Tero Klemola

Experimental tests of predation and food hypotheses for population cycles of voles

Pronounced population cycles are characteristic of many herbivorous small mammals in northern latitudes. Although delayed density–dependent effects of predation and food shortage are often proposed as factors driving population cycles, firm evidence for causality is rare because sufficiently replicated, large–scale field experiments are lacking. We conducted two experiments on Microtus voles in four large predator–proof enclosures and four unfenced control areas in western Finland. Predator exclusion induced rapid population growth and increased the peak abundance of voles over 20–fold until the enclosed populations crashed during the second winter due to food shortage. Thereafter, voles introduced to enclosures which had suffered heavy grazing increased to higher densities than voles in previously ungrazed control areas which were exposed to predators. We concluded that predation inhibits an increase in vole populations until predation pressure declines, thus maintaining the low phase of the cycle, but also that population cycles in voles are not primarily driven by plant–herbivore interactions.

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.

From Plants to Birds: Higher Avian Predation Rates in Trees Responding to Insect Herbivory

Background An understanding of the evolution of potential signals from plants to the predators of their herbivores may provide exciting examples of co-evolution among multiple trophic levels. Understanding the mechanism behind the attraction of predators to plants is crucial to conclusions about co-evolution. For example, insectivorous birds are attracted to herbivore-damaged trees without seeing the herbivores or the defoliated parts, but it is not known whether birds use cues from herbivore-damaged plants with a specific adaptation of plants for this purpose. Methodology We examined whether signals from damaged trees attract avian predators in the wild and whether birds could use volatile organic compound (VOC) emissions or net photosynthesis of leaves as cues to detect herbivore-rich trees. We conducted a field experiment with mountain birches (Betula pubescens ssp. czerepanovii), their main herbivore (Epirrita autumnata) and insectivorous birds. Half of the trees had herbivore larvae defoliating trees hidden inside branch bags and half had empty bags as controls. We measured predation rate of birds towards artificial larvae on tree branches, and VOC emissions and net photosynthesis of leaves. Principal Findings and Significance The predation rate was higher in the herbivore trees than in the control trees. This confirms that birds use cues from trees to locate insect-rich trees in the wild. The herbivore trees had decreased photosynthesis and elevated emissions of many VOCs, which suggests that birds could use either one, or both, as cues. There was, however, large variation in how the VOC emission correlated with predation rate. Emissions of (E)-DMNT [(E)-4,8-dimethyl-1,3,7-nonatriene], β-ocimene and linalool were positively correlated with predation rate, while those of highly inducible green leaf volatiles were not. These three VOCs are also involved in the attraction of insect parasitoids and predatory mites to herbivore-damaged plants, which suggests that plants may not have specific adaptations to signal only to birds.

Birch (Betula spp.) leaves adsorb and re‐release volatiles specific to neighbouring plants – a mechanism for associational herbivore resistance?

Plant-emitted semi-volatile compounds have low vaporization rates at 20-25 degrees C and may therefore persist on surfaces such as plant foliage. The passive adsorption of arthropod-repellent semi-volatiles to neighbouring foliage could convey associational resistance, whereby a plants neighbours reduce damage caused by herbivores. We found that birch (Betula spp.) leaves adsorb and re-release the specific arthropod-repelling C(15) semi-volatiles ledene, ledol and palustrol produced by Rhododendron tomentosum when grown in mixed association in a field setup. In a natural habitat, a higher concentration of ledene was released from birches neighbouring R. tomentosum than from birches situated > 5 m from R. tomentosum. Emission of alpha-humulene, a sesquiterpene synthesized by both Betula pendula and R. tomentosum, was also increased in R. tomentosum-neighbouring B. pendula. In assessments for associational resistance, we found that the polyphagous green leaf weevils (Polydrusus flavipes) and autumnal moth (Epirrita autumnata) larvae both preferred B. pendula to R. tomentosum. P. flavipes also preferred birch leaves not exposed to R. tomentosum to leaves from mixed associations. In the field, a reduction in Euceraphis betulae aphid density occurred in mixed associations. Our results suggest that plant/tree species may be protected by semi-volatile compounds emitted by a more herbivore-resistant heterospecific neighbour.

Natural host-plant quality affects immune defence of an insect herbivore

We examined the effect of natural host‐plant quality on immune resistance in the autumnal moth, Epirrita autumnata (Borkhausen) (Lepidoptera: Geometridae). The division of mountain birches [Betula pubescens ssp. czerepanovii (Orlova) Hämet‐ahti (Betulaceae)] into two categories, high‐ and low‐quality food for larvae, was based on previous years’ results on the relative growth rate of the autumnal moth on the trees selected. The strength of the immune defence of autumnal moths was determined by measuring their encapsulation rate to exposure to a foreign antigen and the phenoloxidase (PO) activity of the pupal haemolymph. We found that individuals reared as larvae on naturally low‐quality food had a significantly higher encapsulation rate at the pupal stage than individuals reared on high‐quality food. Females also had a higher encapsulation rate than males. Food quality did not have statistically significant effect on PO activity, nor did this response variable show any differences between the sexes. Using half‐sib analyses, we found significant heritable variation in the encapsulation rate; the heritable variation in PO activity was near to significant, although equally strong. Heritability estimates (h2: 0.19–0.27) for immune defence traits were relatively low and only moderate when compared to other studies with insects. We also found a negative genetic correlation between pupal mass and PO activity, but not between PO activity and encapsulation rate. Our results suggest that the quality of food affects immune defence in the autumnal moth. Thus an intricate tritrophic relationship exists between the folivorous insect, the host tree, and the insects natural enemies (e.g., pathogens, parasites, and parasitoids). This study demonstrates that natural variation within a food plant species has an effect on the innate immune system of an herbivorous insect.

Small Mustelid Predation Slows Population Growth of Microtus Voles: A Predator Reduction Experiment

1. The effects of predator reduction on the breeding performance and sex ratio of Microtus voles were studied in a cyclically fluctuating vole assemblage in western Finland, where the field vole (Microtus agrestis) and the sibling vole (M. rossiaemeridionalis) are the main prey of small mustelids. 2. The densities of small mustelids [the least weasel (Mustela nivalis nivalis) and the stoat (M. erminea)] were reduced experimentally in three large (2-3 km 2 ) unfenced areas in 1992, during a crash phase of the vole cycle, and in three different areas during the following crash phase in 1995. The reproductive performance of Microtus voles was compared between control and manipulation areas before and after reducing predators. 3. The reduction of predators increased the productivity of female voles, mainly due to an increased proportion of pregnancies, whereas the body condition of voles was not affected by the manipulation. This suggests that high predation risk in control areas suppressed the breeding of free-living voles. 4. The sex ratio of trapped voles before the manipulation did not differ between reduction and control areas, but after predators were reduced the sex ratio was more male-biased in the control areas. This indicates that small mustelids selectively killed female voles. 5. Our results suggest two possible mechanisms which may have operated concurrently. An adaptive explanation is that voles traded their current reproductive investment against future breeding under high predation risk. A simpler explanation is that small mustelids selectively preyed on pregnant female voles. Both suppressed breeding and selective killing would lead to a lower proportion of reproducing individuals in the vole population. Therefore, our results show that the presence of small mustelid predators slowed the population growth of Microtus voles.

Birds help plants: a meta-analysis of top-down trophic cascades caused by avian predators

The tritrophic interactions between plants, herbivores and avian predators are complex and prone to trophic cascades. We conducted a meta-analysis of original articles that have studied birds as predators of invertebrate herbivores, to compare top-down trophic cascades with different plant responses from different environments and climatic areas. Our search found 29 suitable articles, with a total of 81 separate experimental study set-ups. The meta-analysis revealed that plants benefited from the presence of birds. A significant reduction was observed in the level of leaf damage and plant mortality. The presence of birds also positively affected the amount of plant biomass, whereas effects on plant growth were negligible. There were no differences in the effects between agricultural and natural environments. Similarly, plants performed better in all climatic areas (tropical, temperate and boreal) when birds were present. Moreover, both mature plants and saplings gained benefits from the presence of birds. Our results show that birds cause top-down trophic cascades and thus they play an integral role in ecosystems.

Vole cycles and predation

In a recent article in TREE [1], Madan K. Oli claimed that an experimental reduction of weasel density in Kielder Forest [2] shows that specialist mammalian predators are neither sufficient nor necessary to drive multiannual population cycles of field voles Microtus agrestis. Here, we argue that this claim is misleading because he overlooked three important issues: the uniqueness of the Kielder Forest vole cycles compared with elsewhere; the limitations in the Kielder Forest experiment to test current predation hypotheses; and the contribution of other recent experiments on predation and vole cycles. The multiannual vole cycles in Kielder Forest and in northern Europe (northern vole cycles) differ in at least three fundamental ways to suggest that the Kielder Forest experiment provides limited insight into the role of predators in vole cycles elsewhere. First, in the low phase of northern vole cycles, densities of voles are much lower than in Kielder Forest (, 1h a 21 versus 25‐ 50 ha 21 ). Northern vole cycles are also characterized by 50- to 500-fold differences between peak and lowest densities, whereas vole cycles in Kielder Forest are low amplitude cycles with only tenfold differences between peaks and lows that would provide greater interannual stability in food supply for vole-eating predators. Second, spatial synchrony of Kielder Forest vole cycles is much

Fecundity of the autumnal moth depends on pooled geometrid abundance without a time lag: implications for cyclic population dynamics.

1. The abundance and fecundity-related body size variation of the cyclic autumnal moth Epirrita autumnata were monitored from the early increase phase and throughout the outbreak to the end of the density decline in northernmost Norway during 1999-2006. Another geometrid, the winter moth Operophtera brumata, did not increase in density until the autumnal moth had its post-peak in 2004, and was at its own peak concurrent with the steeply declining autumnal moth abundance in 2005-06. 2. The body size variables measured (forewing lengths of males and females and hind femur lengths of males) of the autumnal moth showed a similar density-dependent response, i.e. increasing density was associated with decreasing body size and fecundity. Nevertheless, regression analyses clearly ranked the pooled geometrid abundance without a time lag as the best predictor for the body size variation, ahead of the abundance of the autumnal moth or past abundance of all geometrids. 3. Nondelayed effects of lowered food quality and absolute shortage of foliage under congested conditions are the most plausible reasons for reduced body size. 4. Two most commonly proposed causal factors of the autumnal moth population cycle, i.e. delayed inducible resistance of the host plant (mountain birch Betula pubescens czerepanovii) and delayed density-dependent parasitism by specialized hymenopteran parasitoids, cannot easily explain the diverging population trends between the autumnal and winter moths. 5. We suggest that either the inducible resistance of the host tree or the host utilization of the most important parasitoids and/or pathogens have to be strictly species-specific between these closely related moth species to produce the population dynamics observed. That fecundity of the autumnal moth was best related to the pooled geometrid abundance weakens support for the former hypothesis, while our lack of host-specific information limits conclusions about the role of natural enemies.

Reduction in size and fecundity of the autumnal moth, Epirrita autumnata, in the increase phase of a population cycle

Increasing fecundity with increasing density has been observed for many cyclic herbivore populations, including some forest Lepidoptera. We monitored population density, body size and reproductive capacity of the cyclic lepidopteran, the autumnal moth (Epirrita autumnata, Geometridae), from the early increase phase to the devastating outbreak density in northernmost Norway. Larval density of the species increased exponentially from 1998 to 2002 and remained at the outbreak level also in 2003. Within the same period, the body size and fecundity of individuals reduced as analysed from several parallel datasets on larvae, pupae and adults. In another study area in northernmost Finland, the density increase of the autumnal moth was moderate only, and true outbreak density was not attained during the study. Despite that, a reduction was again detected in the size and fecundity of individuals. Possible factors responsible for the reduced size and fecundity of individuals in the Norwegian population were quantitative shortage of foliage, rapid and delayed inducible resistances of the host, mountain birch (Betula pubescens ssp. czerepanovii), as well as crowding-induced responses of larvae. These factors likely acted in concert, although non-delayed responses to the density were emphasized. Our findings did not support the hypotheses of climatic release, inducible susceptibility of the host tree and mast depression (i.e. lowered chemical defence of the host tree after its mast seeding) as promoters of the fecundity-based density increase of the autumnal moth, since the reduced fecundity in relation to increased density was strongly against the predictions of these hypotheses. Therefore, we suggest that the density increase of autumnal moth populations is promoted by high survival rather than exceptionally high fecundity.