Food for sex

18 03 2013
Quercus_KakFeed Photo
Kakapo are unique among the ~ 400 parrot species (Psittaciformes) for being flightless, nocturnal and extremely long-lived (up to 100 years!). Additionally, they are herbivorous (seeds, fruits, polen, plants), males can weigh up to 2-4 kg (40% heavier than females), and females lay their eggs on the ground or cavities – i.e., 3 eggs in a single clutch annually, although 2 clutches might occur if the nest fails at the beginning of the reproductive season or if the eggs are taken for artificial incubation.Native to New Zealand, kakapo once inhabited the subalpine fringes of forest and scrub. Polynesians (1000 years ago) and Europeans (mostly in the XIX Century) arrived in the archipelago accompanied by dogs, cats, rats and mustelids that cornered kakapo populations in the Fiordland region (south-west of the South Island) where it was declared extinct in 1989. In 1977, a population of some 200 individuals was found on Stewart Island - this population was already in decline to the claws and jaws of feral cats. By the 1980s, the failure of captive breeding programs prompted the transfer of 60 individuals from Steward to carnivore-free islands. The global (known) population ‘rocketed’ from 50 individuals in 1999 to 126 in the 2012 censuses and, consequently, the kakapo’s IUCN status changed in 2000 from ‘Extinct in the Wild’ to ‘Critically Endangered’. Under the management of the Kakapo Recovery Programme, kakapo are now present on the islands of CodfishAnchor and Little Barrier.

Inbreeding, system shocks caused by fire or cyclones (for example), or demographic stochasticity (by which two or more outcomes are possible) such as how many males and females will be born in a single year, are all factors that threaten the persistence of small and fragmented populations. They can, however, be reverted by conservation actions.

If you have ever taken dancing classes, you will be familiar with the scarcity of male partners and how this can jeopardize group learning. When reproduction, rather than salsa pirouettes, is at stake, a biased sex ratio can compromise the persistence of species. For instance, when females are unable to find males (or vice versa), fertility rates can collapse as a result – a well-known cause of an Allee effect (1). Curiously, natural selection can promote such bias by favouring a species’ investment in litters dominated by one of the two genders. The evolutionary formulation of such scenario is that females can adjust the sex ratio of their offspring depending on the amount of available resources (2) – see contrasting cross-taxa studies on this subject (3-5). Thus, when resources abound (e.g., food), mothers can afford the offspring’s gender requiring more resources to reach adulthood or once adulthood is reached, is less likely to reproduce successfully (6). This predisposition to one gender or another can be key to the conservation of endangered species (7).

The kakapo case

At the end of the 1990s, the New Zealand Department of Conservation placed dispensers of supplementary food in the territories of some kakapo (a rather enormous, flightless parrot Strigops habroptilus) to encourage their reproduction. Back then, only 60 individuals were left of the entire species . Unfortunately, those females with access to the supplemental food conceived 67% of male chicks (so exacerbating the fact that kakapo populations are naturally male-biased), while those females without extra feeding had 71% of female chicks (8). Something wasn’t working. Read the rest of this entry »





De-extinction is about as sensible as de-death

15 03 2013

Published simultaneously in The Conversation.


On Friday, March 15 in Washington DC, National Geographic and TEDx are hosting a day-long conference on species-revival science and ethics. In other words, they will be debating whether we can, and should, attempt to bring extinct animals back to life – a concept some call “de-extinction”.

The debate has an interesting line-up of ecologists, geneticists, palaeontologists (including Australia’s own Mike Archer), developmental biologists, journalists, lawyers, ethicists and even artists. I have no doubt it will be very entertaining.

But let’s not mistake entertainment for reality. It disappoints me, a conservation scientist, that this tired fantasy still manages to generate serious interest. I have little doubt what the ecologists at the debate will conclude.

Once again, it’s important to discuss the principal flaws in such proposals.

Put aside for the moment the astounding inefficiency, the lack of success to date and the welfare issues of bringing something into existence only to suffer a short and likely painful life. The principal reason we should not even consider the technology from a conservation perspective is that it does not address the real problem – mainly, the reason for extinction in the first place.

Even if we could solve all the other problems, if there is no place to put these new individuals, the effort and money expended is a complete waste. Habitat loss is the principal driver of species extinction and endangerment. If we don’t stop and reverse this now, all other avenues are effectively closed. Cloning will not create new forests or coral reefs, for example. Read the rest of this entry »





Translocations: the genetic rescue paradox

14 01 2013

helphindranceHarvesting and habitat alteration reduce many populations to just a few individuals, and then often extinction. A widely recommended conservation action is to supplement those populations with new individuals translocated from other regions. However, crossing local and foreign genes can worsen the prospects of recovery.

We are all hybrids or combinations of other people, experiences and things. Let’s think of teams (e.g., engineers, athletes, mushroom collectors). In team work, isolation from other team members might limit the appearance of innovative ideas, but the arrival of new (conflictive) individuals might in fact destroy group dynamics altogether. Chromosomes work much like this – too little or too much genetic variability among parents can break down the fitness of their descendants. These pernicious effects are known as ‘inbreeding depression‘ when they result from reproduction among related individuals, and ‘outbreeding depression‘ when parents are too genetically distant.

CB_OutbreedingDepression Photo
Location of the two USA sites providing spawners of largemouth bass for the experiments by Goldberg et al. (3): the Kaskaskia River (Mississipi Basin, Illinois) and the Big Cedar Lake (Great Lakes Basin, Wisconsin). Next to the map is shown an array of three of the 72-litre aquaria in an indoor environment under constant ambient temperature (25 ◦C), humidity (60%), and photoperiod (alternate 12 hours of light and darkness). Photo courtesy of T. Goldberg.

Recent studies have revised outbreeding depression in a variety of plants, invertebrates and vertebrates (1, 2). An example is Tony Goldberg’s experiments on largemouth bass (Micropterus salmoides), a freshwater fish native to North America. Since the 1990s, the USA populations have been hit by disease from a Ranavirus. Goldberg et al. (3) sampled healthy individuals from two freshwater bodies: the Mississipi River and the Great Lakes, and created two genetic lineages by having both populations isolated and reproducing in experimental ponds. Then, they inoculated the Ranavirus in a group of parents from each freshwater basin (generation P), and in the first (G1) and second (G2) generations of hybrids crossed from both basins. After 3 weeks in experimental aquaria, the proportion of survivors declined to nearly 30% in G2, and exceeded 80% in G1 and P. Clearly, crossing of different genetic lineages increased the susceptibility of this species to a pathogen, and the impact was most deleterious in G2. This investigation indicates that translocation of foreign individuals into a self-reproducing population can not only import diseases, but also weaken its descendants’ resistance to future epidemics.

A mechanism causing outbreeding depression occurs when hybridisation alters a gene that is only functional in combination with other genes. Immune systems are often regulated by these complexes of co-adapted genes (‘supergenes’) and their disruption is a potential candidate for the outbreeding depression reported by Goldberg et al. (3). Along with accentuating susceptibility to disease, outbreeding depression in animals and plants can cause a variety of deleterious effects such as dwarfism, low fertility, or shortened life span. Dick Frankham (one of our collaborators) has quantified that the probability of outbreeding depression increases when mixing takes place between (i) different species, (ii) conspecifics adapted to different habitats, (iii) conspecifics with fixed chromosomal differences, and (iv) populations free of genetic flow with other populations for more than 500 years (2).

A striking example supporting (some of) those criteria is the pink salmon (Oncorhynchus gorbuscha) from Auke Creek near Juneau (Alaska). The adults migrate from the Pacific to their native river where they spawn two years after birth, with the particularity that there are two strict broodlines that spawn in either even or odd year – that is, the same species in the same river, but with a lack of genetic flow between populations. In vitro mixture of the two broodlines and later release of hybrids in the wild have shown that the second generation of hybrids had nearly 50% higher mortality rates (i.e., failure to return to spawn following release) when born from crossings of parents from different broodlines than when broodlines were not mixed (4).

Read the rest of this entry »





Ecology is a Tower of Babel

17 09 2012

The term ‘ecology’ in 16 different languages overlaid on the oil on board ‘The Tower of Babel’ by Flemish Renaissance painter Pieter Bruegel the Elder (1563).

In his song ‘Balada de Babel’, the Spanish artist Luis Eduardo Aute sings several lyrics in unison with the same melody. The effect is a wonderful mess. This is what the scientific literature sounds like when authors generate synonymies (equivalent meaning) and polysemies (multiple meanings), or coin terms to show a point of view. In our recent paper published in Oecologia, we illustrate this problem with regard to ‘density dependence’: a key ecological concept. While the biblical reference is somewhat galling to our atheist dispositions, the analogy is certainly appropriate.

A giant shoal of herring zigzagging in response to a predator; a swarm of social bees tending the multitudinous offspring of their queen; a dense pine forest depriving its own seedlings from light; an over-harvested population of lobsters where individuals can hardly find reproductive mates; pioneering strands of a seaweed colonising a foreign sea after a transoceanic trip attached to the hulk of boat; respiratory parasites spreading in a herd of caribou; or malaria protozoans making their way between mosquitoes and humans – these are all examples of population processes that operate under a density check. The number of individuals within those groups of organisms determines their chances for reproduction, survival or dispersal, which we (ecologists) measure as ‘demographic rates’ (e.g., number of births per mother, number of deaths between consecutive years, or number of immigrants per hectare).

In ecology, the causal relationship between the size of a population and a demographic rate is known as ‘density dependence’ (DD hereafter). This relationship captures the pace at which a demographic rate changes as population size varies in time and/or space. We use DD measurements to infer the operation of social and trophic interactions (cannibalism, competition, cooperation, disease, herbivory, mutualism, parasitism, parasitoidism, predation, reproductive behaviour and the like) between individuals within a population1,2, because the intensity of these interactions varies with population size. Thus, as a population of caribou expands, respiratory parasites will have an easier job to disperse from one animal to another. As the booming parasites breed, increased infestations will kill the weakest caribou or reduce the fertility of females investing too much energy to counteract the infection (yes, immunity is energetically costly, which is why you get sick when you are run down). In turn, as the caribou population decreases, so does the population of parasites3. In cybernetics, such a toing-and-froing is known as ‘feedback’ (a system that controls itself, like a thermostat controls the temperature of a room) – a ‘density feedback’ (Figure 1) is the kind we are highlighting here. Read the rest of this entry »





Ghosts of bottlenecks past

25 05 2012

© D. Bathory

I’ve just spent the last week at beautiful Linnaeus Estate on the northern NSW coast for my third Australian Centre for Ecological Analysis and Synthesis (ACEAS) (see previous post about my last ACEAS workshop).

This workshop is a little different to my last one, and I’m merely a participant (not the organiser) this time. Alan Cooper and members of his Australian Centre for Ancient DNA (Jeremy Austin, Vicki Thomson & Julien Soubrier) combined forces this week with Craig Mortiz, Margaret Byrne, Steve Donnellan, Tania Laity, Leo Joseph, Xander Xue and Gabriele Cybis. Our task was to examine the mounting evidence that many Australian species appear to show a rather shallow genetic pool from a (or several) major past bottlenecks.

What’s a ‘bottleneck’? In reference to the form after which it was named, a genetic bottleneck is the genetic diversity aftermath after a population declines to a small size and then later expands. The history of this reduction and subsequent expansion is written in the DNA, because inevitably gene ‘types’ are lost as most individuals shuffle off this mortal coil. In a way, it’s like losing a large population of people who all speak different languages – inevitably, you’d lose entire languages and the recovering population would grow out of a reduced ‘pool’ of languages, resulting in fewer overall surviving languages.

Our workshop focus started, as many scientific endeavours do, rather serendipitously. Several years ago, Jeremy Austin noticed that devils who had died out on the mainland several thousand years ago had a very low genetic diversity, as do modern-day devils surviving in Tasmania. He thought it was odd because they should have had more on the mainland given that was their principal distribution prior to Europeans arriving. He mentioned this in passing to Steve Donnellan one day and Steve announced that he had seem the same pattern in echidnas. Now, echidnas cover most of Australia’s surface, so that was equally odd. Then they decided to look at another widespread species – tiger snakes, emus, etc. – and found in many of them, the same patterns were there. Read the rest of this entry »





Tentacles of destruction

5 04 2012

This last post before Easter is something I’ve thought more and more about over the last few years. I wouldn’t have given it much time in the past, but I’m now convinced roads are one of the humanity’s most destructive devices. Let me explain.

Before I had a good grasp of extinction dynamics, I wouldn’t have attributed much import to the role of roads in conservation. I mean, really, a little road here and there (ok, even a major motorway) couldn’t possibly be a problem? It’s mostly habitat destruction itself, right?

Not exactly. With our work on extinction synergies, I eventually came to realise that roads are some of the first portals to the devastation to come. Read the rest of this entry »





Conservation catastrophes

22 02 2012

David Reed

The title of this post serves two functions: (1) to introduce the concept of ecological catastrophes in population viability modelling, and (2) to acknowledge the passing of the bloke who came up with a clever way of dealing with that uncertainty.

I’ll start with latter first. It came to my attention late last year that a fellow conservation biologist colleague, Dr. David Reed, died unexpectedly from congestive heart failure. I did not really mourn his passing, for I had never met him in person (I believe it is disingenuous, discourteous, and slightly egocentric to mourn someone who you do not really know personally – but that’s just my opinion), but I did think at the time that the conservation community had lost another clever progenitor of good conservation science. As many CB readers already know, we lost a great conservation thinker and doer last year, Professor Navjot Sodhi (and that, I did take personally). Coincidentally, both Navjot and David died at about the same age (49 and 48, respectively). I hope that the being in one’s late 40s isn’t particularly presaged for people in my line of business!

My friend, colleague and lab co-director, Professor Barry Brook, did, however, work a little with David, and together they published some pretty cool stuff (see References below). David was particularly good at looking for cross-taxa generalities in conservation phenomena, such as minimum viable population sizes, effects of inbreeding depression, applications of population viability analysis and extinction risk. But more on some of that below. Read the rest of this entry »





Not magic, but necessary

18 10 2011

In April this year, some American colleagues of ours wrote a rather detailed, 10-page article in Trends in Ecology and Evolution that attacked our concept of generalizing minimum viable population (MVP) size estimates among species. Steve Beissinger of the University of California at Berkeley, one of the paper’s co-authors, has been a particularly vocal adversary of some of the applications of population viability analysis and its child, MVP size, for many years. While there was some interesting points raised in their review, their arguments largely lacked any real punch, and they essentially ended up agreeing with us.

Let me explain. Today, our response to that critique was published online in the same journal: Minimum viable population size: not magic, but necessary. I want to take some time here to summarise the main points of contention and our rebuttal.

But first, let’s recap what we have been arguing all along in several papers over the last few years (i.e., Brook et al. 2006; Traill et al. 2007, 2010; Clements et al. 2011) – a minimum viable population size is the point at which a declining population becomes a small population (sensu Caughley 1994). In other words, it’s the point at which a population becomes susceptible to random (stochastic) events that wouldn’t otherwise matter for a small population.

Consider the great auk (Pinguinus impennis), a formerly widespread and abundant North Atlantic species that was reduced by intensive hunting throughout its range. How did it eventually go extinct? The last remaining population blew up in a volcanic explosion off the coast of Iceland (Halliday 1978). Had the population been large, the small dent in the population due to the loss of those individuals would have been irrelevant.

But what is ‘large’? The empirical evidence, as we’ve pointed out time and time again, is that large = thousands, not hundreds, of individuals.

So this is why we advocate that conservation targets should aim to keep at or recover to the thousands mark. Less than that, and you’re playing Russian roulette with a species’ existence. Read the rest of this entry »





Life, death and Linneaus

9 07 2011

Barry Brook (left) and Lian Pin Koh (right) attacking Fangliang He (centre). © CJA Bradshaw

I’m sitting in the Brisbane airport contemplating how best to describe the last week. If you’ve been following my tweets, you’ll know that I’ve been sequestered in a room with 8 other academics trying to figure out the best ways to estimate the severity of the Anthropocene extinction crisis. Seems like a pretty straight forward task. We know biodiversity in general isn’t doing so well thanks to the 7 billion Homo sapiens on the planet (hence, the Anthropo prefix) - the question though is: how bad?

I blogged back in March that a group of us were awarded a fully funded series of workshops to address that question by the Australian Centre for Ecological Synthesis and Analysis (a Terrestrial Ecosystem Research Network facility based at the University of Queensland), and so I am essentially updating you on the progress of the first workshop.

Before I summarise our achievements (and achieve, we did), I just want to describe the venue. Instead of our standard, boring, windowless room in some non-descript building on campus, ACEAS Director, Associate Professor Alison Specht, had the brilliant idea of putting us out away from it all on a beautiful nature-conservation estate on the north coast of New South Wales.

What a beautiful place – Linneaus Estate is a 111-ha property just a few kilometres north of Lennox Head (about 30 minutes by car south of Byron Bay) whose mission is to provide a sustainable living area (for a very lucky few) while protecting and restoring some pretty amazing coastal habitat along an otherwise well-developed bit of Australian coastline. And yes, it’s named after Carl Linnaeus. Read the rest of this entry »





The rarity paradox

22 06 2011

© C. Madden

My friend and colleague at the Centre National de Recherche Scientfique (CNRS), Laboratoire d’Ecologie Systématique & Evolution based at the Université Paris-Sud in France, Dr. Franck ‘Allee EffectCourchamp, has asked me to help him out finding a suitable candidate for what sounds like a very cool job. If you’re in the market for a very interesting and highly relevant conservation post-doctoral fellowship, please read on.

And even if you’re not looking for a position, but are interested in the anthropogenic Allee effect, then by all means, please read on as well.

This two-year fellowship is part of a grant focused on demonstrating the novel rarity paradox, either in new wildlife trade markets (i.e., exotic pets, traditional medicine, et cetera) or in newly exploited species (e.g., tibetan antilope, seahorses, et cetera). Read the rest of this entry »





Classics: Effective population size ratio

27 04 2011

Here’s another concise Conservation Classic highlighted in our upcoming book chapter (see previous entries on this book). Today’s entry comes from a colleague of mine, Dick Frankham, who has literally written the book on conservation genetics. I’ve published with Dick a few times – absolutely lovely chap who really knows his field more than almost any other. It is a great pleasure to include one of his seminal works as a Conservation Classic.

This entry is highly related to our work on minimum viable population size, and the controversial SAFE index (more on that later).

Although it had long been recognized that inbreeding and loss of genetic diversity were accentuated in small, isolated populations (Charlesworth & Charlesworth, 1987), genetic hazards were generally considered to be of less consequence to extinction risk than demographic and environmental stochasticity. Frankham (1995) helped overturn this viewpoint, using a meta-analysis to draw together comprehensive evidence on the ratio of genetically effective to actual population size (Ne:N). Read the rest of this entry »





Linking disease, demography and climate

1 08 2010

Last week I mentioned that a group of us from Australia were travelling to Chicago to work with Bob Lacy, Phil Miller, JP Pollak and Resit Akcakaya to make some pretty exciting developments in next-generation conservation ecology and management software. Also attending were Barry Brook, our postdocs: Damien Fordham, Thomas Prowse and Mike Watts, our colleague (and former postdoc) Clive McMahon, and a student of Phil’s, Michelle Verant. At the closing of the week-long workshop, I thought I’d share my thoughts on how it all went.

In a word, it was ‘productive’. It’s not often that you can spend 1 week locked in a tiny room with 10 other geeks and produce so many good and state-of-the-art models, but we certainly achieved more than we had anticipated.

Let me explain in brief why it’s so exciting. First, I must say that even the semi-quantitative among you should be ready for the appearance of ‘Meta-Model Manager (MMM)’ in the coming months. This clever piece of software was devised by JP, Bob and Phil to make disparate models ‘talk’ to each other during a population projection run. We had dabbled with MMM a little last year, but its value really came to light this week.

We used MMM to combine several different models that individually fail to capture the full behaviour of a population. Most of you will be familiar with the individual-based population viability (PVA) software Vortex that allows relatively easy PVA model building and is particular useful for predicting extinction risk of small populations. What you most likely don’t know exists is what Phil, Bob and JP call Outbreak – an epidemiological modelling software based on the classic susceptible-exposed-infectious-recovered framework. Outbreak is also an individual-based model that can talk directly to Vortex, but only through MMM. Read the rest of this entry »





Inbreeding does matter

29 03 2010

I’ve been busy with Bill Laurance visiting the University of Adelaide over the last few days, and will be so over the next few as well (and Bill has promised us a guest post shortly), but I wanted to get a post in before the week got away on me.

I’ve come across what is probably the most succinct description of why inbreeding depression is an important aspect of extinctions in free-ranging species (see also previous posts here and here) by Mr. Conservation Genetics himself, Professor Richard Frankham.

Way back in the 1980s (oh, so long ago), Russ Lande produced a landmark paper in Science arguing that population demography was a far more important driver of extinctions than reduced genetic diversity per se. He stated:

“…demography may usually be of more immediate importance than population genetics in determining the minimum viable size of wild populations”

We now know, however, that genetics in fact DO matter, and no one could put it better than Dick Frankham in his latest commentary in Heredity.

I paraphrase some of his main points below:

  • Controversy broke out in the 1970 s when it was suggested that inbreeding was deleterious for captive wildlife, but Ralls and Ballou (1983) reported that 41/44 mammal populations had higher juvenile mortality among inbred than outbred individuals.
  • Crnokrak and Roff (1999) established that inbreeding depression occurred in 90 % of the datasets they examined, and was similarly deleterious across major plant and animal taxa.
  • They estimated that inbreeding depression in the wild has approximately seven times greater impact than in captivity.
  • It is unrealistic to omit inbreeding depression from population viability analysis models.
  • Lande’s contention was rejected when Spielman et al. (2004) found that genetic diversity in 170 threatened taxa was lower than in related non-threatened taxa

Lande might have been incorrect, but his contention spawned the entire modern discipline of conservation genetics. Dick sums up all this so much more eloquently than I’ve done here, so I encourage you to read his article.

CJA Bradshaw

ResearchBlogging.orgFrankham, R. (2009). Inbreeding in the wild really does matter Heredity, 104 (2), 124-124 DOI: 10.1038/hdy.2009.155

Lande, R. (1988). Genetics and demography in biological conservation Science, 241 (4872), 1455-1460 DOI: 10.1126/science.3420403

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Inbreeding bad for invasives too

18 02 2010

I just came across this little gem of a paper in Molecular Ecology (not, by any stretch, a common forum for biodiversity conservation-related papers). It’s another one of those wonderful little experimental manipulation studies I love so much (see previous examples here and here).

I’ve written a lot before about the loss of genetic diversity as a contributing factor to extinction risk, via things like Allee effects and inbreeding depression. I’ve also posted blurbs about our work and that of others on what makes particular species prone to become extinct or invasive (i.e., the two sides of the same evolutionary coin). Now Crawford and Whitney bring these two themes together in their paper entitled Population genetic diversity influences colonization success.

Yes, the evolved traits of a particular species will set it up either to do well or very badly under rapid environmental change, and invasive species tend to be those with rapid generation times, defence mechanisms, heightened dispersal capacity and rapid growth. However, such traits generally only predict a small amount in the variation in invasion success – the other being of course propagule pressure (a composite measure of the number of individuals of a non-native species [propagule size] introduced to a novel environment and the number of introduction events [propagule number] into the new host environment).

But, that’s not all. It turns out that just as reduced genetic diversity enhances a threatened species’ risk of extinction, so too does it reduce the ‘invasiveness’ of a weed. Using experimentally manipulated populations of the weedy herb Arabidopsis thaliana (mouse-ear cress; see if you get the joke), Crawford & Whitney measured greater population-level seedling emergence rates, biomass production, flowering duration and reproduction in high-diversity populations compared to lower-diversity ones. Maintain a high genetic diversity and your invasive species has a much higher potential to colonise a novel environment and spread throughout it.

Of course, this is related to propagule pressure because the more individuals that invade/are introduced the more times, the higher the likelihood that different genomes will be introduced as well. This is extremely important from a management perspective because it means that well-mixed (outbred) samples of invasive species probably can do a lot more damage to native biodiversity than a few, genetically similar individuals alone. Indeed, most introductions probably don’t result in a successful invasion mainly because they don’t have the genetic diversity to get over the hump of inbreeding depression in the first place.

The higher genetic (and therefore, phenotypic) variation in your pool of introduced individuals, the great the chance that at least a few will survive and proliferate. This is also a good bit of extra proof for our proposal that invasion and extinction are two sides of the same evolutionary coin.

CJA Bradshaw

ResearchBlogging.orgCrawford, K., & Whitney, K. (2010). Population genetic diversity influences colonization success Molecular Ecology DOI: 10.1111/j.1365-294X.2010.04550.x

Bradshaw, C., Giam, X., Tan, H., Brook, B., & Sodhi, N. (2008). Threat or invasive status in legumes is related to opposite extremes of the same ecological and life-history attributes Journal of Ecology, 96, 869-883 DOI: 10.1111/j.1365-2745.2008.01408.x

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The elusive Allee effect

8 01 2010

© D. Bishop, Getty Images

In keeping with the theme of extinctions from my last post, I want to highlight a paper we’ve recently had published online early in Ecology entitled Limited evidence for the demographic Allee effect from numerous species across taxa by Stephen Gregory and colleagues. This one is all about Allee effects - well, it’s all about how difficult it is to find them!

If you recall, an Allee effect is a “…positive relationship between any component of individual fitness and either numbers or density of conspecifics” (Stephens et al. 1999, Oikos 87:185-190) and the name itself is attributed to Warder Clyde Allee. There are many different kinds of Allee effects (see previous Allee effects post for Berec and colleagues’ full list of types and definitions), but the two I want to focus on here are component and demographic Allee effects.
© Elsevier
© Elsevier
component Allee effect modifies one or many surrogate measures of fitness (e.g., heterozygosity, survival rate, fertility, etc.), whereas a demographic Allee effect is a manifestation of component Allee effect(s) that lead to a reduction of the population rate of change at low population sizes (or conversely, an increase in the rate of growth as a population expands). The graph to the left shows this concept schematically.

Now, the evidence for component Allee effects abounds, but finding real instances of reduced population growth rate at low population sizes is difficult. And this is really what we should be focussing on in conservation biology – a lower-than-expected growth rate at low population sizes means that recovery efforts for rare and endangered species must be stepped up considerably because their rebound potential is lower than it should be.

We therefore queried over 1000 time series of abundance from many different species and lo and behold, the evidence for that little dip in population growth rate at low densities was indeed rare – about 1 % of all time series examined!

I suppose this isn’t that surprising, but what was interesting was that this didn’t depend on sample size (time series where Allee models had highest support were in fact shorter) or variability (they were also less variable). All this seems a little counter-intuitive, but it gels with what’s been assumed or hypothesised before. Measurement error, climate variability and the sheer paucity of low-abundance time series makes their detection difficult. Nonetheless, for those series showing demographic Allee effects, their relative model support was around 12%, suggesting that such density feedback might influence the population growth rate of just over 1 in 10 natural populations. In fact, the many problems with density feedback detections in time series that load toward negative feedback (sometimes spuriously) suggest that even our small sample of Allee time series are probably vastly underestimated. We have pretty firm evidence that inbreeding is prevalent in threatened species, and demographic Allee effects are the mechanism by which such depression can lead a population down the extinction vortex.

CJA Bradshaw

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ResearchBlogging.orgGregory, S., Bradshaw, C.J.A., Brook, B.W., & Courchamp, F. (2009). Limited evidence for the demographic Allee effect from numerous species across taxa Ecology DOI: 10.1890/09-1128





Wobbling to extinction

31 08 2009

crashI’ve been meaning to highlight for a while a paper that I’m finding more and more pertinent as a citation in my own work. The general theme is concerned with estimating extinction risk of a particular population, species (or even ecosystem), and more and more we’re finding that different drivers of population decline and eventual extinction often act synergistically to drive populations to that point of no return.

In other words, the whole is greater than the sum of its parts.

In other, other words, extinction risk is usually much higher than we generally appreciate.

This might seem at odds with my previous post about the tendency of the stochastic exponential growth model to over-estimate extinction risk using abundance time series, but it’s really more of a reflection of our under-appreciation of the complexity of the extinction process.

In the early days of ConservationBytes.com I highlighted a paper by Fagan & Holmes that described some of the few time series of population abundances right up until the point of extinction – the reason these datasets are so rare is because it gets bloody hard to find the last few individuals before extinction can be confirmed. Most recently, Melbourne & Hastings described in a paper entitled Extinction risk depends strongly on factors contributing to stochasticity published in Nature last year how an under-appreciated component of variation in abundance leads to under-estimation of extinction risk.

‘Demographic stochasticity’ is a fancy term for variation in the probability of births deaths at the individual level. Basically this means that there will be all sorts of complicating factors that move any individual in a population away from its expected (mean) probability of dying or reproducing. When taken as a mean over a lot of individuals, it has generally been assumed that demographic stochasticity is washed out by other forms of variation in mean (population-level) birth and death probability resulting from vagaries of the environmental context (e.g., droughts, fires, floods, etc.).

‘No, no, no’, say Melbourne & Hastings. Using some relatively simple laboratory experiments where environmental stochasticity was tightly controlled, they showed that demographic stochasticity dominated the overall variance and that environmental variation took a back seat. The upshot of all these experiments and mathematical models is that for most species of conservation concern (i.e., populations already reduced below to their minimum viable populations size), not factoring in the appropriate measures of demographic wobble means that most people are under-estimating extinction risk.

Bloody hell – we’ve been saying this for years; a few hundred individuals in any population is a ridiculous conservation target. People must instead focus on getting their favourite endangered species to number at least in the several thousands if the species is to have any hope of persisting (this is foreshadowing a paper we have coming out shortly in Biological Conservationstay tuned for a post thereupon).

Melbourne & Hastings have done a grand job in reminding us how truly susceptible small populations are to wobbling over the line and disappearing forever.

CJA Bradshaw

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Hot inbreeding

22 07 2009
inbreeding

© R. Ballen

Sounds really disgusting a little rude, doesn’t it? Well, if you think losing species because of successive bottlenecks from harvesting, habitat loss and genetic deterioration is rude, then the title of this post is appropriate.

I’m highlighting today a paper recently published in Conservation Biology by Kristensen and colleagues entitled Linking inbreeding effects in captive populations with fitness in the wild: release of replicated Drosophila melanogaster lines under different temperatures.

The debate has been around for years – do inbred populations have lower fitness (e.g., reproductive success, survival, dispersal, etc.) than their ‘outbred’ counterparts? Is one of the reasons small populations (below their minimum viable population size) have a high risk of extinction because genetic deterioration erodes fitness?

While there are many species that seem to defy this assumption, the increasing prevalence of Allee effects, and the demonstration that threatened species have lower genetic diversity than non-threatened species, all seem to support the idea. Kristensen & colleagues’ paper uses that cornerstone of genetic guinea pigs, the Drosophila fruit fly, not only to demonstrate inbreeding depression in the lab, but also the subsequent fate of inbred individuals released into the wild.

What they found was quite amazing. Released inbred flies only did poorly (i.e., weren’t caught as frequently meaning that they probably were less successful in finding food and perished) relative to outbred flies when the temperature was warm (daytime). Cold (i.e., night) releases failed to show any difference between inbred and outbred flies.

Basically this means that the environment interacts strongly with the genetic code that signals for particularly performances. When the going is tough (and if you’re an ectothermic fly, extreme heat can be the killer), then genetically compromised individuals do badly. Another reasons to be worried about runaway global climate warming.

Another important point was that the indices of performance didn’t translate universally to the field conditions, so lab-only results might very well give us some incorrect predictions of animal performance when populations reach small sizes and become inbred.

CJA Bradshaw





Perceptions on poverty: the rising Middle Class

16 03 2009

I’m being somewhat ‘lazy’ this week in that I have unfortunately less time to spend on pertinent blog posts than I’d like (lecturing, looming deadlines, that sort of thing). So, I start out this week’s posts with one of my favourite TED talks – Hans Rosling debunks myths about the developing world.

What’s the relevance to biodiversity conservation? I’ll admit, it may appear somewhat tangential, but there are a few important messages (both potentially good and bad):

1. POSSIBLE BENEFIT #1: The rising wealth in the developing world and associated reduction in family size may inevitably curb our human population growth rates;

2. POSSIBLE DISADVANTAGE #1: Rising wealth will necessarily mean more and more consumption, and as we know at least for tropical developing nations, resource consumption is killing biodiversity faster than anywhere else on the planet;

3. POSSIBLE DISADVANTAGE #2: As family wealth rises, so too do opportunities do opportunities for the Anthropogenic Allee effect (consuming rare species just because you can afford to do so);

4. POSSIBLE BENEFIT #2: Better health care associated with rising wealth and lower infant mortality might make education a higher priority, teaching more people about the necessity of safeguarding ecosystem services.

I’m not convinced the advantages will necessarily outweigh the disadvantages; regardless, Prof. Rosling’s amazing 20-minute presentation will both entertain and enlighten. I recommend it for a lunchtime sitting or that late-afternoon attention wain.

CJA Bradshaw

more about “Hans Rosling shows the best stats you…“, posted with vodpod




Rare just tastes better

11 02 2009

I had written this a while ago for publication, but my timing was out and no one had room to publish it. So, I’m reproducing it here as an extension to a previous post (That looks rare – I’ll kill that one).

As the international market for luxury goods expands in value, extent and diversity of items (Nueno & Quelch 1998), the world’s burgeoning pool of already threatened species stands to worsen. Economic theory predicts that harvested species should eventually find refuge from over-exploitation because it simply becomes too costly to find the last remaining wild individuals (Koford & Tschoegl 1998). However, the self-reinforcing cycle of human greed (Brook & Sodhi 2006) can make rare species increasingly valuable to a few select consumers such that mounting financial incentives drive species to extinction (Courchamp et al. 2006). The economic and ecological arguments are compelling, but to date there has been little emphasis on how the phenomenon arises in the human thought process, nor how apparently irrational behaviour can persist. Gault and colleagues (2008) have addressed this gap in a paper published recently in Conservation Letters by examining consumer preferences for arguably one of the most stereotypical luxury food items, caviar from the 200-million-year-old sturgeon (Acipenser spp.).

Sturgeon (6 genera) populations worldwide are in trouble, with all but two of the 27 known species threatened with extinction (either Near Threatened, Vulnerable, Endangered or Critically Endangered) according to the International Union for Conservation of Nature and Natural Resources’ (IUCN) Red List of Threatened Species. Despite all 27 species also having strict international trade restrictions imposed by the Convention on International Trade in Endangered Species (CITES) (Gault et al. 2008), intense commercial pressure persists for 15 of these at an estimated global value exceeding US$200 million annually (Pikitch et al. 2005). The very existence of the industry itself and the luxury good it produces are therefore, at least for some regions, unlikely to endure over the next decade (Pala 2007). What drives such irrational behaviour and why can we not seem to prevent such coveted species from spiralling down the extinction vortex?

Gault and colleagues addressed this question specifically in an elegantly simple set of preference experiments targeting the very end-consumers of the caviar production line – French connoisseurs. Some particularly remarkable results were derived from presentations of identical caviar; 86 % of attendees of luxury receptions not only preferred falsely labelled ‘rarer’ Siberian caviar (A. baeri) after blind tasting experiments, they also scored what they believed was caviar from the rarer species as having a higher ‘gustative quality’. These high-brow results were compared to more modest consumers in French supermarkets, with similar conclusions. Not only were unsuspecting gourmands fooled into believing the experimental propaganda, subjects in both cases stated a preference for seemingly rarer caviar even prior to tasting.

The psycho-sociological implications of perceived rarity are disturbing themselves; but Gault and colleagues extended their results with a mathematical game theory model demonstrating how irrational choices drive just such a harvested species to extinction. The economic implications of attempting to curb exploitation as species become rarer when the irrationality of perceived rarity was taken into consideration were telling – there is no payoff in delaying exploitation as more and more consumers are capable of entering the market. In other words, the assumption that consumers apply a positive temporal discount rate to their payoff (Olson & Bailey 1981) is wrong, with the demographic corollary that total depletion of the resource ensues. The authors contend that such artificial value may drive the entire luxury goods market based mainly on the self-consciousness and social status of consumers able to afford these symbols of affluence.

The poor record of species over-exploitation by humans arising from the Tragedy of the Commons (Hardin 1968) is compounded by this new information. This anthropogenic Allee effect (Courchamp et al. 2006) provides a novel example mechanism for how small populations are driven ever-downward because low densities ensure declining fitness. Many species may follow the same general rules, from bluefin tuna, Napoleon wrasse lips and shark fins, to reptile skins and Tibetan antelope woollen shawls. Gault and colleagues warn that as the human population continues to expand and more people enter the luxury-goods market, more wildlife species will succumb to this Allee effect-driven extinction vortex.

The authors suggest that a combination of consumer education and the encouragement of farmed substitute caviar will be more effective than potentially counter-productive trading bans that ultimately encourage illegal trade. However, the preference results suggest that education might not promote positive action given that reluctance of affluent consumers to self-limit. I believe that the way forward instead requires a combination of international trade bans, certification schemes for ‘sustainable’ goods that flood markets to increase supply and reduce price, better controls on point-of-origin labelling, and even state-controlled ‘warning’ systems to alert prospective consumers that they are enhancing the extinction risk of the very products they enjoy. A better architecture for trading schemes and market systems that embrace long-term persistence can surely counteract the irrationality of the human-induced destruction of global ecosystem services. We just need to put our minds and pocketbooks to the task.

CJA Bradshaw

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Just give them a lift

16 01 2009
© iClipart

© iClipart

One of the main problems in a rapidly changing world, whether that change arises from habitat loss, invasive species or climate change, is that often the pace of change is simply too fast for many species to keep up. History (both ‘deep-time’ and contemporary evidence) tells us this fact very clearly in the record of extinctions – species that have ‘slow’ life histories (i.e., those that mature late in their lives, produce few young and breed infrequently) are the most susceptible to extinction. More often than not, these tend to be the big organisms because the pace of life scales to body size nonlinearly (the so-called allometry of vital rates). The problem extends to evolution – when the pace of change happens faster than mutation and subsequent natural selection, you are unable to ‘evolve’ to the new environmental state fast enough. The end result – extinction.

So, can we help? Well, it’s fairly difficult to alter reproductive rates unless you do some assisted breeding programme (which generally don’t do much for the conservation status of a species) and you can’t really alter age at maturity or growth rates. You can stop or reverse habitat destruction, and you can translocate species in some circumstances.

So, in the case of climate change, if local conditions become too unbearable for a species (temperature, salinity, precipitation, etc.), just give them a lift to another spot where the new conditions suit! Sounds simple, but it could be rather difficult.

A relatively new Policy Forum piece in Science outlines how ‘assisted colonisation‘ could work for some species. The issues are many – most translocations fail for one reason or another (too few individuals moved, unforeseen predators or competitors, lack of appropriate habitat, etc.), but as we’ve seen the world over in the case of successful alien species, invasions can be remarkably successful (at least from the perspective of the invading species).

The key then is to think very carefully about which species to move and which to leave alone. Of course, generalist, highly adaptable and dispersed species probably don’t need the help, but restricted-range species or habitat specialists could really benefit from such action. You also run the risk of creating more problems than you solve (e.g., new invasive pests, disease introduction). However, a select group of species might just need this very assistance to persist given how much we’ve already change the biosphere, and how much more it will change due to shifting climate in the near future.

It’s controversial, but it could work in many circumstances. That’s why I’m adding this paper (Hoegh-Guldberg et al. – Assisted colonization and rapid climate change) to the Potential list.

CJA Bradshaw

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