This is the first in a regular series of mini-review which highlight outstanding recently
published papers that shed new light on biological responses to climate change. We
chose migration as the topic for the first mini review because its global geographical
scale makes migrating individuals particularly vulnerable to climate change, and at
the same time, the process of migration has fundamental impacts on ecological processes
and biodiversity.
Movement is an integral part of the ecology of many animals, and it can affect individual
fitness and population persistence by enabling foraging and predation, behavioural
interactions, and migration 1]. Migration, in particular, affects biodiversity at regional and global scales, and
migratory animals affect ecosystem processes. Animals use predictable environmental
cues for the timing and navigation of migration. A change in these cues will affect
the phenology and extent of migration. Arrival date and hatching date are phenological
markers in migrating birds, for example, that can be strongly affected by global warming.
These dynamics have been incorporated into a mathematical model recently 2]. Higher temperatures cause earlier appearance of the insect prey of hatchling birds,
which exerts pressure on birds to breed earlier so that hatchling development coincides
with peak prey abundance. Advanced breeding is dependent on the arrival time of the
adults at the breeding site, as well as the delay between arrival and the start of
breeding. These traits can change synchronously or asynchronously, and a mismatch
between prey abundance and hatching can cause population declines. The mathematical
model 2] explores the dynamics of these interactions and their evolutionary trajectories,
and it can explain patterns observed in European flycatchers. Conversely, departure
from their non-breeding grounds in Africa also appears to occur earlier for at least
some Palearctic migratory birds 3]. Hence, there is a global shift in departure and arrival times that affects migratory
bird movement and local abundance as a result of climate warming.
Phenological shifts in migration of endothermic birds are linked to the abundance
of their ectothermic prey. Although endotherms are also directly affected by changes
in temperature, which affects their metabolic demands for thermoregulation, these
direct effects are more pronounced in ectotherms. The body temperature and hence physiology
of ectotherms such as invertebrates and fish is closely tied to environmental temperatures.
Climate warming will therefore influence metabolism and other physiological processes
directly in ectotherms, and this can have pronounced effects on movement and migration.
The proximate mechanisms that enable movement are the physiological functions that
provide energy to the muscles and the muscles themselves that transform chemical energy
(ATP) to work. All physiological processes are influenced by temperature, to varying
degrees and usually optimal physiological rates are achieved within a relatively narrow
temperature range. At extreme low or high temperatures, cessation of physiological
functions leads to mortality 4]. But even at more benign temperatures that nonetheless diverge from the optimal range,
decreases in physiological performance increase ecological failure by impairing movement
5]. Hence, changing environmental temperatures, including changes resulting from anthropogenic
global warming, impact migration and other ecological processes via the thermal sensitivity
of physiological processes.
A new theoretical model now suggests that in Chinook salmon, metabolic constraints
exacerbate the effect of temperature on the metabolic costs of migration 6]. Salmon often migrate hundreds of kilometres from their natal riverine areas to the
ocean and return to their natal areas for spawning. Salmon prefer relatively cool
water, and increasing water temperatures compromise their cardiovascular and metabolic
physiology 5]. If fish did not have to replenish metabolic substrates (in particular glycogen)
during their migration, the effects of warm water could be mitigated by swimming through
warm sections of river rapidly. However, the need to replenish substrates by resting
in tranquil warm water increases migration times and therefore exposure to warm waters
6]. Replenishment of substrates and increased exposure to warm water reduce the metabolic
scope, that is the energy available for migration, because metabolic maintenance costs
increase in warmer water. These effects are amplified because cardiovascular efficiency
is compromised as temperatures increase beyond optimal ranges, thereby further reducing
metabolic scope. These physiological dynamics mean that climate warming along the
North American west coast has already affected salmon migration 5], 6]. The examples from salmon emphasise that predictions of future effects of climate
change require detailed physiological studies.
Similar to birds, a recent study has shown that the phenology of migration of aphids
in the UK has changed as a result of climate change 7]. Seven hundred seventy trap-years of data collected over the past 50Â years showed
that over 55 species of aphids started flying progressively earlier in the year, and
most species showed increasing duration of their flying season. The severity of the
previous winter was the best predictor for the onset of the subsequent flying season,
and the number of days above 16 °C predicted flying behaviour later in the year 7]. Correlations of phenological changes with climate change are essential starting
points that need to be followed up with experimental approaches to determine the cause-and-effect
relationships between climate change and animal responses 8]. The strength of the salmon studies 5], 6] is that at least some of the mechanistic bases for the climate-dependent change in
migration pattern have been identified. Hence, it is possible to determine the thermal
sensitivity of, for example, cardiovascular function and metabolism experimentally,
and use these data to predict the effects of future or regional climate change.
In addition to shifts in phenology of migrating animals, some species have reduced
their migratory behaviour or even formed sedentary populations as a result of anthropogenic
changes to the environment 9], 10]. A new study now shows that changes in migratory behaviour also alter the incidence
of infectious disease and its transmission 11]. Migration can reduce the incidence of disease because individuals leave contaminated
habitats periodically, individuals are more separated from each other during migration,
and infected individuals are likely to succumb to demanding long-distance movement.
Monarch butterflies in the US have drastically changed their migratory behaviour in
recent years as a result of habitat alterations, and the incidence of sedentary, non-migratory
populations is increasing. Non-migratory populations have a significantly greater
rate of infection by the protozoan Ophryocystis elektroscirrha compared to migratory populations. Infected butterflies have significantly reduced
lifespan 11]. Changes in animal movement and migration as a result of habitat modification and
climate change may therefore alter lifetime fitness of individuals in addition to
biodiversity and ecosystem processes at regional and global scales.