Download Red in tooth and claw: how top predators shape terrestrial ecosystems

Journal of Animal Ecology 2010, 79, 723–725
doi: 10.1111/j.1365-2656.2010.01706.x
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Red in tooth and claw: how top predators shape
terrestrial ecosystems
A young Eurasian lynx (Lynx lynx). Photo by Gilbert Ludwig taken at Ähtäri Zoo.
Elmhagen, B., Ludwig, G., Rushton, S.P., Helle, P. & Linden, H. (2010) Top predators, mesopredators and their prey: interference ecosystems along bioclimatic productivity gradients. Journal
of Animal Ecology 79, 785–794.
Top predators are increasingly recognized as important regulators of ecosystem structure. Elmhagen
et al. in this issue show how a recolonizing population of lynx in Finland is in the process of imposing
control of the abundance of a mesopredator, the red fox and relaxing predation pressure on a prey
species. Their study shows how ecological restoration programs could use the power of top predators
to limit mesopredator populations and control total predation pressure on prey species.
Large predators are in retreat throughout the world. This is
especially true of predator species that threaten (or at least,
frighten) people, and that attack our livestock. Such species
have suffered intense persecution for centuries, and efforts to
eliminate them from the more densely populated parts of the
world have mostly succeeded (Prugh et al. 2009). Now,
changed attitudes to the conservation of wild predators are
allowing, and in some places encouraging, their return to
ecosystems. In Europe and North America the recovery of
populations of big predators is providing outstanding oppor-
*Correspondence author. E-mail: [email protected]
2010 The Author. Journal compilation 2010 British Ecological Society
tunities to study the ways in which these species shape terrestrial communities. An example is the effects of the removal
and then the restoration of wolves Canis lupus in the Yellowstone Ecosystem. Loss of wolves led to irruption of large herbivores (wapiti Cervus canadensis) and decline of woodlands
by over-browsing; wolf restoration has brought wapiti back
under control and is allowing woodland recovery (Beschta &
Ripple 2009).
The wolf-wapiti-plant system is a classic three-level
community, which behaves as predicted by Hairston, Smith
& Slobodkin (1960) in their ‘green world’ hypothesis: predators protect plant biomass by checking the abundance of herbivores. But species like wolves and big cats were removed
724 C. N. Johnson
from ecosystems that also contained smaller predators. Interactions between top predators and these ‘mesopredators’
provide another pathway by which top predators can structure ecosystems (Soulé et al. 1988; Crooks & Soulé 1999).
Mesopredators are often generalist carnivores that, in the
absence of top-down control, can reach high population
densities and impose high predation pressure on a wide range
of small prey species. By controlling mesopredators, top
predators indirectly protect biodiversity at lower tropic levels
from the effects of over-predation (Prugh et al. 2009; Ritchie
& Johnson 2009).
The interaction of top predators with mesopredators is
analysed in the new paper by Elmhagen et al. (2010), who
show how the lynx Lynx lynx population of Finland, now
returning under protection from hunting, is in the process of
re-organizing the boreal ecosystem. The study is made possible by an extraordinary ecological database created by the
‘Finish Wildlife Triangle Scheme’. This consists of a network
of about 900 transects, each about 12 km long, distributed
over an area of 200 000 km2 (i.e. most of Finland), that are
surveyed by hunters each winter for tracks. Analysis of
17 years of data from this giant monitoring program allows
Elmhagen et al. to demonstrate that recolonizing lynx are
strengthening top-down control in this ecosystem. Increasing
lynx populations suppress fox Vulpes vulpes populations, and
this reduces the impact of fox predation on the mountain
hare Lepus timidus.
In Finland, both lynx and fox prey on hares. Lynx are
larger than foxes, but foxes form a negligible part of the diet
of lynx. These species therefore belong to a simple three-level
community, if that is defined according to what they eat: lynx
and foxes prey on hares, and hares eat plants. Elmhagen
et al. analyse the changing structure of this community along
a gradient of productivity, from the productive southwest of
Finland to the relatively unproductive northeast. They do
this because they want to understand how productivity
affects the structure of their system, and because Oksanen &
Oksanen (2000) have provided clear predictions on the way
in which productivity gradients should affect the distribution
of biomass among trophic levels in ecosystems with topdown control by predators (Fig. 1). Oksanen & Oksanen’s
‘exploitation ecosystem hypothesis’ argues (for endotherms)
that in unproductive environments, herbivore populations
will be too sparse to support predators. In the absence of
predator control, herbivores hold plant biomass low.
Increased productivity allows plants to make more tissue,
but this surplus is consumed by herbivores. So as productivity rises, herbivore biomass increases, but standing plant
biomass does not. At the point where there are enough herbivores to support a predator, productivity-driven increases in
recruitment to the herbivore population are consumed.
Predator populations therefore increase with productivity
while herbivore populations are held constant, and this
allows plant biomass to increase with productivity, creating
Hairston et al.’s green world.
Viewing the lynx-fox-hare system as the top part of a simple three-level predator-herbivore-plant community there-
(a)
(b)
Top predator
Mesopredator
Predator
Herbivore
Plants
Ecosystem productivity
Fig. 1. Summary of predictions tested by Elmhagen et al. (2010). (a)
Biomass in relation to productivity in a 3-level community: with no
predator, herbivore populations increase with productivity, but
biomass of a single mesopredator increases with productivity while
herbivore biomass does not. (b) Effects of suppression of mesopredators by a top predator: total predator biomass is reduced (because
top predators have low population density, but strong effect on
mesopredators) so herbivore biomass is greater, and biomass of top
predators and herbivores respond to productivity while biomass of
mesopredators does not.
fore leads to this prediction: the biomass of lynx and fox
should increase along productivity gradients, while hare biomass should be constant. But while lynx rarely eat foxes, they
do attack and kill them. In Sweden where lynx are also
currently increasing, 50% of the deaths recorded in a radiotracked sample of foxes were due to attacks by lynx, which
caused an annual mortality of 14% (Helldin, Liberg &
Gloersen 2006). This aggression can be interpreted as a
strong form of interference competition for a shared prey, in
which lynx pre-empt competition from foxes by killing them.
Lynx should therefore have a strong negative effect on fox
biomass, and that effect is likely to be strongly amplified if
foxes avoid habitats where they are likely to encounter lynx
(Ritchie & Johnson 2009). However, because (as Elmhagen
et al. show) lynx are on average about 40 times less abundant
than foxes, the impact of lynx predation on hare biomass
should be less than that of an unconstrained fox population.
So, applying the logic of Oksanen & Oksanen (2000) to this
case of interference between predators leads to the following
predictions (Fig. 1): the biomass of lynx should increase with
productivity, while the biomass of foxes should not; the
biomass of hares should also increase with productivity, but
it should on average be higher than it would be if no lynx
were present and hare populations were held constant by fox
predation.
Elmhagen et al.’s analysis shows rapid population increase
of lynx since the early 1990¢s. Lynx and fox biomass were
negatively related, while lynx and hare biomass were positively related. By constructing models that account for variation in productivity, Elmhagen et al. show that fox biomass
was lower than expected from productivity where lynx biomass was high, while hare biomass was lower than expected
where fox biomass was high.
The re-establishment of lynx is not yet complete, and they
are still increasing throughout the country. This observation
suggests another way in which productivity could affect the
2010 The Author. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 723–725
Red in tooth and claw 725
lynx-fox-hare system. In unproductive systems, where foxes
and hares have naturally low abundances, a smaller population of lynx will be needed to enforce control of foxes. This
will be achieved earlier in the process of population growth.
Thus, Elmhagen et al. find that in the unproductive northeast
of Finland top-down control is currently strongest: as predicted (Fig. 1), lynx and hare biomass increase with productivity within this region, while fox biomass does not. In the
productive southwest, where lynx biomass relative to productivity is still low, fox biomass increases with productivity
while hare biomass does not. The southwest appears to be a
‘mesopredator-release system’ in which top-down control of
mesopredators biomass has not yet been restored; presumably, this will happen over the next few years if lynx are
allowed to continue their recovery.
As yet, there has been no general increase of hares in Finland following lynx re-invasion. This is possibly because climate effects – recent warm winters – have disadvantaged
hares, and the effect of lynx has been to offset the impact of
this and allow them to sustain their populations. Elsewhere,
recovery of lynx has allowed increase in the prey of red foxes,
such as hare and grouse (Helldin et al. 2006), or of competitors of red foxes such as arctic foxes (Shirley et al. 2009). This
effect is likely to be strongest in places where the preferred
prey of lynx (small deer) are abundant, because then lynx
continue to suppress red foxes but without hunting the same
species as foxes.
Elmhagen et al.’s study provides a striking demonstration
of the power of large predators to regulate interactions in
communities, and control the abundance of other species
through cascading effects. Their approach elegantly reveals
the dynamics of the effects of a top predator as it returns to
an ecosystem, and by focussing on productivity gradients
they provide a link to classical ecological theory based on
energy flows through distinct trophic levels. They also show
that this classical approach is not useful in cases where species have strong antagonistic interactions that do not consist
simply of eating and being eaten. Viewing this system simply
as a food web is inadequate, and to understand the mechanisms involved and predict its dynamics it will be much more
useful to take an approach based on network theory, as
recently argued by Ings et al. (2009). This will be especially
valuable when we come to tackle more complex systems, in
which top predators interact with multiple mesopredator species as well as with their own prey and (indirectly) with the
prey of mesopredators, while mesopredators also interfere
with one another.
Many conservation biologists now advocate the restoration of top predators as a way to restore stability to ecosystems, and prevent extinction of species vulnerable to the
impacts of over-abundant mesopredators (Terborgh et al.
1999; Hayward & Somers 2009). The story of lynx in Finland,
as it continues to unfold, will be especially valuable as a demonstration of the results that predator restoration could bring
elsewhere.
Christopher N. Johnson*
School of Maine and Tropical Biology, James Cook
University, Townsville, Northern Queensland, Australia
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Received 28 March 2010; accepted 20 April 2010
Handling Editor: Corey Bradshaw
2010 The Author. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 723–725