Factors regulating population dynamics and reproductive success of animals in varying environmental conditions

By prof. Erkki Korpimäki at Section of Ecology, Department of Biology, University of Turku e-mail ekorpi@utu.fi

 

Description of the major projects

1) Natural enemies and food supply as regulating factors in population fluctuations of small mammals and small game

2) Invasion of an alien predator and return of a native top-predator: impacts on biodiversity in the Baltic Sea

3) Individual-level approach to animal populations: natural variation and responses to human-induced changes in forest and agricultural ecosystems

4) Habitat selection, diet choice and mobility of predators

5) Reproductive decisions in variable environments

6) Immunocompetence, parasites and health status

7) Importance of ultraviolet vision in foraging and communication of vertebrate animals

1) Natural enemies and food supply as regulating factors in population fluctuations of small mammals and small game

Cyclic multiannual (3-4-yr) fluctuations of population densities of northern small mammals (voles, mice and shrews) have been described as the main puzzle of population dynamics in major ecological textbooks. Four-year population cycles of voles are of great importance to northern ecosystems, because in the peak phase of the cycle, voles may induce changes in plant quantity and quality, and high predator densities in turn may reduce densities of other animals, such as small game (hare and grouse). The main question of this project is the role of extrinsic factors (natural enemies and food supply) in population cycles of voles.

The main findings of our novel large- and small-scale experiments with small mammals can be summarized as follows:

(1) The large-scale reduction of predator densities increased the autumn density of Microtus voles by four-fold in the low phase, accelerated the increase by two-fold, retarded the initiation of decline, and prevented the summer decline of vole populations.

(2) Extrapolating these experimental results to their expected long-term dynamic effects through a demographic model for Microtus voles and their predators produced changes from regular multiannual cycles to annual fluctuations with declining densities of specialist predators, whereas reduction of generalist avian predators tended to increase the amplitude of these fluctuations.

(3) Predator exclusion induced rapid population growth and increased the peak abundance of voles over 20-fold compared to control areas until the enclosed populations crashed during the second winter due to food shortage. Delayed effects of overgrazing on population growth of voles in enclosures were not detected, which suggests that population cycles in voles are not proximately driven by delayed effects of deficient food quality or quantity.

(4) The predation hypotheses for vole cycles, as formulated through mathematical population models, inherently require a direct density dependent mechanism to slow prey population growth in the increase phase of the cycle, so that predator populations can catch up on populations of their prey. To identify this mechanism, a two-year replicated two-factor experiment was performed in our fences. In the first winter, food supplementation increased vole population growth significantly in predator exclosures, but not in unfenced areas. During the second winter, food supplementation prevented the crash of vole populations in predator exclosures, whereas again no effect was found in the unfenced control areas. These results indicate that vole populations which 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.

In summary, these results largely solve the puzzle of multiannual population cycles of voles. The most likely hypothesis is that 3-5-yr population cycles of northern voles are driven by delayed density dependent losses to predators but that vole populations which have succeeded in escaping regulation by predators are limited in growth by a shortage of winter food.

Main references:

Korpimäki, E. & Norrdahl, K. 1998, Ecology 79: 2448-2455.
Klemola, T. et al. 2000, Proc. R. Soc. Lond. B 267: 351-356.
Klemola, T. et al. 2000, Oikos 90: 509-516.
Norrdahl, K. & Korpimäki, E. 2000, Oikos 91: 528-540.
Bêty, J. et al. 2002, J. Anim. Ecol. 71: 88-98.
Klemola, T. et al. 2002, Oikos 96: 291-298.
Korpimäki, E. et al. 2002, Proc. R. Soc. Lond. B 269: 991-997.
Huitu, O. et al. 2003, Oecologia 135: 209-220.
Huitu, O. et al. 2003, Ecology 84: 2108-2118.
Korpimäki, E. et al. 2003, Trends Ecol. Evol. 18: 494-495.

Korpimäki, E. et al. 2004, BioScience 54:1071-1079.

Korpimäki, E. et al. 2005, Proc. T Soc. Lond. B 272:193-202.

Korpimäki, E. et al. 2005, J. Anim. Ecol. 74:1150-1159.

 

2) Invasion of an alien predator and return of a native top-predator: impacts on biodiversity in the Baltic Sea

Feral predators are a major threat to biodiversity worldwide; few ecosystems have escaped their impact, but in Finland the problem is relatively recent. Understanding how feral predators affect their prey is a crucial conservation objective, not only to identify and protect prey species at risk but also to ensure efficient and targeted management of the problem.

An invasion of an alien predator, American mink, to the archipelagos of the Baltic Sea is thought to have had vast detrimental effects on biodiversity. The feral mink is a generalist carnivore that can destroy colonies of seabirds. Therefore, it has been suggested that the colonization of feral mink is the most important factor causing the recent decline of many bird species in archipelagos of the Baltic Sea. Yet, the invasion of feral mink to the outer archipelago may have been aided by the drastic population decline of the native top-predator, the white-tailed sea eagle in 1960s and 1970s. Sea eagles are the only potential enemies of mink in the outer archipelago. At present, sea eagles are returning to breed everywhere in coastal areas of Finland, largely due to effective conservation programmes.

We have studied the effects of large-scale experimental removal of feral mink on the number of birds breeding on small islands of the Baltic Sea. During 1992/93 to 2001/02 mink were removed from 60 islands (total area 72 km2), while mink were not removed from 37 islands (35 km2). Second removal (62 islands, 125 km2) and control areas (64 islands, 130 km2) were established during 1998-2001. We collected data on the breeding densities of birds on these islands. Our results show that 8 waterfowl, 2 wader, 3 gull and 2 passerine species markedly increased as a response to mink-removal, while the breeding densities of three large waterfowl species did not show obvious increases after mink removal. Two species already extinct in the study areas, the razorbill and the black guillemot returned to breed in old removal area. Thus, it is possible to remove feral mink on a large scale, and that mink removal increases the breeding densities and species richness of archipelago birds.

We also studied the dynamics of voles on 40 small islands under variable rainfall as part of this mink removal experiment. Occupancy, extinction and colonisation processes of voles were negatively influenced by island isolation. High summer rainfall in 1998 lead to large vole populations where mink were absent, which then crashed in 1999 and 2000 when below average rains fell over the summer. Where mink were present however, vole abundance remained more constant between years with no boom-bust apparent. Feral mink may prevent rapid population growth of voles after good summer rains which would otherwise lead to overexploitation of food plants on small islands forcing animals to disperse to other islands to avoid starvation.

Amphibians are undergoing enigmatic global declines variously attributed to a complex web of anthropogenic forces, including impacts of alien predators. While amphibian eggs and tadpoles are vulnerable to aquatic predators the role of predators on adult, reproducing frogs, which most influence amphibian population processes, is unknown. A long-term, large-scale removal of American mink increased both the densities and distribution of common frogs but not those of common toads, which appear to escape mink predation because of their unpalatable skin. Importantly, the largest benefits of mink removal to frog recovery were slow to appear as frogs apparently have a delayed maturation in these harsh environments, which cautions reliance upon short-term results.

In the ongoing project, we propose to concentrate on impacts of top-down processes on the biodiversity of the Baltic Sea in order to better understand the complexity of impacts and provide vital information for better management of feral mink. Our main objective is to investigate the effects of island characteristics, removal of feral mink and occurrence of sea eagles on the biodiversity, including birds, small mammals, amphibians and plants. To do this we will undertake several unique experiments that focus on the consequences of interactions between these two top predators and their prey.

Main references:

Nordström, M. et al. 2002, Ecography 25: 385-394.
Nordström, M. et al. 2003, Biological Conservation 109: 359-368.
Banks, P. et al. 2004, Oikos 105:79-88.
Nordström, M. & Korpimäki, E. 2004, J. Anim. Ecol. 73: 424-433.
Nordström, M. et al. 2004, Behav. Ecol. Sociobiol. 55: 454-460.

Ahola, M. et al. 2005, Proc. R. Soc. Lond. B (in press).

 

3) Individual-level approach to animal populations: natural variation and responses to human-induced changes in forest and agricultural ecosystems

In northern areas, many animal populations exhibit extensive natural size variation. Therefore, it is difficult to detect whether the decline in some particular animal population is due to natural factors or to human-induced environmental changes.

Although habitat loss by human actions is the largest worldwide hazard to biodiversity, little is known about the effects of habitat loss and change on reproduction and survival at the level of individual animals. We have shown that lifetime reproductive success (LRS) of forest-dwelling Boreal Owls increased with proportion of old forests and decreased with proportion of agricultural land in the territory. LRS increased with old forest because of higher number of breeding attempts, whereas it decreased with agricultural land because of declining fledging success in years when main prey populations crashed during the breeding of owls. These unique results demonstrate how human influence on the landscape can affect life history traits through various pathways.

Our main aim is to find out how much spatial and temporal variation in the density of animals can be explained by natural environmental variation and by, for example, forest fragmentation, air pollution and changes in agricultural practices. In the forest areas, our main study species are Tengmalm's owl, the pygmy owl, the pied flycatcher, red squirrel and bank vole, and in agricultural areas the curlew, the kestrel, some small passerine species, and Microtus voles.

Main references:

Korpimäki, E. 1992, J. Anim. Ecol. 61: 103-111.
Norrdahl, K. & Korpimäki, E. 1995, Oecologia 101: 105-109.
Hakkarainen, H. et al. 1996, Wildl. Biol. 2: 253-258.
Norrdahl, K. & Korpimäki, E. 1998, J. Avian Biol. 83: 259-272.
Currie, D. & Valkama, J. 1998, Environ. Poll. 101: 253-261.
Valkama, J. et al. 1999, Ecoscience 6: 497-504.
Österblad, M. et al. 2001, Nature 409: 37-38.
Hakkarainen, H. et al. 2003, Oikos 100: 162-171.
Laaksonen, T. et al. 2004, Proceedings of the Royal Society of London B (Suppl.) 271: S461-S464.

4) Habitat selection, diet choice and mobility of predators

Main aim is to find out how avian and mammalian predators feeding on cyclically fluctuating food sources can survive over "lean" periods and benefit from food abundance.

Responses of predators to fluctuations in prey abundance may be either numerical or functional. The numerical response is due to changes in natality, mortality, immigration, and emigration. Thus, the ability to respond numerically to the fluctuations of prey populations depends on the mobility, reproductive potential, and generation time of the predator. The availability of preferred and alternative prey, the ability to shift to alternative prey, and interspecific competition for food affect the functional response of the predator.

Predators can adopt three basic strategies when living under fluctuating food conditions. Resident generalists (for example, the red fox and the Eagle owl) occupy their territories throughout the year or show only limited mobility. They are able to shift their diet to alternative prey when main prey abundance declines. Nomadic or migratory avian predators (for example, the kestrel and the short-eared owl) specialise on small rodents and shift their nesting sites over long distances (even >500 km) nearly every year. Resident specialist predators (for example, the least weasel) use small rodents as their main food (nearly independently of vole abundance in the field), and are able to move over only short distances (<30 km).

Main references:

Korpimäki, E. et al. 1991, Oecologia 88: 552-561.
Korpimäki, E. & Norrdahl, K. 1991, Ecology 72: 814-826.
Korpimäki, E. 1992, Can. J. Zool. 70: 2373-2381.
Korpimäki, E. 1993, J. Anim. Ecol. 62: 606-613.
Hakkarainen, H. & Korpimäki, E. 1996, Ecology 77: 1134-1142.
Norrdahl, K. & Korpimäki, E. 1998, Ecology 79: 226-232.
Hakkarainen, H. & Korpimäki, E. 1998, Oecologia 114: 578-582.
Klemola, T. et al. 1999, Ann. Zool. Fenn. 36: 75-82.
Hakkarainen, H. et al. 2001, Oecologia 126: 355-359.
Reif, V. 2001, Ecography 24: 267-274.
Hakkarainen, H. et al. 2002, Oecologia 131: 83-88.
Valkama, J., Korpimäki, E. et al. 2005, Biological Reviews 80:171-203.

Tornberg, R., Korpimäki, E.  et al. 2005, Oikos 111:408-415.

5) Reproductive decisions in variable environments

Life-history theory developed to explain the determination of clutch size, size and sex of offspring, and age at first reproduction is mostly based on studies on birds, where clutch size, sex ratio and hatching spans of broods are usually examined separately. Moreover, theories on the determination of clutch size of birds and other animals have been separately developed from theories on sex allocation, and hypotheses on hatching asynchrony and sibling rivalry. When birds are investing in reproduction, however, they should "decide" at the same time the number and sex of eggs, and whether they will hatch their chicks synchronously or asynchronously to vary the size hierarchy (and thus the degree of sibling rivalry) among members of their brood.

Offspring sex ratio may be an unpredictable component of life history that might select for behavioural plasticity in parental care. If the parents do not have such plasticity and the two sexes of offspring differ in size, individuals in a brood or litter biased towards the larger sex offspring may suffer from food shortage. We created single-sex broods of sexually size-dimorphic Eurasian kestrels with mixed-sex control broods in order to test whether parents have behavioural plasticity to respond to the sex ratio of their brood and whether smaller male chicks suffer from reduced health status because their larger female siblings outrival them in sibling competition. The experiment was conducted in two years that differed in the abundance of voles, the main natural prey of kestrels. No obvious effects of the brood sex ratio manipulation on parental effort were detected, as there were no differences in prey delivery rate, biomass of prey brought to the nest, body mass or heterophile/lymphocyte ratio of the parents. Female chicks in all-female broods had lower hematocrit levels than those in mixed-sex broods in a year of low vole abundance. As hematocrit is an index of nutritional condition and health state, this result indicates that in the year of low vole abundance the female chicks in all-female broods fledged in poorer condition than those in mixed-sex broods. These results indicate that when the parents do not alter their level of parental effort in response to the sex ratio of their brood, the young in a brood biased towards the larger sex offspring can be reared successfully when food is abundant, while they may suffer under food shortage situations.

It has been suggested that that variation in hatching asynchrony in birds of prey, particularly in owls, is extensive, and therefore, they should be excellent objects to study effects of spatio-temporal variation in food abundance on this phenomenon. Female Tengmalm’s owls lay eggs at 48-h intervals, and start to incubate, on average, after laying their second egg, which results in highly asynchronous hatching of eggs. Hatching span of Tengmalm's owls averaged 6-7 days (range 0-13 days) and increased with clutch size. Food supply did not directly influence levels of hatching asynchrony but it influenced indirectly via marked among-year changes in clutch size. During the decline phase of the vole cycle the proportion of hatchlings producing fledglings decreased with asynchrony, suggesting that chick mortality was most common among asynchronous broods when food became scarce. This finding is consistent with the brood reduction hypothesis, i.e. that if food becomes scarce during the nestling period the youngest nestlings would die first without endangering the survival of the whole brood.

Main references:

Korpimäki, E. 1994, J. Anim. Ecol. 63: 619-628.
Tolonen, P. & Korpimäki, E. 1995, Behav. Ecol. 6: 435-441.
Korpimäki, E. et al. 1996, Anim. Behav. 51: 945-955.
Wiehn, J. & Korpimäki, E. 1997, Ecology 78: 2043-2050.
Korpimäki, E. & Wiehn, J. 1998, Oikos 83: 259-272.
Wiebe, K. et al. 1998, J. Anim. Ecol. 67: 908-917.
Wiehn, J. et al. 2000, J. Anim. Ecol. 69: 85-95.
Korpimäki, E. et al. 2000, J. Avian Biol. 31: 128-134.
Laaksonen, T. et al. 2002, J. Anim. Ecol. 71: 23-31.
Valkama, J. et al. 2002, Oecologia 133: 334-341.
Fargallo, J. A. et al. 2003, Evol. Ecol. Res. 5: 549-558.
Laaksonen, T. et al. 2004, J. Anim. Ecol. 73: 342-352.
Laaksonen, T. et al. 2004, Evolutionary Ecology 18: 215-230.

6) Immunocompetence, parasites and health status

Costs of reproduction are defined as allocation trade-offs between current reproductive effort and future reproductive potential. When organisms invest in current reproduction their future survival and/or reproductive output will be reduced, possibly because of somatic deterioration or increased predation risk. Actual mechanisms underlying reproductive costs are still largely unknown but it has been suggested that parasites may mediate costs of reproduction. Because reproduction and immune defence are both thought to be energetically costly, there may be a trade-off between allocation of resources to reproduction and immunity. Our main aim is to find out interactive effects of immune response and parasites on health status, survival and reproductive success of birds in varying environmental conditions.

We studied the assumptions of benefits and costs of defence against blood parasites with vole-eating Tengmalm's owls and kestrels. First, we found that blood parasite infections were more prevalent in poor food years. Second, we found that successful defense against blood parasites may be beneficial, as seen in the reduced clutch size of female owls infected with leucocytozoids, and later start of egg-laying in kestrel females mated with haemoproteid infected males. Third, with supplementary food experiments and brood size manipulations we showed that defending against blood parasites is costly, and that the costs may be modified by environmental conditions, and that the expected costs can vary between the sexes due to their different parental roles. The prevalence of trypanosomes among female owls was lower in food supplemented nests than in control nests, whereas in female kestrels food supplements reduced trypanosome and haemoproteid prevalences only in a year of low natural food supply. Manipulations of kestrel brood size revealed that trypanosome prevalence in males increased with experimental brood size, and the difference in prevalences between reduced and enlarged broods increased with decreasing natural food supply. These results may help in explaining why the appearance of reproductive costs may be associated with sex of the avian host or with variation in environmental conditions.

We manipulated clutch sizes of Eurasian kestrels by one egg to estimate possible cumulative effects of incubation and chick rearing costs on parental body condition, feeding effort and offspring viability. No obvious effects of clutch size manipulations on parental effort were found, while feeding effort was adjusted to the original clutch size. Enlarged and control nests suffered from higher nestling mortality than reduced nests, and chicks of the enlarged group were in poorer body condition than chicks of the reduced group.Male chicks exhibited lower immune response than females but only in treatments suffering from food restrictions, as indicated by chick starvation. Variation in immunity was not interfered by ectoparasite infection.These novel results reveal inter-sexual differences in nutritional resource allocation in early life, suggesting sex-related differences in susceptibility to disease and consequently in survival prospects of offspring.

Main references:

Korpimäki, E. et al. 1993, Funct. Ecol. 7: 420-426.
Korpimäki, E. et al. 1995, Ecoscience 2: 335-343.
Wiehn, J. & Korpimäki, E. 1998, Proc. R. Soc. Lond. B 265: 1197-1201.
Wiehn, J. & Korpimäki, E. 1999, Oikos 84: 87-98.
Ilmonen, P. et al. 1999, Oikos 86: 79-86.
Ilmonen, P. et al. 2000, Proc. R. Soc. Lond. B 267: 665-670.
Fargallo, J. A. et al. 2002, Ecology Letters 5: 95-101.

7) Importance of ultraviolet vision in foraging and communication of vertebrate animals

Our main aim is to find out importance of ultraviolet (UV) vision in food detection and communication of birds and other vertebrates.

Scent markings are important in the social and sexual behaviour of mammals, and odours of small mammals may be equivalent to secondary sexual characteristics of many other animal groups. Scent marks of mice are known to be visible in UV light but a new finding was that vole scent marks have also a special hue only visible in UV light. Therefore, predators that are able to detect UV could use scent marks to find vole patches and assess prey densities.

Our aviary and field experiments indicated that kestrels are attracted to vole scent marks in the presence of UV light and use them as a cue when hunting. UV reflectance of scent marks differs between species and also between reproductive categories of voles, and kestrels may be able to distinguish these differences. Our results also show that other diurnal birds of prey, such as rough-legged buzzards, are attracted to vole scent marks, whereas nocturnal Tengmalm's owls are not.

Reproductive activities, including signalling with scents, may increase the risk of predation. Mammalian predators, like small mustelids, find voles by odour cues of scent marks, which also are visible in UV (a cue used by diurnal raptors). We have performed a field experiment to find out whether manipulation of scent markings affects the density, survival and mobility of free-living voles. Predators were more often hunting on scent manipulation than control plots leading to lower survival time of voles. Although scent manipulation attracted avian predators, small mustelids were the main predators of radio-collared voles. Our results suggest that odour of scent marks may be a larger risk to voles than UV-visibility of scent marks.

References:

Viitala, J. et al. 1995, Nature 373: 425-427.
Koivula, M. et al. 1997, Anim. Behav. 54: 873-877.
Koivula, M. & Viitala, J., J. Avian Biol. 30: 329-332.
Koivula, M. et al. 1999, Ecoscience 6: 415-420.
Koivula, M. & Korpimäki, E. 2001, Oikos 95: 275-281.
Honkavaara, J. et al. 2002, Oikos 98: 505-511.