The Wildlife Side of Ebola: What Animal Ecology Can Contribute to Studying the Spread of a Deadly Virus

chimpanzee troop 6 v2

Chimpanzees in Kibale National Park, Uganda. Photo: Julie Rushmore.

Ebola virus as a zoonotic pathogen

The current Ebola virus outbreak in West Africa is very much on people’s minds as a story of human suffering and death, with nearly 15,000 Ebola cases reported from West Africa as of November. Ebola virus spreads rather slowly but causes a remarkably high fatality rate, with 50% or more of human cases ending in death. The current epidemic dwarfs the cumulative number of cases in previous localized outbreaks, motivating new research into vaccines, treatments, and efforts to slow Ebola spread. Promising signs of slowing transmission have emerged in recent weeks, but many experts predict that widespread vaccination will be needed to fully halt the epidemic. The social, political and economic impacts of the current Ebola virus epidemic will likely linger for years to come.

What many people do not realize is that humans are atypical hosts for Ebola virus, and the origin of this pathogen is far removed from cities, airports and hospitals, and reminds us of the connections between human and animal health. Ebola virus most commonly exists in and around the African rainforests in the Congo Basin, with previous outbreaks extending east to Uganda, north to Sudan and west to Gabon and the Ivory Coast. Other species have died from this virus: most notably, Ebola killed scores of chimpanzees and gorillas in recent decades. Estimates suggest that in one outbreak alone (2002-2003), thousands of gorillas died, and some researchers saw their entire study populations eliminated in a matter of weeks. Given that wild apes are already highly endangered and reproduce slowly, population recovery from Ebola outbreaks could take decades or longer. Other animals, including forest antelopes can also die from the virus. The routes of forest animal infection remain unclear, but wild bats are thought to be the likely natural reservoir for the virus, meaning they could carry and transmit the pathogen with little or no signs of illness. Further Ebola-wildlife connections are underscored by the fact that the butchering and consumption of wild animals, especially apes that had died from Ebola, can provide a clear route for entry into human populations. In David Quammen’s book Spillover, the author noted that wildlife deaths in surrounding forests were harbingers of outbreaks in human villages.

From our own experiences studying wildlife-pathogen interactions, including work on great apes in Africa, we think that animal ecology has much to contribute to efforts to predict the spread of Ebola virus and prevent future outbreaks. Here, we touch on three ways animal ecology can inform our understanding of Ebola virus dynamics, including studies of pathogen spread on great ape social networks, research regarding bats as reservoirs for Ebola and other deadly viruses, and new efforts for wildlife surveillance to predict Ebola outbreak risk in humans. We also note that the ongoing Ebola outbreak has dire consequences for efforts to conserve wildlife by curbing ecotourism and potentially increasing hunting pressure on already-imperiled species.

Social network studies and Ebola transmission in apes

Ebola virus transmits through close contact of body fluids, which means that host sociality can determine transmission dynamics within a population. The precise behaviors that transmit Ebola infections in wildlife are unknown, but the highly social nature of great apes could make them particularly vulnerable to outbreaks of Ebola virus and other socially-transmitted pathogens. During a 2003-2004 Ebola outbreak in the Odzala-Kokoua National Park in the Republic of Congo, one study found that gorillas living in social groups were twice as likely to become infected with Ebola as solitary males. Despite this difference, mortality rates across both solitary and social individuals were staggeringly high (77% – 97%). At the end of the outbreak, only 20 of the roughly 360 gorillas remained, underscoring the catastrophic effects of Ebola virus on wild ape demography. An important question is whether Ebola outbreaks impact ape social structure in ways that delay population recovery. A new study in Journal of Animal Ecology indicates that gorilla social structure is remarkably resilient following Ebola outbreaks. The study’s authors found that birth rates, as well as survival and social dynamics for the affected Odzala-Kokoua National Park population have since returned to their pre-Ebola state. However, there’s still a long road ahead. The population remains small and demographic models suggest that gorillas could require over 100 years to fully rebound from an Ebola outbreak.

Incorporating social behavior into infectious disease models can tell us how contagious pathogens are likely to spread throughout a population. A modeling study by Charlie Nunn and colleagues made the realistic assumption that, after a silverback gorilla dies of Ebola, females and juveniles quickly disperse to new groups. This means that Ebola virus might spread faster through populations of gorillas versus chimpanzees, because chimpanzees, which have multi-male multi-female communities, would be less likely to disperse after the death of a single individual. Additionally, social network analysis has been used to make predictions about which animals are likely to acquire an infection and which intervention methods might be most effective for preventing outbreaks. One recent study simulated the spread and control of Ebola virus (among other pathogens) in wild chimpanzee social networks. By comparing random vs. targeted vaccination strategies, Rushmore and colleagues showed that targeting the most connected individuals in a population for vaccination could prevent large outbreaks and substantially reduce the number of individuals requiring vaccination. Similar types of social network analysis could be applied to human outbreak data to assess the role of “superspreaders” in the current human Ebola outbreak, and to establish initial vaccine distribution strategies following the release of a human vaccine. Notably, network approaches have provided crucial insights towards the control of other human infectious diseases, including influenza, SARS and HIV/AIDS.

Bats as reservoirs for Ebola and other lethal pathogens

Ebola virus is one of many zoonotic pathogens to emerge and spread in human populations. Zoonotic diseases are caused by pathogens typically harbored by animals, and include diseases such as H5N1 and H1N1 influenza (originating in birds and swine), rabies (from carnivores and bats), Lyme disease (from white-footed mice) and West Nile fever (amplified by numerous wild bird species). Zoonotic diseases account for well over half of new and emerging diseases affecting humans. These diseases remind us that human activities such as agriculture, mining, forest clearing and bushmeat hunting are bringing people into closer contact with animal pathogens than ever before. How these pathogens shift from animals to humans, and why this seems to be happening more and more in recent years, is a topic of great concern.

Bats are the source for a disproportionate number of emerging zoonotic human infectious diseases, including SARS, Marburg (another filovirus like Ebola), Nipah, Hendra and rabies. A recent comparison of bats and rodents found that even though rodents as a group harbor more zoonotic pathogens than bats, after controlling for life history and ecological differences among species, bats harbored more zoonotic viruses on a per species basis than rodents. One reason for this could be the high level of spatial overlap among bat species, allowing for cross-species transmission of a diversity of pathogens. Other work suggests that owing to their high metabolic rates during flight, bats have a unique immune physiology that involves daily cycling between high and low temperatures (“flight as fever”), forcing the viruses that infect them to become more tolerant to fever responses. Yet another idea is that the high mobility of bats, combined with dense roosting aggregations leads to small world networks that can maximize pathogen transmission and support high viral diversity in wild bat populations.

Importantly, relatively little is known about the natural ecology of viruses in wild bats. There are practical limitations to studying bats: they are nocturnal, spend a great deal of time in flight, and roost in caves or other hidden areas, making them challenging to capture and observe visually. Overcoming these limitations is important, because understanding the mechanisms of pathogen persistence in bat populations, and effects of seasonality and environmental stressors on bat-pathogen transmission could be crucial for predicting human and livestock exposures. Beyond their role as reservoirs of zoonotic pathogens, bats are critically important in natural ecosystems, offering services in the form of pollination, seed dispersal and insect control. Therefore, efforts to minimize pathogen spread through culling bats are not to be encouraged, and in fact, some recent work indicates that culling bats to prevent disease exposures might do more harm than good.

Consequences of the Ebola epidemic for wildlife conservation

The current Ebola outbreak in West Africa is already having negative impacts on wildlife conservation as fear surrounding Ebola turns travelers away from ecotourism activities across Africa. Sadly, this drop-off is widespread – even affecting countries without any Ebola cases and thousands of miles away from the current outbreak. The drastic reduction in tourism dollars will likely result in decreased funds for wildlife conservation, including funds for park staff and ranger salaries. With less on-the-ground protection, many fear that this chain of events will ultimately increase poaching and weaken wildlife protection in regions most impacted by tourism declines.

Food insecurity in Ebola-hit West African countries could also affect West African wildlife. Quarantines and travel restrictions now limit the labour force leading to substantially reduced annual harvests. Border closings have severely decreased trade, threatening food supply and causing food prices to soar. Vincent Martin from FAO told Reuters reporters in a September 2014 news report “In the three countries severely affected by Ebola, the agriculture and food security situation is really deteriorating. People either cannot afford to buy food or it is not accessible anymore.” If the lack of food options translates into increased hunting, the problem could be two-fold. Additional hunting pressure on wildlife would exacerbate an already dire situation for many endangered wildlife species. Even though bushmeat hunting is common in many West African countries, additional reliance on forest animals for food (e.g., bats, primates) could intensify the chances of another zoonotic spillover event from wildlife into people. Thus, Ebola-linked food insecurity presents a clear risk for both conservation and human health, demonstrating the urgent need for campaigns that provide alternative food solutions and educate hunters about the dangers of bushmeat.

Ways moving forward: Ebola research at the animal interface

Animal ecology has much to contribute to future Ebola research. Increased knowledge about the ecology and behavior of natural reservoir species could be key to understanding the dynamics of Ebola transmission and predicting the risk of future outbreaks. Towards this end, several organizations are actively studying bats and other wildlife host species. FAO recently created a job position for a wildlife expert to examine links between wildlife, bush meat and Ebola. The EcoHealth Alliance is leading studies on bat ecology, physiology and immune defense to understand their role in shedding Ebola and other important emerging pathogens. Beyond the reservoirs, wildlife species (e.g., primates, duikers) infected with Ebola can transmit the virus to humans through close contact. Surveying great ape faeces for Ebola virus antibodies offers a unique way to non-invasively determine previous exposure and monitor great ape prevalence rates over time. While Ebola vaccines are not currently used in wild ape populations, a “conservation-oriented vaccine trial” recently showed a virus-like particle vaccine to be safe and immunogenic against Ebola virus in captive apes. Additionally, the Wildlife Conservation Society is working to develop methods for delivering an oral Ebola vaccine to wild great apes.

The current outbreak in West Africa is far from over, and it is clear that more volunteers and more funds are needed to bring the epidemic to a halt. After the outbreak subsides, it would serve us all – humans and wildlife – to keep the momentum going and to focus our energy on Ebola prevention. Wildlife and human outbreaks are tightly connected: not only do primate die-offs in the forest often precede human outbreaks in villages, but human contact with dying primates could provide a direct link for Ebola entry into human populations. Thus, increasing funding at the federal and global levels for research aimed at understanding the natural ecology of Ebola virus, and other zoonotic infectious diseases, will benefit both conservation and public health efforts.

Sonia Altizer
Associate Editor Journal of Animal Ecology
(email: soniaaltizer@gmail.com)

Julie Rushmore, PhD
(email: julierushmore@gmail.com)

* Updated 5/12/14 16:10 GMT

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It is alright to be wrong and was Wright right?

Max Planck famously said ‘science advances one funeral at a time’. Sadly there is still some truth to this: some scientists are incapable or unprepared to change their views despite overwhelming scientific evidence that they are wrong*. Outdated ideas often only die with their advocates. One thing I try to teach students is that it is alright to be wrong: many ideas turn out to be incorrect, lots of exciting hypotheses end up not being supported, and frequent promising avenues turn out to be cul-de-sacs. But that is how science progresses. We need to rule out some competing hypotheses in order to advance knowledge.

Years ago one of my colleagues was embroiled in a heated scientific argument with a collaborator over the interpretation of patterns in data he had published. My collaborator made an interesting point when she recounted the events to me. She felt that, in reality, the prize of winning the argument was small, as few people cared, and the argument had got heated for just that reason. As with any arguments that can be parodied as two bald men fighting over a comb, because the outcome will have little impact beyond the pride of the two protagonists, it can become bitter. But this argument got me thinking. It helps to have an enemy when making an argument, so perhaps the desire to cling to one’s misguided beliefs until death aids younger scientists in delivering a paradigm shift.

Paradigm shift is defined in the Oxford English Dictionary as a ‘conceptual or methodological change in the theory or practice of a particular science or discipline’. Most science, including ecology, advances incrementally rather than through major conceptual shifts. But there have been important breakthroughs in animal ecology in recent times, and most, to my knowledge, have not involved acrimonious debate.

Most of the major advances in ecology and evolution over the past decade or so have been methodological. The ability to assemble genomes is obviously one such exciting and important advance. This really has breathed new life into animal ecology. Some of the research is genomic natural history, with researchers reporting interesting facts about unusual aspects of a species’ genome. For example, it is fascinating that cod lack the MHC II genes, and identifying this surprising absence leads to the obvious, but thrilling, question: why? As we have begun to get a better understanding of the genomic differences between species, populations and individuals, we have begun to shed light onto how different speciation processes generate different genomic signatures. As the cost and ease with which genomes can be identified increases, it is clear that our understanding of the processes underpinning evolution, and the mechanisms that convert them into patterns written in the genome will exponentially increase.

Another remarkable methodological breakthrough is the advent of wearable tech for animals. This has provided important insights into animal behaviour, including detailed information of the routes animals use to migrate, how they use space, and how they interact with one another. In addition, technological advances now allow us to measure heart rate and metabolic rates in free-living animals, as well as accurately determining their diet. Such advances are important from both an ecological and conservation perspective. Clearly understanding how animals behave is useful when planning conservation strategies. From an ecological and evolutionary perspective it is remarkable quite how much variation there is at all levels of biological organization – from between individuals to between populations. Understanding how this variation is generated, maintained and its consequences for ecological and evolutionary dynamics is currently at the heart of animal ecology.

One of my first papers introduced what I thought of as a methodological advance. My coauthors and I developed a statistic we called mean d2 based on the squared difference between microsatellite allele repeat lengths at a locus. We proposed that the measure captured two processes: recent inbreeding as well as mating patterns from deeper in the pedigree. It got widely used, often incorrectly as just a measure of inbreeding. The measure is at best very noisy, and it is quite challenging to interpret what it really captures. Subsequent, much better, measures of inbreeding from marker data have been developed, and I now consider mean d2 as an idea that didn’t quite work. In retrospect, I should have realized issues with the measure when I wrote the papers, and should have devised a more useful metric. So I made a mistake, and am happy to admit it. But hopefully the science didn’t set the field back for more than a couple of minutes.

Inbreeding started featuring in my thoughts again recently (no, I haven’t married a cousin). I have just finished reading Will Provine’s book ‘The ‘Random Genetic Drift’ Fallacy”. In this book he argues that in simplifying population genetics down to a single, neutral locus on a chromosome, Fisher set population genetics on the wrong course. Fisher’s motivation for working with a single locus was to use developments in statistical physics to understand evolution, and some sort of simplification like this was, and still is, absolutely necessary. However, Provine argues that ignoring chromosomes and recombination led to Fisher – and nearly every population geneticist afterwards, including Wright – to confuse random genetic drift and inbreeding. If Provine is right, population genetics theory needs a major overhaul. And a consequence of that might be to revisit Wright’s shifting balance theory that has fallen from favour in recent years. If Provine is right, that really would be a paradigm shift in our field. But I’d be somewhat surprised – I still have a lot of respect for Fisher’s science.

So what happened to my colleague and her protagonist? It turned out she was right. She rose through the ranks, and is now a highly respected epidemiologist. Her meteoritic rise had nothing to do with the spat that she now chuckles about. But her protagonist remained bitter about the whole debacle and didn’t experience the successes my colleague did. For many years he apparently felt that she undermined his greatest scientific achievement, and that this prevented him achieving his true potential. Fortunately time is a great healer and I hear that he rarely mentions her name in anger now. And I suspect no one cares: certainly I can no longer remember what the issue was they were arguing over.

Tim Coulson
Senior Editor, Journal of Animal Ecology
Twitter: @tncoulson

* the urge to mention the government and badger culls is just too strong

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Archive your data!

When you submit a manuscript to the Journal of Animal Ecology you are asked the following question: ‘If your paper is accepted for publication where do you expect to archive your data or, if already archived where are the data held?’ Recently, we received a manuscript where the author had responded to this question with: ‘the data will be archived with the lead author’. This is not an appropriate digital data archive!

On about the same date that the previous was submitted, one of us wrote to the authors of a paper published just over a decade ago. In the email, data underpinning the paper were requested, as it seemed plausible that the paper’s conclusions were a consequence of an error in analysis. The authors were unable to provide the data because they had changed computers several times in the last decade and it had been lost somewhere along the line. This won’t be the only time this has happened. In fact, not so long ago, one of us has had to play the embarrassing role of replying to request a for data with the news that it was in a file format that was inaccessible on any current operating system. Fortunately, these sort of things shouldn’t happen in future for Journal of Animal Ecology papers as one of the reasons we require authors to upload data associated with their papers to a respected data repository is to avoid just such scenarios.

There are advantages of having data associated with a paper freely available other than allowing others to verify results. For example, new methods can be applied to old data to see whether methodological advances substantially alter conclusions, and data can be collated across species to allow new comparative and meta-analyses. There’s an obvious reason why Bumpus’s (1898) famous data on sparrows has been analysed in so many ways to quantify natural selection: because it was accessible. In addition, there is a compelling ethical reason to upload your data: If its collection was funded by the public purse, it should be made available for the public to access.

Both of us frequently work with long-term individual-based data sets. We have helped fund the collection of long-term data, spent time in the field collecting it, and (increasingly it seems…) spent time in the office analyzing it. Both of us have had many debates about data access with those in the community of researchers working with long-term data. And, as with any field, there are both advocates and opponents of data archiving. One frequently aired argument against it is that some unscrupulous bastard will download it, use it to address a question you were planning to address at some point in the future, and steal your intellectual thunder. They might even use inappropriate analyses and arrive at erroneous conclusions. This is a risk, but both of us consider it small, and outweighed by the benefits, and both of us advocate data archiving for all types of ecological and evolutionary data.

Over the past 20 odd years that each of us has been involved with long-term individual-based studies, we have both seen numerous approaches from researchers asking whether they can have access to data. In nearly all cases the request has been granted. Very occasionally a student or post-doc was already testing the same hypothesis as that proposed, using the same methods. In that case, access was denied, but it was also explained that data would be made available for other analyses if desired. It would of course be awful to be gazumped by someone who has downloaded your archived data, but is this sufficient argument not to archive data? We suspect that this would happen rarely, and that the risk is consequently low. It can also be easily addressed by proposing some simple data etiquette: If you are about to launch into an analysis of someone else’s data it would be strongly advisable to approach them and to let them know your plans. If they write back stating that someone else is just about to submit a manuscript on the same topic using that data, then you have potentially spared yourself considerable wasted time. It is also worth pointing out that restricting access to data doesn’t prevent people testing the same idea in other data sets, so the risk of losing out on your pet project isn’t at all prevented by data restrictions.

Another concern that we have heard raised, though not, we hasten to add, by any of our collaborators, is that someone has spent many years collecting data and they’re damned if they’re going to make it available to anyone else to parasitize. The most amusing version of this was from a researcher who told one of us that the reason they were not going to make their data available was they would rather die than let the RSPB have it! The reason had something to do with a dispute with the organization aeons ago. So long ago, in fact, that the data owner was unable to remember any real details about the conflict! If data were collected by funding from the public purse, and the data collector’s salary was paid from the same source at the time, this argument is really indefensible. It benefits science, and future generations of scientists, if you make your data available.

A possible final concern is that the data may be analyzed by people who don’t understand the system and that this might result in dubious insights. We always wondered what metadata were for. If methods sections are sufficiently detailed then it shouldn’t be too hard for major sources of bias in data to be flagged.

Finally, the number of people who really care about your data at this moment in time is probably quite small. Most people have their own data that they are interested in and pursue their own questions in those data. This is particularly true for long-term studies. How do we know this? In 2008 we made available for free download three long-term individual-based studies on birds http://lits.bio.ic.ac.uk:8080/litsproject/. A paper was published to accompany their release (Jones et al. 2008). Andy Village’s kestrel dataset, Ian Patterson’s rook dataset and Ian Newton’s sparrowhawk data set are all freely available. To our knowledge, they have very rarely, if ever, been used.

Neither of us is convinced by the arguments against data archiving. We believe the benefits far outweigh the costs. The British Ecological Society shares this view, and it requires data archiving for all papers published in all its journals. At the Journal of Animal Ecology, the only reason we would waive this requirement were for compelling ethical reasons. So next time you submit to us, the correct thing to write in response to the where will you archive data question is something like ‘the digital data archive, Dryad (http://datadryad.org/)’.

Tim Coulson (twitter: @tncoulson)
Ben Sheldon (twitter: @ben_sheldon_EGI)
(Senior Editors, Journal of Animal Ecology)

References

Bumpus, Hermon C. (1898) Eleventh lecture. The elimination of the unfit as illustrated by the introduced sparrow, Passer domesticus. (A fourth contribution to the study of variation.) Biological Lectures: Woods Hole Marine Biological Laboratory, 209-225.

Jones, O.R. et al. (2008) A web resource for the UK’s long-term individual-based time-series (LITS) data. Journal of Animal Ecology 77, 612–615.

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A Call for Pre-Proposals

This year I have written two UK research council proposals and a European Research Council grant. They are each on completely different topics. I suspect it has taken about six months of my time. I was pleased with each application, but I don’t have high hopes for any of them, simply because funding rates are low. I am not atypical, and this is not an atypical year for me.

What happens at the UK research councils is one receives reviewer comments on the proposal. From my experience, about half of the reviews are positive suggesting funding, and the remaining ones grumble. They rarely raise any scientific objectives that cannot very easily be dealt with. They often criticize the research team, complain that some key literature is missing and request additional methodological details. A colleague of mine once told me that he had had several grants rejected at NERC that were better than everything he had ever been asked to review, and consequently always wrote grumpy reviews. He is a little delusional. Anyway, once reviewer comments are received, a response can be written. The committee assesses all grants, reviewer comments and responses, ranks proposals and the top few get funded.

The funding rate at most research councils is low, and lots of good grants deserving of funding are submitted. So not all good grants get funded. There is an element of luck in which good grants get funded, which may boil down to a committee member being sufficiently enthused by your application to champion it. The only way to guarantee getting any funding from a research council is consequently to submit many good proposals, with chance meaning the odd one will get funded. It is a strategy that many academics follow.

If a research council has a funding rate of 10% then the average researcher would need to write 10 grants to have an odds on chance of one being awarded one. Some will get lucky and get their first submission funded, other might have to write many more than 10. If a good grant takes two months to write and polish, on average nearly two years are required in order to secure a grant that would probably last three years.

There must be a better way. The National Science Foundation in the US has a two-stage policy. First, a short pre-proposal is submitted. Most are rejected. If your pre-proposal is not rejected you are invited to submit a full proposal. If you are invited to submit a full proposal, the odds of success are reasonable – sometimes as high as 50%. I would much rather write a pre-proposal and fail than write a full grant and fail, simply because of the time commitment. I could then spend the time gained to write up papers. Should we encourage the research councils to go down the pre-proposal route?

If they do, I will have more time to write papers. But what should I write a paper on? If I don’t have a grant, I won’t have any new data coming in. At least data that other people collect under research council funding now has to be made available, so there is the opportunity to use these data to address questions. But perhaps that is a question for another blog entry. So maybe I’d write a review on eco-evolutionary dynamics. It must at least two weeks since I’ve seen a new review on this topic.

Tim Coulson
Senior Editor, Journal of Animal Ecology
(twitter: @tncoulson)

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Begging for funding?

Understanding ecological systems takes time. While some experimental ecological work, performed under controlled lab conditions, can be conveniently fitted into the short-term periods beloved of funding bodies, much of ecology requires a longer-term perspective. Why is that? First, life-histories frequently operate at generational scales approaching decades. To have any hope to make sense of patterns of inheritance, selection or demography we need data spanning multiple generations, and that may mean multiple decades. Second, almost all ecological studies reveal heterogeneity among individuals – frequently in terms of vital rates, or detection probability, or other aspects of life-histories. Such heterogeneity makes it very hard to extrapolate from cross-sectional observations to understand the true sources of variation driving a population.

Third, as anyone who has carried out a field study knows, a sample of just a few years can be hopelessly unrepresentative of the overall pattern of variation. To illustrate with a personally relevant example, the last two years of the long-running Wytham great tit population study (which I now oversee) saw a year with one of the latest ever spring breeding seasons (2013), immediately followed by one of the earliest (2014). This pair of years – in an unbroken sequence of 68 years – provide a fascinating contrast, because they enable us to compare how the same individuals respond to markedly differing conditions, but we can only make that comparison informed by the long history of this study.

Finally, and the flip-side of the argument above, is that ecological processes may sometimes be influenced by rare events, or themselves occur rarely. For example, it will usually be hard to perform a study of inbreeding in a wild animal population with only a few years’ data because close inbreeding is rare. But understanding the many demographic causes and selective effects of inbreeding, or the how the evolution of inbreeding avoidance drives patterns of dispersal in populations, requires sufficient of these rare events to draw robust conclusions. Equally, if we want to understand the influence of extreme climatic events, or of sudden human-caused events, we need a long sequence of data for comparison.

No doubt all of these points are familiar to most readers; and indeed they have been made many times, as has the point that long-term studies are disproportionately influential in terms of their contribution to science. So, why make the point again?

I was sparked into action by a colleague’s solution to a threat to the viability of a long-term population study. Tim Birkhead – my former PhD supervisor – has run a long-term study of a seabird, the guillemot Uria aalge, on Skomer, off the West coast of Wales, ever since he began studying the population as a PhD student in the 1970s. Over the 40 years of the study, Tim and colleagues have documented changes in demography as the population has steadily climbed from a population trough1,2, analysed how the population recovers from sudden events3, as well as using the population as the basis of several PhDs on the behaviour and ecology of monogamy in birds (the results from which have featured in several successful books). In global biodiversity terms, one of the few things the UK is really important for is its coastal seabird populations, and there have been worrying signs that, in some parts of the UK, these populations are in a parlous state. Understanding why some populations – like that of the guillemot on Skomer – are doing well is therefore of considerable conservation relevance. Continued monitoring of the guillemot population on Skomer also provides the raw data to track the way the population responds to future hazards and threats, and interpret these in the light of past responses.

All of this scientific utility from this one study is generated by simple, good-old-fashioned field ecology. A few days’ clambering around on the cliffs at mid-summer each year yields a cohort of colour-ringed young guillemots of known age and origin. Several months of patient observation (and reading leg-rings in colonies of tightly packed guillemots surely takes patience!) each spring and summer yields resightings of these birds, from which recruitment and survival rates can be estimated. That description of fieldwork is – in essence – true for the core data that underpins many long-term studies: it is, on the face of it, simple to collect, but generates tremendous value. We shouldn’t confuse the complexity with which data are collected with their utility. What we should appreciate about studies like this is that continuity is vital. A gap of a single year means, not just potentially missing data on annual variation in recruitment and survival rates, but an entire missing cohort of marked birds, for which nothing will ever be known. For a long-lived species like a guillemot, this cohort might make up a relatively small proportion of the population; for shorter-lived species a missing year would be catastrophic in terms of population coverage.

Tim’s guillemot project costs about £12K a year to fund. Small change, really, when the typical research council grant in the UK – running over three years – comes in at something like £500K. For a long time, the project was funded by the Countryside Council for Wales, but, in its new guise as Natural Resources Wales (NRW; what is it with rebranding? I wonder how much that cost anyhow…), it took the decision to axe the study.

And now to the title of this piece: frustrated by NRW’s refusal to revisit the funding decision, Tim has decided to make a foray into crowd-sourcing to generate the funds to keep the study going. This has gone well with the target reached in only a few weeks, with an average donation of just under £20. In some ways this is very encouraging – if you wish to donate, please visit https://www.justgiving.com/timbirkheadguillemots/ – but it also raises many worries about the long-term vitality of such studies. While Tim is to be congratulated for exploring this alternative source of funds, I doubt it is viable for many such cases. Few of us have quite as much drive and charisma as Tim has with which to engage the public, and guillemots on rugged cliffs may also engage the public more than, say, a long-term study of plant ecology. Inevitably, one suspects that the public will only have a limited amount of interest in long-term studies, before compassion fatigue sets in.

“Wait a minute”, you may be saying, “aren’t many long-term studies funded by research council grants? Isn’t that a sign that they are attracting the resources they need? If they produce such good science shouldn’t they be competitive for that sort of funding?” Well, yes, this is true for some of these studies. Famously, one particular long-term study (red deer on Rum) is said to have had 36 years’ consecutive funding from UK research councils, all in the form of three-year grants. However, I think that reliance on standard grant funding as a way to fund the core parts of longitudinal studies creates three different types of perverse incentive, none of which is good for science in the long run. Arguably, this may actually reduce the funding available for other types of ecology.

First, because grants are short-term (relative to long-term studies), the focus on grant assessment is on testing new hypotheses, and these frequently have to be approached using an experimental approach. Experiments may have all sorts of consequences, and could easily undermine the future utility of the long-term data that led to them. Second, I think that part of the reluctance of those running long-term studies to make their data freely available stems from their need to parcel out their ideas about analyses possible in their data sets to different small and short-term grants. The worry about making data open is that others might carry out and publish such analyses and that this would then compromise the ability to secure funding in the future. Finally, the emphasis on novelty in standard grant applications (as opposed to seeing the value of continuity) leads to large and complex grants that emphasise the testing of new ideas, even if those applying for funding might be prepared to accept funding at a lower level to maintain continuity. Indeed, the ‘core’ data collection of long-term studies sometimes represents a byproduct of these larger grants, even if it is this byproduct that may, in the long run, be more valuable. After all, novel ideas frequently fail to generate more than a lot of hot air, but core data on individual-level life histories has a proven utility.

What is the solution to this situation? For some time I have felt that a relatively small investment by UK research councils, or (dare I say it) by some of the larger professional organisations such as the British Ecological Society, might actually be a cost-effective solution. Most long-term studies are – at their hearts – cheap to run. £12K for annual monitoring of guillemots might be towards the low end, but in many cases, I suspect that the annual costs for the core data are of the order of £25-£50K. Most of this goes on paying salaries of field and research assistants. So, allowing for inflation, for an investment of £2M, I suspect that we could fund a dozen or more of the most extensive long-term studies for at least a decade each to collect their core data. At current rates, that’s about four standard grants’ worth, which would on average generate only about a tenth of the same type of data which, if not continuous, might have much less than one tenth the value. Remove the extra costs associated with writing (and refereeing and assessing) multiple grant applications along the way, and the equation looks even better. Such an arrangement could be linked to making the data sets openly accessible, and generate even more return by enabling others to analyse these data. My personal view is that this would be desirable, although this issue is controversial among those who run such studies. Roche and colleagues4 have some interesting suggestions about how to increase buy-in to this activity, and it is an issue to which we’ll return soon in this blog.

I should declare an interest here: I’ve inherited running the long-term studies of tits based at Wytham Woods near Oxford, from which we continuously extract data collected over decades, some of it before I was born. I can’t take any credit for the founding, or the basic design, of that study, but I am keenly aware of both the value of continuity, as well as the pressure to keep the funding flowing.

Of course, funders may ask what the expected outcome of such long-term funding might be, but one of the many lessons learnt from long-term studies is that the uses that we can think of for data now only capture a small part of their subsequent utility. In the 1980s, few would have guessed how important such studies would have been for understanding biotic responses to climate change; in the 1990s, few would have guessed how much genetics would play a role in modern animal ecology, and writing now, it is clear that only a few years ago we underestimated how much we’d be able to make use of very high density phenotypic data from continuous tracking and observations of animals. And this simply illustrates the often-made point that predicting the future utility of science is difficult, if not impossible. In other fields in environmental biology, long-term monitoring is well-established as a recipient of Research Council funding, and indeed played a vital role in the detection of the ozone hole over Antarctica5; it just seems that not all fields have historically had access to such funding.

A substantial part of decisions on funding are made on the basis of the track-record of investigators, and it makes sense to also allow the track-record of study systems to govern funding decisions. After all, if a particular study continues to generate ground-breaking work over decades, even though the PIs running it may have turned over several times, it’s not an especially brave prediction to suggest that it will continue to do so.

Ben Sheldon
Senior Editor, Journal of Animal Ecology
(twitter: @Ben_Sheldon_EGI)

References

  1. Meade, J.C. et al. (2013) The population increase of common guillemots Uria aalge on Skomer Island is explained by intrinsic demographic properties. J Avian Biol. 44, 55-61.
  2. Votier, S.C. et al. (2008) Recruitment and survival of immature seabirds in relation to oil spills and climate variability. Anim. Ecol. 77, 974-983.
  3. Votier, S.C. et al. (2005) Oil pollution and climate have wide-scale impacts on seabird demographics. Ecology Letters 8, 1157-1164.
  4. Roche, D.G. et al. (2014) Trouble-shooting public data archiving: suggestions to increase participation. PLOS Biology 12, e1001779. http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001779
  5. http://planetearth.nerc.ac.uk/features/story.aspx?id=509&cookieConsent=A
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Transparency and Evidence-Based Policy: An Open Letter to Defra from Journal of Animal Ecology

As a scientific journal, we are in the business of independently assessing the rigour of work conducted by the research community, including the methods it uses to collect, analyse and interpret appropriate data. We are therefore well placed to judge the merits of relevant scientific endeavour and to provide constructive feedback. On October 30th 2014, the UK’s Shadow Farming Minister, Huw Irranca-Davies, called for an independent review of the methods being used to assess the outcomes of the ongoing pilot badger culls in England 1. Such a review requires a detailed understanding of the behaviour, dynamics and management of wild animal populations – disciplines that are at the heart of the field of animal ecology. As the UK’s leading animal ecology journal, we hereby offer our services to the Secretary of State to provide an independent assessment of the methods and data collected as part of this year’s badger cull.

Badgers and bovine TB

Bovine tuberculosis (bTB) is a terrible problem for Britain’s cattle farmers, costing an estimated £100m in 2013 alone and resulting in the slaughter of more than 32,000 cattle. Unfortunately, bTB control is hampered by persistent infection in populations of wild badgers, which can transmit infection to cattle 2. The challenges of controlling this disease have been identified repeatedly in this and other British Ecological Society journals 3-6, and these peer-reviewed publications provide some of the evidence-base for making decisions about the potential contribution of badger culling to control bTB.

A programme of pilot badger culls began in 2013, and shortly ministers from the UK Department of Environment, Food and Rural Affairs (Defra) will decide whether to expand badger culling to other bTB-affected parts of England. Their decision will rest partly on the estimated level of reduction in badger numbers achieved by the 2013 and 2014 pilot culls. Evaluating such culling effectiveness is important because killing too few badgers has been found to increase bTB in cattle rather than reduce it 7-8. In line with this scientific evidence, Defra’s policy requires that each annual cull should reduce badger density by at least 70% 9.

As most animal ecologists will know, estimating the density reduction achieved by culling is technically challenging and this is especially true for badgers due to them being nocturnal and burrow-dwelling. On the advice of an Independent Expert Panel (IEP), which included our senior editor Tim Coulson, in 2013 both the numbers of badgers and the proportion culled were estimated using molecular methods to identify individual badgers from hair snagged in barbed wire traps 10. However, in 2014 Defra dispensed with both the IEP and the molecular methods it recommended. Instead, Defra plans to estimate badger density reduction internally, using information from culling companies on their culling effort, and the numbers and locations of badger kills 9. Precise details of the planned methods have not yet been made public.

Why is this important?

The implications of these estimates of culling effectiveness are of great interest to policymakers, farmers, wildlife groups, and the general public. This interest is justified because the density reduction achieved by badger culling determines whether this approach will improve or worsen the prospects for bTB control. Due to a lack of transparency concerning the assessment of the 2014 pilot culls, significant concerns have been raised about the methods being used and their utility in assessing the impact of the pilot culls 11,12.

An offer from the Journal of Animal Ecology

In response to recent calls for an independent review of the methods being used to assess the outcomes of the 2014 pilot badger culls, and in the absence of an IEP, we offer Defra the services of Journal of Animal Ecology editors and reviewers to critically appraise the methods used and their power to determine the success of this year’s cull. Should Defra accept our offer, we would provide a transparent and independent review of the available evidence using our extensive international network of reviewers, comprising scientists with acknowledged expertise in wildlife population monitoring and management, as well as expert statisticians and modellers. The Senior Editors of the Journal would personally handle the reviewing process and draw on their team of highly-skilled Associate Editors and external reviewers. To ensure complete independence and transparency, we would avoid calling on scientists that have previously played a part in the contentious badger culling debate, including Tim Coulson, and all reviewers will be identified. In addition, and in line with Journal policy, all relevant data will be archived in a Data repository, such as Dryad or Figshare, where it will be made securely available to the wider stakeholder community. We look forward to hearing from you.

Professor Ken Wilson
Professor Jean-Michel Gaillard
Professor Ben Sheldon
(Senior Editors, Journal of Animal Ecology)

References

  1. Hansard (2014). Badger Cull. Commons Hansard 30 Oct 2014, Column 382. http://www.publications.parliament.uk/pa/cm201415/cmhansrd/cm141030/debtext/141030-0001.htm
  2. Donnelly, C. A. et al. (2006) Positive and negative effects of widespread badger culling on cattle tuberculosis. Nature 439: 843-846.
  3. Vicente, J. et al. (2007) Social organization and movement influence the incidence of bovine tuberculosis in an undisturbed high-density badger Meles meles population Journal of Animal Ecology 76: 348-360.
  4. Hone, J. & Donnelly, C.A. (2008) Evaluating evidence of association of bovine tuberculosis in cattle and badgers. Journal of Applied Ecology 46: 1660-1666.
  5. Bohm, M. et al. (2008) Dynamic interactions among badgers: implications for sociality and disease transmission. Journal of Animal Ecology 77: 735-745.
  6. Woodroffe, R. et al. (2009) Social group size affects Mycobacterium bovis infection in European badgers (Meles meles). Journal of Animal Ecology 78: 818-827.
  7. Donnelly, C. A. et al. (2003) Impact of localized badger culling on TB incidence in British cattle. Nature 426: 834-837.
  8. Woodroffe, R. et al. (2008) Effects of culling on badger abundance: implications for tuberculosis control. Journal of Zoology 274: 28-37.
  9. Defra (2014). Setting the minimum and maximum numbers for Year 2 of the badger culls: advice to Natural England. (http://www.gov.uk/government/uploads/system/uploads/attachment_data/file/347536/badger-cull-setting-min-max-numbers-2014.pdf )
  10. Independent Expert Panel (2014). Pilot badger culls in Somerset and Gloucestershire – Report by the Independent Expert Panel. (https://www.gov.uk/government/publications/pilot-badger-culls-in-somerset-and-gloucestershire-report-by-the-independent-expert-panel).
  11. Woodroffe, R. (2014) British government on the badger cull: ask scientists for help then ignore them. (https://theconversation.com/british-government-on-the-badger-cull-ask-scientists-for-help-then-ignore-them-31435).
  12. Coulson, T. (2014) Name: UK government. Animal ecology test score: 0. (http://journalofanimalecology.wordpress.com/2014/06/23/name-uk-government-animal-ecology-test-score-0/).
Posted in Uncategorized | 2 Comments

Solving the skewed sex ratio problem in science

In 2003 Milner-Gulland et al. wrote a paper on extreme adult sex ratios in saiga antelope. Males had become so rare in some years that the behavior of the system became dysfunctional and population performance suffered catastrophically. The only other environments where I know of heavily skewed adult sex ratios are university science faculties. Except here the skew is in the other direction, with females being rare. Social scientists have shown that skewed sex ratios in the workplace can negatively impact many performance metrics (e.g. Fenwick and Neal 2001).

Many scientists are rightly concerned by the paucity of women on the faculty of many science departments, and there has been much contemplation on the causes of attrition as more men progress from Ph.D. to post-doc to a faculty position to full professor than women. There are hypotheses proposed to explain this ranging from men being more likely than women to express the traits thought to aid success in academia including self-belief and an ability to brush off criticism, through to a lack of adequate home life provision. However, identification of these causes does not seem to be having much of an effect on reducing the skewed sex ratio. For example, of 43 researchers offered prestigious Royal Society University Research Fellowships this year, 41 were men (see here). I am not entirely surprised by this. Many ‘solutions’ I have heard proposed to address the skewed sex ratio problem seem unlikely to succeed. For example, one popular call is for women’s groups to be set up. No one has ever succeeded in explaining to me how that is supposed to lead to change.

Whatever the proximate reasons for the skewed sex ratio, the possible ultimate solutions are clear. It is demographically obvious how to modify adult sex ratios. You either eradicate any differential mortality rates between the sexes at each age or stage, or you skew the birth sex ratio to ensure the adult sex ratio is close to unity. Clearly I am not going to advocate any mechanisms to actually elevate the mortality rate of male scientists but it is clear how to reduce the loss of women to science at each of the career transitions where attrition occurs. You mandate the appointment of equal numbers of men and women at each level. So the Royal Society would appoint an equal number of male and female URFs, and 50% of faculty positions and full professorships would go to women. I don’t have a strong opinion of how this is done, but suspect a change in the law may be necessary. Sex-specific job calls, or a mandate that a moving window of previous appointments must not stray between 45% and 55% are two possible mechanisms. There will be other possibilities too.

Such an idea will doubtless generate some dissent. What if you don’t end up appointing the best person because it happened to be a female only job call and a fabulous man wanted to apply? If we are serious about addressing the skewed sex ratio problem then this is a cost we may occasionally have to bear. To my mind, it is a lower cost than hearing of another excellent woman leaving science because she couldn’t find a way to progress. Another argument likely to be raised might be what if there are just insufficient women studying for undergraduate degrees in a particular subject? I will assume that when the majority of people start their Ph.D. studies they envisage a career in academia. So start with the sex ratio of applications to study for a Ph.D. and set mandated targets on that sex ratio rather than a sex ratio of unity. Another argument I have heard raised – primarily by men – is that women won’t want to feel they are being advantaged. Given the current skewed sex ratio, men must be being advantaged, and I don’t hear too many men complaining. I imagine women will be able to cope with a level playing field.

I suspect that once a mandated system has been in place for a generation it could be removed and the sex ratio problem would not return. Although we may never fully understand all the reasons that led to the skewed sex ratio problem we experience today, we will at least have cured the ill. And personally I’d rather be rid of the problem while not completely understanding it, than fully understanding it and not having solved it. In the meantime, as well as implementing mandating we should also pursue other initiatives to improve working academic conditions for both men and women.

I am fed up of hearing about the problem of too few women in science coupled with inaction. I am also fed up of listening to solutions I cannot see working. We need to get our house in order, and there is a way of doing this. I’d be interested to hear what is to stop us levelling the playing field so men and women both have an equal chance of progressing through the ranks.

Tim Coulson
Senior Editor, Journal of Animal Ecology
(twitter: @tncoulson)

References

Fenwick, G.D., and Neal, D.J.. “Effect of gender composition on group performance.” Gender, Work & Organization 8.2 (2001): 205-225.

Milner-Gulland, E. J., et al. “Conservation: reproductive collapse in saiga antelope harems.” Nature 422.6928 (2003): 135-135.

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Where have all the insects gone?

armyworm
Recently, we commissioned one of Journal of Animal Ecology‘s most experienced Associate Editors, Simon Leather, to compile a Virtual Issue on his great passion – insects. The journal has published many classic insect ecology papers over the years and Simon does a great job of highlighting some of these as well as many new papers that we hope will go on to become classics themselves. In his preface to the VI, Simon bemoans the fact that back in the 1970s, when he first began subscribing to the journal, there were many more papers on insects than there are now and that the journal has perhaps become vertebrate-centric in recent years.

This got me thinking – is this really true? And if it is, then why do we publish fewer entomological papers now than back then? Are we alone in this trend or is it common across other general ecological journals? And, either way, should we be worried about the taxonomic distribution of our papers?

The data

As a scientist, I’m not a great fan of anecdotes so I wanted some quantitative data to answer these questions. I went to Web of Science and used a key word search to establish how many papers Journal of Animal Ecology published over the last 40 years on insects and other taxonomic groups. For comparison, I did the same for the ESA journal, Ecology. To account for year to year variation in the number of papers published, I simply calculated the percentage of papers in each category. So, what did I find?

The results

Annoyingly, Simon was correct – as usual (Figure 1). Over the last 4 decades, the number of papers JAE published that included ‘insect’ as a key word has roughly halved: in the 1970s, more than 40% of our papers included insects, whereas in the 2010s it averages at around 20%. Other invertebrate taxa (crustaceans, annelids and non-insect arthropods such as spiders) have either remained constant over time or have also declined slightly.

By contrast, the number of vertebrate papers has increased over the same period. For example, the proportion of papers that include mammals has nearly doubled in the last 40 years, from about 14% to 26%; bird papers increased from about 15% to 30% between the 1970s and 1990s, and has since either stabilised or declined slightly; and the number of fish papers has increased from about 7% to 12%. Of course, many of the papers we publish will include multiple taxa, perhaps even whole communities, so we need to interpret these findings with some caution.

 

Post 1_Fig 1

Figure 1. Trends in the number of citations per taxon in Journal of Animal Ecology.

This lead to me to wonder whether this trend is shared by other ecological journals and can therefore be explained by genuine changes among the research community. Perhaps the priorities of funding agencies have changed, such that researchers are increasingly working on charismatic mega-faunae to the detriment of more numerous (and some might say, more interesting!) smaller organisms like insects? Or maybe researchers simply can study vertebrates more easily these days with the increased availability of techniques and tools such as remote sensing and bio-logging, for example.

A comparison with our US counterpart, Ecology, suggests that these taxonomic shifts are not universal (Figure 2), and similar trends are seen for Oikos (data not shown). For none of the 8 taxa I searched for was there a major temporal change in its frequency of occurrence in this journal, though as an aside it is noteworthy that whereas JAE now publishes around twice as many papers on mammals as fish, for Ecology this trend is reversed, so each journal has its own taxonomic biases!

 

Post 1_Fig 2

Figure 2. Trends in the number of citations per taxon in Ecology (data for the period 1978-1990 are excluded due to poor data quality).

Potential explanations for the trends

So, what has brought about the demise in invertebrate studies published in JAE and the upsurge in vertebrate studies?

In his preface to the VI, Simon alludes to potential biases in the senior editors of the journal. Back in the 1970s, the journal editors were often entomologists, whereas latterly they have often been dominated by vertebrate ecologists. However, there has been a fairly frequent turnover of senior editors over this period, and until very recently, the 4 senior editors were evenly split between those that work mostly invertebrates (Mike Boots & Ken Wilson) and those that study vertebrates (Tim Coulson & Graeme Hays).

Based on my own personal experiences as a senior editor, I certainly do not believe there has been any great conspiracy to exclude insects or to promote mammals. Every paper reviewed by JAE is sent to experts in their respective fields and I do not feel that entomologists are any harder on their fellow ecologists than are mammalogists.  Of course, we cannot exclude the possibility that senior editors (or associate editors or reviewers), subconsciously favour taxa close to their hearts at the expense of other taxa.

I suspect, however, that the change is more a reflection of the subject areas that these taxa are the subject of. We probably publish more papers now in the fields of demography, evolutionary ecology, spatial ecology and disease ecology, and these are fields that tend to be dominated by vertebrate systems. These may also appear to be more novel when vertebrate systems are involved and the authors use fancy technological, modelling or statistical tools. So, the challenge for entomologists is to ensure that their studies have sufficient novelty to compete in a highly competitive environment (JAE currently rejects around 85% of the manuscripts we receive). Acceptance rates for insect papers are similar to those for papers on birds and mammals, so the number of entomological papers we publish reflects the number we receive – send us more good papers and we will likely publish more.

Another possibility is that the shortfall of entomology papers in JAE is balanced by an increase in the number of insect papers published in our sister journals, Journal of Applied Ecology – which began in the early 1960s, three decades after JAE was launched – and Functional Ecology – which began in the late 1980s. But, no, a quick look at these two journals suggests that they also publish fewer insect papers now – a decline from ~36% to ~20% over the last 30 years of Applied, and a decline from ~45% to ~30% over the last 20 years in Functional. In Applied, their place has been taken by birds and mammals, and in Functional by birds and fish.

So perhaps this tells us something about British ecologists (or at least ecologists that publish in the British Ecological Society journals)? Arguably, there are relatively fewer insect ecologists in the UK now than there once were, so perhaps this is the cause of entomology’s decline. Or perhaps entomologists are just choosing to publish in more specialist entomological journals where they may better reach their target audience – certainly there has been an increase in the number of specialist entomological journals over this period.

What should we do?

Whatever the reason for the gradual decline in the number of invertebrate studies we publish, should we be worried? And do we need to do something about it?

My feeling is that the apparent slump in insect ecology (in BES journals, at least) is not terminal and there is no need to panic!

For a start, nearly a quarter of all of JAE papers feature insects – comparable to the proportion of papers on both birds and mammals, and a similar proportion to that seen in Ecology. And what about those of us working on earthworms or frogs, I hear you cry, let’s have more annelid and amphibian papers – there are many more of them than birds and mammals! Well, if the number of papers we published on each taxon reflected the number of species on the planet, then for every 1000 insect papers we publish, we should publish just 31 papers on fish, 13 on reptiles & amphibians, 10 on birds, and a miserly 5 papers on mammals! Clearly, this would be ridiculous.

Besides, these things often go in phases – as an example, notice the recent glut of high-profile papers on pollination ecology driven by global concerns over the decline in bee numbers. New advances in molecular ecology, computational biology and remote sensing will likely translate into a fresh wave of exciting invertebrate studies, and we encourage authors to consider Journal of Animal Ecology as a home for these, as well as their (our) more traditional hypothesis-driven insect ecology studies – as always, the key criteria for publication are genuine novelty and broad ecological appeal.

A more important point, perhaps, is that Journal of Animal Ecology focuses on broad ecological themes, principles and concepts, and most of the papers we publish use specific species, taxa or communities as model systems for understanding these. So it shouldn’t really matter how the taxonomic balance of the journal changes as long as the quality of the papers remains high and they help to improve our understanding of general ecological principles. For taxon-specific papers, there are plenty of excellent specialist journals, including one or two edited by our good friend Simon.

The challenge

So, reader, what do you think?

Ken Wilson (Executive Editor, Journal of Animal Ecology)

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Name: UK government. Animal ecology test score: 0

© Andrew Byrne

© Andrew Byrne

Every now and again animal ecology findings make it into the news. Press coverage often focuses on cases where a species is on the edge of extinction, has erupted to plague proportions, or exhibits some quirky behaviour. One of the positive things about such coverage is that the public appreciates that animal ecology is a mature field of study that uses high-tech methods of data collection, cutting-edge statistical methods and mathematically elegant models. But all too often animal ecology stories are little more than a curiosity, chosen to fill the ‘And finally…’ slot. Occasionally animal ecology research influences government policy – something that has happened with the control of tuberculosis (TB) in cattle. However, this particular case is not a good news story – sound animal ecology advice is being ignored by the current UK government. The reason? A cynic might speculate that it is because following best animal ecology practice might lead to conclusions at odds with what the government seems unjustifiably determined to do.

I believe that policy should always be guided by the best possible evidence available. If I am offered policy based on science, or policy based on conjecture, anecdote and innuendo, I will go with the science-based view as long as it is ethical and humane. I suspect that such a position is considered rather extremist by the current, and recent, British administrations, but I consider it defensible.

Everyone I have spoken to on the issue of TB in cattle wants it eradicated. I have not spoken to the Secretary of State for Environment, Food and Rural Affairs about it. This is perhaps a little surprising. I was a member of the Independent Expert Panel (IEP) appointed to assess the efficacy, humaneness and safety of the badger cull by the Secretary of State’s department – Defra. In retrospect, I think the IEP should have had access to the Secretary of State so we could present our findings and discuss them directly with him. He might have found it useful. I won’t agree to serve on such a government committee again without agreed access to the appropriate minister.

So what were the culls about? Previous research in England had convinced the government that a reduction in badger numbers of at least 70% would be sufficient to eradicate TB in cattle. But how best to achieve this? Gassing, trapping or shooting at night? Gassing was not an option since it was banned for being inhumane decades ago. So that left shooting and trapping. If badger numbers could be humanely reduced by 70% by controlled shooting then a workable solution to TB in England would have been found. So two areas were identified – one in Gloucestershire and one in Somerset – and planning for the multi-year pilot culls commenced.

The first job of the IEP was to devise methods to assess efficacy and humaneness. The methods needed to be robust to fraud by anti-cull protesters making the cull look less effective than it was, and by contractors returning badger carcasses shot elsewhere to make the cull look more effective. The IEP came up with the following method to assess effectiveness: hair traps were used to sample the badger population in the pilot areas, with individuals uniquely identified through genotyping. Hair samples were also taken from culled animals and individually identified with the same genotyping methods. The proportion of the original sample among culled animals gives an estimate of the effectiveness of the cull. Robust estimates of population size can also be obtained using our approach. The method does make assumptions, and we devised a suite of statistical analyses to check for biases and to estimate uncertainties. Once the cull was over, and all analyses were conducted, we were able to say with 95% confidence that the culls failed to deliver anywhere near the 70% target. The probability of either cull having achieved the requisite 70% or more reduction in badger numbers are similar to me – a middle-aged, overweight, unfit Brit – being selected to captain the Brazilian football team in the World Cup. Zero. The culls were not effective, and we can say that with strong statistical support based on the analysis of high quality data.

The assessment of humaneness is a little less certain, but was based on survival analysis with censoring of animals that were shot at. There is greater uncertainty around our conclusions of this analysis. However, we were able to conclude that it was highly improbable that the culls met Defra’s humaneness target of no more than 5% of badgers taking more than 5 minutes to die.

The IEP also made several recommendations on improvements to the way the cull is delivered that the government accepted. For example, we made recommendations on the way that contractors are trained.

So that was year 1 of the pilot culls. Year 2 is approaching. Given the success of the animal ecology methods used, presumably the government would continue to use these tried and tested methods? Methods that are hard to cheat. Methods based on mark-recapture analysis, which is arguably the most innovative statistical development in animal ecology in the last 25 years. Surprisingly, not, despite the IEP recommending it. The government has not announced exactly what they are going to do, but they will not use methods that allow the effectiveness of the continuing pilots to be assessed in year 2 in the same way they were assessed in year 1. Any results they do achieve will be incomparable. If one of my undergraduate students made such an elementary mistake in an exam essay they would be heavily marked down. A change of protocol half way through an experiment reveals such a limited understanding of the scientific method that I am tempted to speculate that the government no longer wants to know whether the pilots are effective or humane. They just want to cull badgers, regardless of whether the population or humaneness consequences can be assessed.

In addition to changing the protocols, there is to be no more independent oversight of the ongoing culls. So who will oversee the analysis of data and the interpretation of results? The same folk that have decided to change the protocols half way through the experiment? I’m not a dyed-in-the-wool Bayesian, but this is a case where I think I might be justified in working with a well-informed prior that the conclusions will be unlikely to stand up to scrutiny.

Government agencies are stuffed full of very competent scientists. Presumably the concerns that they must have raised are being wilfully ignored by government. I wonder why? I wonder if the government no longer wants to know the answer to whether their ongoing pilot culls will deliver the required outcome. I wonder if conducting the pilot culls is the easiest way for the government to look as if it is tackling the awful issue of bovine TB, even though a large body of animal ecology has concluded it is unlikely to be the solution in England? I fear we may hear that the second year is a success once it is over. But such a statement would be hollow.

Not all government policy can be based on science. Often ministers need to work out how to carve up funds. There may be no right or wrong answer on how to do this, and the decision may be based on who shouts loudest, or what seems ‘right’ given the minister’s philosophy. But when animal ecology – and more generally science – can inform a policy debate, scientific approaches must be used and scientific conclusions should not be ignored. The government’s decision to ignore best scientific practice has not been justified by the Secretary of State. I’d be surprised if he changes his mind. U-turns are seen as a sign of weakness. But what is incredibly sad about the whole sorry affair is we are missing an opportunity to assess whether the pilot culls that the government implemented can solve the dreadful scourge of bovine TB. The existing evidence strongly suggests that culling is not the solution in England, and that the ongoing culls were on course to add more evidence in support of this view. The government’s recent actions rob us of this evidence. And this means we will be delayed in solving the TB problem, that farmers will continue to carry the cost of this dreadful disease for years to come and that badgers will be culled without justification. The issue is not the badgers moving the goalposts as the Secretary of State famously claimed. It is the government. But why they have moved them to make it so easy to score an own goal in the fight against TB is beyond me.

You can download the IEP report here. If you want animal ecology to be relevant to policy, and not just a curiosity used by the media for a bit of light relief, speak up for it! Writing to your MP about it and being vocal on social media is an easy way to make an impact. If enough ecologists speak up for their field, future governments perform better in the use of animal ecology evidence.

Tim Coulson
Editor, Journal of Animal Ecology
(twitter: @tncoulson)

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