Otso Huitu

Europe-Wide Dampening of Population Cycles in Keystone Herbivores

Cycling in Unison Many small mammals, especially voles, display semi-regular cycles of population boom and bust. Given the fundamental importance of small mammals as basal consumers and prey, such cycles can have cascading effects in trophic food webs. Cornulier et al. (p. 63) collated raw data from vole populations across Europe collected over the past 18 years. Reduction in winter growth rate was common across a wide variety of habitats with very different local climates, suggesting the presence of a continental-scale climatic driver of vole populations. Synchronicity in vole population fluctuation across Europe suggests a common climatic driver. Suggestions of collapse in small herbivore cycles since the 1980s have raised concerns about the loss of essential ecosystem functions. Whether such phenomena are general and result from extrinsic environmental changes or from intrinsic process stochasticity is currently unknown. Using a large compilation of time series of vole abundances, we demonstrate consistent cycle amplitude dampening associated with a reduction in winter population growth, although regulatory processes responsible for cyclicity have not been lost. The underlying syndrome of change throughout Europe and grass-eating vole species suggests a common climatic driver. Increasing intervals of low-amplitude small herbivore population fluctuations are expected in the future, and these may have cascading impacts on trophic webs across ecosystems.

Predator–induced synchrony in population oscillations of coexisting small mammal species

Comprehensive analyses of long–term (1977–2003) small–mammal abundance data from western Finland showed that populations of Microtus voles (field voles M. agrestis and sibling voles M. rossiaemeridionalis), bank voles (Clethrionomys glareolus) and common shrews (Sorex araneus) fluctuated synchronously in 3 year population cycles. Time–series analyses indicated that interspecific synchrony is influenced strongly by density–dependent processes. Synchrony among Microtus and bank voles appeared additionally to be influenced by density–independent processes. To test whether interspecific synchronization through density–dependent processes is caused by predation, we experimentally reduced the densities of the main predators of small mammals in four large agricultural areas, and compared small mammal abundances in these to those in four control areas (2.5–3 km2) through a 3 year small–mammal population cycle. Predator reduction increased densities of the main prey species, Microtus voles, in all phases of the population cycle, while bank voles, the most important alternative prey of predators, responded positively only in the low and the increase phase. Manipulation also increased the autumn densities of water voles (Arvicola terrestris) in the increase phase of the cycle. No treatment effects were detected for common shrews or mice. Our results are in accordance with the alternative prey hypothesis, by which predators successively reduce the densities of both main and alternative prey species after the peak phase of small–mammal population cycles, thus inducing a synchronous low phase.

WINTER FOOD SUPPLY LIMITS GROWTH OF NORTHERN VOLE POPULATIONS IN THE ABSENCE OF PREDATION

Mathematical models have suggested that population cycles of northern voles are generated by a combined effect of delayed and direct density-dependent mechanisms. Predation is considered to be the most likely mechanism affecting vole populations in a delayed density-dependent manner. We conducted a replicated two-factor experiment with the field vole (Microtus agrestis) during 1999-2001 in western Finland, manipulating both predation rate and winter food supply to evaluate whether a shortage of winter food has the potential to limit the growth of vole populations in a direct density-dependent manner. Vole populations in fenced predator exclosures rapidly attained higher densities than in unfenced areas, with the difference persisting until the end of the experiment. In the first winter, food supplementation increased vole population growth in fenced areas, but not in unfenced areas. The growth of vole populations in both supplemented and nonsupplemented fenced areas became limited in a direct density-dependent manner during the first winter. During the second winter, food supplementation prevented the crash of vole populations within fences, whereas again no obvious effect was found in the areas exposed to predation. Furthermore, supplemental winter food increased the overwinter survival of voles in fenced areas in both winters. Our results indicate that Microtus vole populations that have succeeded in escaping regulation by predators are limited in growth by a lack of winter food. This factor is thus a strong candidate for the direct density dependence inherently necessary for the occurrence of population cycles.

Nonlinear effects of climate on boreal rodent dynamics: mild winters do not negate high-amplitude cycles

Small rodents are key species in many ecosystems. In boreal and subarctic environments, their importance is heightened by pronounced multiannual population cycles. Alarmingly, the previously regular rodent cycles appear to be collapsing simultaneously in many areas. Climate change, particularly decreasing snow quality or quantity in winter, is hypothesized as a causal factor, but the evidence is contradictory. Reliable analysis of population dynamics and the influence of climate thereon necessitate spatially and temporally extensive data. We combined data on vole abundances and climate, collected at 33 locations throughout Finland from 1970 to 2011, to test the hypothesis that warming winters are causing a disappearance of multiannual vole cycles. We predicted that vole population dynamics exhibit geographic and temporal variation associated with variation in climate; reduced cyclicity should be observed when and where winter weather has become milder. We found that the temporal patterns in cyclicity varied between climatically different regions: a transient reduction in cycle amplitude in the coldest region, low-amplitude cycles or irregular dynamics in the climatically intermediate regions, and strengthening cyclicity in the warmest region. Our results did not support the hypothesis that mild winters are uniformly leading to irregular dynamics in boreal vole populations. Long and cold winters were neither a prerequisite for high-amplitude multiannual cycles, nor were mild winters with reduced snow cover associated with reduced winter growth rates. Population dynamics correlated more strongly with growing season than with winter conditions. Cyclicity was weakened by increasing growing season temperatures in the cold, but strengthened in the warm regions. High-amplitude multiannual vole cycles emerge in two climatic regimes: a winter-driven cycle in cold, and a summer-driven cycle in warm climates. Finally, we show that geographic climatic gradients alone may not reliably predict biological responses to climate change.

Female field voles with high testosterone and glucose levels produce male-biased litters

The proximate physiological mechanisms producing the parental ability to vary offspring sex ratio in many vertebrates remain elusive. Recently, high concentrations of maternal testosterone and glucose and low concentrations of maternal corticosterone have been suggested to explain male bias in offspring sex ratio. We examined how these factors affect secondary offspring sex ratio in nondomesticated field voles, Microtus agrestis, while controlling for maternal age, testosterone level of the male and body condition of both the female and the male. We found that females with high preconception serum testosterone and glucose levels produced a male-biased litter, whereas there was no association between maternal corticosterone level and litter sex ratio. Older females produced a bias towards sons, but neither their body condition nor paternal testosterone level correlated with litter sex ratio. Finally, females mated with a high body-condition male tended to deliver a male-biased litter. Our results suggest that several physiological traits of the mother may simultaneously be related to offspring sex ratio in mammals.

Predation on European wild forest reindeer (Rangifer tarandus) by wolves (Canis lupus) in Finland

It is generally accepted that predation by wolves Canis lupus is one of the major factors limiting densities of woodland caribou Rangifer tarandus caribou in North America. Conversely, little is known about the role of European wild forest reindeer R. t. fennicus as wolf prey, or about the influence of wolf predation on populations of this rare subspecies. This relationship was examined in east-central Finland, where wild forest reindeer coexist with moose Alces alces at a numerical ratio of c. 1 reindeer to 1.5 moose. During the study, moose were clearly the primary prey of wolves. Reindeer were, however, an important part of wolf diet in summer, autumn and early winter, when their remains comprised roughly 20–50% of all food items identified in wolf scats. Wolves exhibited a slight preference for reindeer over moose as prey during early winter (November–December) when the reindeer were moving towards their wintering ranges. Virtually no reindeer were killed by wolves during midwinter (January–March). This held also for a pack whose territory was located in the middle of the wintering range of reindeer, where reindeer outnumbered moose during the winter months. After the approximate ratio of wolves to reindeer increased from 0.004 (1998) to 0.02 (2000), wolf predation became the most common source of mortality (50%) for reindeer. The annual net increase in the reindeer population decreased from 13% to 7% because of increased wolf predation. The results indicate that wolf predation was an important factor limiting reindeer population growth. Wolves were, however, unable to prevent entirely the number of reindeer from increasing, partly owing to behavioural traits used by reindeer during winter and calving times.

Landscape effects on temporal and spatial properties of vole population fluctuations.

Populations of northern small rodents have previously been observed to fluctuate in spatial synchrony over distances ranging from tens to hundreds of kilometers between sites. It has been suggested that this phenomenon is caused by common environmental perturbations, mobile predators or dispersal movements. However, very little focus has been given to how the physical properties of the geographic area over which synchrony occurs, such as landscape composition and climate, affect spatial population dynamics. This study reports on the spatial and temporal properties of vole population fluctuations in two areas of western Finland: one composed of large interconnected areas of agricultural farmland interspersed by forests and the other highly dominated by forest areas, containing more isolated patches of agricultural land. Furthermore, the more agricultural area exhibits somewhat milder winters with less snow than the forested area. We found the amplitude of vole cycles to be essentially the same in the two areas, suggesting that the relative amount of predation on small rodents by generalist versus specialist predators is similar in both areas. No seasonal differences in the timing of synchronization were observable for Microtus voles, whereas bank vole populations in field habitats appeared to become synchronized primarily during winter. Microtus populations in field habitats exhibited smaller spatial variation and a higher degree of synchrony in the more continuous agricultural landscape than in the forest-dominated landscape. We suggest that this inter-areal difference is due to differences in the degree of inter-patch connectivity, with predators and dispersal acting as the primary synchronizing agents. Bank vole populations in field habitats were more synchronized within the forest-dominated landscape, most likely reflecting the suitability of the inter-patch matrix and the possibility of dispersal. Our study clearly indicates that landscape composition needs to be taken into account when describing the spatial properties of small rodent population dynamics.

The impact of climate and cyclic food abundance on the timing of breeding and brood size in four boreal owl species

The ongoing climate change has improved our understanding of how climate affects the reproduction of animals. However, the interaction between food availability and climate on breeding has rarely been examined. While it has been shown that breeding of boreal birds of prey is first and foremost determined by prey abundance, little information exists on how climatic conditions influence this relationship. We studied the joint effects of main prey abundance and ambient weather on timing of breeding and reproductive success of two smaller (pygmy owl Glaucidium passerinum and Tengmalm’s owl Aegolius funereus) and two larger (tawny owl Strix aluco and Ural owl Strix uralensis) avian predator species using long-term nation-wide datasets during 1973–2004. We found no temporal trend either in vole abundance or in hatching date and brood size of any studied owl species. In the larger species, increasing late winter or early spring temperature advanced breeding at least as much as did high autumn abundance of prey (voles). Furthermore, increasing snow depth delayed breeding of the largest species (Ural owl), presumably by reducing the availability of voles. Brood size was strongly determined by spring vole abundance in all four owl species. These results show that climate directly affects the breeding performance of vole-eating boreal avian predators much more than previously thought. According to earlier studies, small-sized species should advance their breeding more than larger species in response to increasing temperature. However, we found an opposite pattern, with larger species being more sensitive to temperature. We argue that this pattern is caused by a difference in the breeding tactics of larger mostly capital breeding and smaller mostly income breeding owl species.

Silicon, endophytes and secondary metabolites as grass defenses against mammalian herbivores

Grasses have been considered to primarily employ tolerance in lieu of defense in mitigating damage caused by herbivory. Yet a number of mechanisms have been identified in grasses, which may deter feeding by grazers. These include enhanced silicon uptake, hosting of toxin-producing endophytic fungi and induction of secondary metabolites. While these mechanisms have been individually studied, their synergistic responses to grazing, as well as their effects on grazers, are poorly known. A field experiment was carried out in 5 × 5 m outdoor enclosures to quantify phytochemical changes of either endophyte-infected (E+) or endophyte-free (E-) meadow fescue (Schedonorus pratensis) in response to medium intensity (corresponding with densities of ca. 1200 voles/ha for 5 weeks during 3 months) or heavy intensity (ca. 1200 voles/ha for 8 weeks during 3 months) grazing by a mammalian herbivore, the field vole (Microtus agrestis). A laboratory experiment was then conducted to evaluate the effects of endophyte infection status and grazing history of the grass diet on vole performance. As predicted, grazing increased foliar silicon content, by up to 13%. Grazing also increased foliar levels of phosphorous and several phenolic compounds, most notably those of the flavonols isorhamnetin-diglycoside and rhamnetin derivative. Silicon concentrations were consistently circa 16% higher in E+ grasses than in E-grasses, at all levels of grazing. Similarly, concentrations of chlorogenic acid derivative were found to be consistently higher in E+ than in E- grasses. Female voles maintained on heavily grazed grasses suffered higher mortality rates in the laboratory than female voles fed ungrazed grass, regardless of endophyte infection status. Our results conclusively demonstrate that, in addition to tolerance, grasses employ multi-tiered, effective defenses against mammalian grazers.

Sex–biased maternal investment in voles: importance of environmental conditions

Adaptive bias in sex allocation is traditionally proposed to be related to the condition of mothers as well as to the unequal fitness values of produced sexes. A positive relationship between mother condition and investment into male offspring is often predicted. This relationship was also recently found to depend on environmental conditions. We studied these causalities experimentally using a design where winter food supply was manipulated in eight outdoor–enclosed populations of field voles Microtus agrestis. At the beginning of the breeding season in spring, food–supplemented mothers seemed to be in a similar condition, measured as body mass, head width, body condition index and parasite load (blood parasite Trypanosoma), to non–supplemented mothers. Food supplements affected neither the litter size, the reproductive effort of mothers, nor the litter sex ratios at birth. However, food supplementation significantly increased the birth size of male offspring and improved their condition, as indicated by reduced parasite loads (intestinal Eimeria). Interestingly, mothers in good body condition produced larger male offspring only when environmental conditions were improved by food supplements. Although the adaptiveness of variation in mammalian sex ratios is still questionable, our study indicates that mothers in good condition bias their investment towards male offspring, but only when environmental conditions are favourable.