Species at the opposite ends of the life span-brood value spectrum will be most likely to survive climate change
They're everywhere: Burmese pythons, tree rats, kudzu, cockroaches, zebra mussels, lantana, European starlings, purple loosestrife, house sparrows, house mice, house cats -- even viruses, such as West Nile Virus and HIV. These exotics are some of the many species that have managed to gain a foothold in a new area they've never before lived in, and to establish themselves under circumstances they've never before experienced -- often because humans (also an invasive species) have put them there. Some introduced invasives, like brown tree snakes and common brown rats, have decimated the fauna of entire islands. Others, like Chinese mitten crabs, are important to human economies.
Although plenty of plants and animals have successfully invaded an area that is new to them, at least as many such invasion events are unsuccessful. But since species evolve to fill niches in their local habitat, how does a species adapt so effectively to a habitat it's never before experienced so that it becomes a local pest? Is there a special quality that allows a species to become a successful invasive?
Perhaps the most widely-held idea is that invasive species reproduce rapidly. Although this hypothesis is intuitively obvious, it's not as straighforward as it appears. There are two opposing strategies for accomplishing this goal, and they both involve a number of life history trade-offs:
Strategy one: making current reproduction the top priority by quickly producing large broods, thereby allowing the population to grow rapidly. This aggressive reproductive effort reduces the time period when the introduced population is very small and thus vulnerable to extinction due to a random localised event. The trade-offs: reproduction is a metabolically, physiologically and behaviourally demanding activity that significantly reduces adult survival. Since fast-living species invest most of their energy into rapidly producing the next generation, they invest little into anything else and thus, they tend to have short life spans and small body and brain sizes. This set of strategies is known as the population growth hypothesis.
Strategy two: making future reproduction the top priority, thereby providing time for introduced individuals to adapt to the local environment and to investigate their local habitat (if they are animals). This familiarity with a new area makes the introduced population less vulnerable to extinction due to a random localised event and prepares them (and their offspring, when the adults do reproduce) to better cope with the local environment. The trade-offs: the introduced individuals may not survive long enough to reproduce at all. Since they invest their energy into realising future reproductive rewards, many slow-reproducing species have long life spans and large body and brain sizes. This set of strategies is known as the future returns hypothesis.
These two hypotheses are a variation on the old "quantity" versus "quality" argument. But neither hypothesis has much empirical evidence to support it as an effective foundation to support successful invasion.
To gain insight into which life history qualities are shared by invasive species, a team of scientists focused on one taxon: birds. Birds are especially well-suited for these sorts of studies because we know so much about their habits and behaviours, and because we have such a wealth of accurate information about avian introductions. Thus, using bird data from current and historical introductions, it is possible to test individual variables of each hypothesis.
This international scientific team, led by Daniel Sol, a National Spanish Research Council research scientist at the Centre for Ecological Research and Forestry Applications in Catalonia, analysed information collected from 2760 introductions of 428 species of birds from 49 taxonomic families. Forty-seven percent of these introductions were successful somewhere in the world. To analyse the effects of each life history trait on species invasiveness, the team used a generalized linear mixed model (GLMM), the assumption of these models being that when data points deviate from a random distribution, they describe either a positive or negative effect (figure 1):
As predicted by the future returns hypothesis, species with low brood values show a higher probability of establishment than those with a high brood value (figure 1D). The analysis also confirms previous findings that having a large brain relative to body size does promote establishment (figures 1E).
But one finding surprised Dr Sol and his team: the data indicate that producing larger clutches is worse for invaders than producing smaller clutches (figure 1A). But that doesn't make sense ... or does it? Certainly clutch size and brood value are correlated because large clutches are energetically expensive and, for this reason, are very valuable. Thus, loss of a large clutch can be catastrophic.
Interestingly, although the likelihood of establishment increases with the number of individuals introduced, when the team included the size of the founder population -- propagule size -- into their model, none of the conclusions changed.
So the team separately examined the effects of propagule size on establishment success (figure 2):
Based on actual propagule sizes for historic introductions (figure 2A), Dr Sol and his team found that 300 individual birds were sufficient to protect the introduced species from random events that may lead to extinction (figure 2B). They also found that adding more than 300 individuals to the founder population does not significantly increase establishment success.
Having identified the most effective propagule size, the team then tested the effect of growth rates -- "fast-slow" -- on introduction success. They ran 5000 population simulations (figure 2C) and found that slow-lived species are more likely to become established than a fast-lived species (figure 2D), probably because fast-lived species are less likely to have adaptations -- particularly large brain size -- that buffer individuals from random local events.
So clearly, these findings don't disprove the population growth hypothesis, but they certainly do show that growing fast is advantageous only in very special circumstances.
"Growing fast may be advantageous when the population is small, and hence prone to extinction due to demographic accidents, and also when the new environment is similar to that the species finds in its native range", Dr Sol says in email.
But the "fast-slow" life history strategy does not directly consider the effects of another, different, life history strategy: brood value. In short, the fewer reproductive attempts that individuals of a particular species have during their lifetimes, or the larger each brood is, the greater the value of those reproductive attempts, and thus, the higher the brood value. In contrast, low brood value means that the total reproductive effort is distributed over many attempts, either in the same season or in different ones.
Brood value is certainly related to lifespan since long-lived species will probably have more reproductive opportunities than short-lived species -- provided the individual lives long enough to reproduce at all.
"For an invader, unfamiliarity and insufficient adaptation to resources, enemies, and other hazards are likely to increase the risk of reproductive failure", Dr Sol explained in email. "Consequently, the inability to spread the risk over several breeding attempts and/or to delay reproduction if conditions are unfavourable may have important costs."
However, brood value is not entirely dependent upon lifespan, indicating this is a different life history trait.
"You can also have a low brood value if you reproduce frequently", notes Dr Sol. "For example, feral pigeons may lay many clutches in a same year, so for them, losing a reproductive event has little fitness effects because they can ... reproduce again in the near future."
To untangle the effects of these two life history strategies, Dr Sol and his team constructed a regression tree describing brood value in relation to maximum lifespan and invasion potential (figure 3):
As you can see in the above figure, the opposite ends of the brood value-life history spectrum make the most successful invaders: those species that either combine a short life span with several broods per year or a very long life span with a single clutch per year are significantly more successful invaders than species that have high brood values. In fact, there is no single strategy necessary to be a successful invader.
"[This] explains why the type of species that are frequently successful invaders are not the ones one would expect", wrote co-author Rob Freckleton in email. Professor Freckleton is a Royal Society University Research Fellow and Professor of Population Biology at the University of Sheffield.
For example, some of these unexpected invasives in the UK include ring-necked parakeets, collared doves, little egrets, and spoonbills and cattle egrets have been breeding in the UK in recent times.
This research has important applications for conservation biology.
"Re-invasions and re-introductions have been successful for ospreys and red kites amongst others", Professor Freckleton continued. "These are not the sort of species one thinks of when considering invasives -- in other taxa, invasives tend to be species with much 'faster' life-histories."
But these findings are based on data gathered from invasive bird species; so how applicable are they to other taxa, such as mammals, reptiles -- I am thinking of brown tree snakes and boa constrictors in particular -- or even plants?
"We expect similar results in other vertebrates," replied Dr Sol in email. "[B]ut it is possible that a high current reproductive effort (in contrast to a future reproduction strategy) exerts greater influence on establishment success in organisms with more limited capacity than birds to explore the environment and to develop behavioral responses to novel challenges. This will have to be validated in the future."
These findings serve to underscore the complexities involved in predicting which species may become invasive.
"Our results seem to indicate that single trait explanations of invasiveness are not likely to be general: one needs a more 'holistic' view that accounts for the stochastic nature of the environments in which species find themselves", Professor Freckleton explained in email. "Hence our measure of brood value, which accounts for the ability of species to prioritise current survival over future reproduction."
"The finding that investing in future rather than in current reproduction is not unexpected," since the future returns hypothesis predicts this, Dr Sol explains. "[B]ut it had never been suggested in the invasion biology literature."
At the theoretical level, the observation that investing in future reproductive returns facilitates invasion success integrates a variety of hypotheses that view different life histories as evolutionary solutions to environmental uncertainties. Thus, these findings have broader implications beyond helping scientists conserve endangered species and predicting which species are most likely to become invasive, if provided the opportunity to do so -- these findings can also help identify species that are most vulnerable to climate change.
"We predict that species with high brood value should be more vulnerable to climate change, as they should suffer more from extreme events", writes Dr Sol in email.
"[S]pecies that invest in future reproduction should be better able to deal with climate change, as the fitness value of losing a reproductive event are less important", explains Dr Sol. "[I]n addition, these species may have more time to behaviorally adjust to the changes."
Dr Sol then points out that this is an empirical issue, that "one may also argue that species that have short generation times are more able to produce evolutionary responses to climate change."
So it would seem that, as with invasive species, one may argue that species at the opposite ends of the life span-brood value spectrum will be most likely to survive climate change.
Sources:
Daniel Sol, Joan Maspons, Miquel Vall-llosera, Ignasi Bartomeus, Gabriel E. García-Peña, Josep Piñol, & Robert P. Freckleton (2012). Unraveling the Life History of Successful Invaders. Science, 337 (6094), 580-583. doi:10.1126/science.1221523
Rob Freckleton, emails: 30 July 2012.
Daniel Sol, emails: 3, 6 & 22 August 2012.
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