes apparently experience a trade-off between reproduction and somatic investment during moult. We therefore suggest that a pronounced moult-breeding overlap is not a typical strategy used by long-distance migrants to adjust to the short breeding season at northern latitudes. Received: 7 May 1998 / Accepted: 24 August 1998