Predation risk and plasticity in vigilance behaviour headline our pick of recent research this week. We continue the predation risk theme with an example of climate-mediated changes in predation risk. We look at an overview of the relationship between ecosystem services and population abundance – it is not as clear-cut as one might think. We also have a fascinating paper about co-evolution of a pathogen and its host species. We end off the peer-reviewed section with a thought-provoking piece – an ecological warning to humankind. This week, as a bonus, we have included two articles from popular literature that cover research topics that could be of interest … the scientific paper is dead; the AMOC is running amok. Pieter Cronje is our featured conservation artist this week, with “Tiger Tragedy”. Sign up below if you would prefer to receive this digest as an email.

1

Cheetahs strategise to deal with cheaters

Cheetahs are sometimes considered the weaklings in their guild, often losing kills (kleptoparasitism) or losing cubs (predation) to larger carnivores like lion and spotted hyaena. A recent study published in Behavioral Ecology and Sociobiology shows how cheetahs in the Serengeti National Park exhibit plasticity in their vigilance and foraging behaviours. Hilborn et al. (2018) draw on a long-term dataset (35 years) and a huge number of observation hours in the field to show how cheetahs balance their predation risk and food intake. Essentially, animals that are at risk of kleptoparasitism but not cub predation (male coalitions and single adult females) reduce vigilance and eat quickly. However, females that have cubs, increase vigilance, delay their own feeding, and spend longer handling the kill – thus allowing these mothers to expend more effort detecting potential predators and allowing their cubs to feed.

DOI: 10.1007/s00265-018-2481-y

Ed: Full disclosure – I know the authors and was privileged to be able to spend some time in the field with them. This is a fascinating ecosystem, and this long-term project has produced some remarkable ecological insights.

2

Finding Nemo and his cousins just became easier … a tale of cascades, multiple symbioses, climate change, and predation risk

One of the fall-outs of climate change is ocean warming, which is some areas is causing mass bleaching of anemones and corals. Corals and anemones depend upon an algal symbiosis, whereby algal symbionts, zooxanthellae, photosynthesise and provide nutrients to the host organism (which may additionally feed on zooplankton). Many corals kept in the dark (so that their zooxanthellae cannot photosynthesise) but kept with a plentiful supply of zooplankton, will begin to die unless the zooxanthellae return to photosynthesis. Increases in ocean temperature are believed to result in the loss of these zooxanthellae.

In Proceedings of the Royal Society B, recently, and in Nature Communications last year, we find a pair of studies looking at the metabolic and physiological costs of this coral and anemone bleaching on its symbiont, the orange-fin anemonefish (Amphiprion chrysopterus). As with other clownfish and anemonefish, this relationship forms part of a service-service mutualism (anemones provide protection to anemonefish from their predators and vice versa) with a possible service-resource component (waste ammonia from the fish may feed the zooxanthellae).

The two papers show firstly that anemonefish exhibit higher stress hormone (cortisol) levels and lower reproductive hormone (ketotestosterone and estradiol) levels during bleaching events. Further, this is linked to a fitness effect, whereby bleaching events are associated with less spawning, lower egg production, and higher egg mortality.

The authors conclude: “Why anemonefish should exhibit a stress response to host bleaching is not known, but may be in response to a perceived increased risk of predation either from the shrinking of the anemone, or a reduced neurotoxicity of venom from bleached anemones. Alternatively their increased conspicuousness might lead to increased harassment from heterospecifics.”

The more recent paper adds a layer of complexity to this issue, by showing that the anemonefish from bleached anemones had higher standard metabolic rates (SMRs) than anemonefish from unbleached anemones, even though both groups did not differ in their activity levels.

Metabolic costs:
DOI: 10.1098/rspb.2018.0282

Stress hormones:
DOI: doi:10.1038/s41467-017-00565-w

Ed: Similar outcomes have been found for other animals that recently, due to climate change, find their perceived predation risk changing. For example, the snowshoe hare may be shifting its geographic range in relation to the snow-pack (see here). The hares in some areas exhibit a seasonal moult to a white winter coat which provides camouflage against the snow background. Populations that cannot adapt quickly enough to changing snowfall patterns in a warming climate might suffer fitness consequences (getting nabbed by predators due to a colour mis-match, e.g. here) or physiological consequences (as seen in the anemonefish above). Some populations of hares have, however, already developed some plastic moult strategies to prevent this mis-match (again here).

3

At your service … for now

It is well established that biodiversity is associated with ecosystem services – certain species and community assemblages provide services (sometime unique to that taxon). However, it isn’t immediately clear how declines in population numbers of those species would affect the provision of the services they provide. The simplest a priori assumption might be that the relationships are both positive and linear. Gaston et al. (2018) provide a good overview of this issue in the journal BioScience. They use birds as an example taxonomic group to show that although population abundance and ecosystem service provision are usually positively related, this is not always true, and the forms of the positive relationships may seldom be linear.

DOI: 10.1093/biosci/biy005

Ed: This paper illustrates an important point – we might assume in many cases that the abundance of a species (or population) is linearly and positively related to the services the species (or population) provides, BUT, that relationship may be non-linear and thus include inflection or tipping points.

4

Some froggin’ good news

Amphibians have generally had a rough time as humans have degraded habitat and polluted air and water with toxins and endocrine disruptors. To make matters worse, many amphibian species have suffered dramatic declines in the last two decades, linked to chytrid fungus epidemics. Batrachochytrium dendrobatidis is the fungal pathogen believed to cause chytridiomycosis in amphibian hosts.

Voyles et al. (2018) recently gave us some good news from Panama where they looked at detection of frog species and pathogen and host attributes nearly 10 years apart. The initial data were collected during outbreaks (epidemic or epizootic events) around 2004. Twelve riparian frog species had either been driven to critically-low population levels or had putatively been extirpated by chytridiomycosis. Ten years later, nine of those species appeared to be recovering, even after a period of no detection during the outbreaks.

Typically, it isn’t a good idea for pathogens to wipe out their hosts because they would get wiped out with them. Thus, diseases typically shift from initial epizootic (epidemic or outbreak) phases where hosts suffer high morbidity and mortality to enzootic (endemic) phases where morbidity and especially mortality are greatly reduced. It is not yet well-established how this transition occurs … through attenuation of the pathogen (i.e. its pathogenicity is reduced) or through improved host defenses or decreased host susceptibility. Voyles et al. (2018) show that in this case, Batrachochytrium dendrobatidis is no less pathogenic now than it was ten years prior at the height of the outbreak in Panama. Instead, some of the amphibian hosts appear to have more effective defenses.

DOI: 10.1126/science.aao4806

Ed: This is a really fascinating study and offers some hope for amphibian assemblages that have been ravaged by chytrid fungus. On the issue of co-evolution of a pathogen and its host, this study provides a great entry point, and opens up so many new questions. It would be great to compare this co-evolving system which has a single pathogen and multiple host species, with a system that has a single pathogen with high host specificity (perhaps just a single host species). In the former system, it may well be the case that multiple host species provide reservoirs for the pathogen – i.e. some insurance against obliterating its host. The latter system of a single host species offers less insurance, and I would suspect that pathogenicity might evolve quicker than host defenses to prevent a catastrophic host population crash. 

5

We need to have a talk …

At the end of 2017 a sizeable portion of the world’s scientific community published a frank warning to humanity (Ripple et al., 2017). This letter had over 15,000 academic signatories from 184 countries. This letter marked the 25th anniversary of the last time such a warning was made – then by more than 1,700 signatories (including most living Nobel laureates in the sciences). Recently, BioScience published some follow-up letters (here, here, and here) and a response from Ripple et al. (2017) (response).

Ripple et al. (2017) summarised broad environmental trends since the previous warning was issued. For the most part those trends have continued unabated, suggesting that, in general, the first warning was not heeded. The only success has been in stabilising the stratospheric ozone layer. They provided 13 potential steps that humanity could take to make the transition to sustainability: 1) prioritising connected, well-funded and well-managed in situ conservation in reserves; 2) halting habitat conversion; 3) restoring habitat on a large scale, particularly forests; 4) re-wilding areas, including re-introducing top predators; 5) enforcing strong policies to prevent poaching, exploitation, and trade of threatened species; 6) reducing humanity’s food waste; 7) promoting dietary shifts to mostly plant-based diets; 8) reducing human fertility rates by increasing access to education and family-planning services; 9) increasing education about, engagement with, and appreciation of nature; 10) redirecting investing and purchasing choices to promote positive environmental change; 11) promoting green technologies and renewable energy production while phasing out reliance on fossil fuel-derived energy; 12) reforming economies to reduce inequality, and to price in environmental externalities; 13) determining and striving for a sustainable long-term human population size.

The follow-up letters briefly address three additional steps to be taken: 14) transitioning economies away from a growth model (the underlying premise is that the finite resources of the planet cannot sustain infinite growth); 15) developing a new global ethic (in which we are part of the biosphere, it is part of us, and morality includes environmental concerns); 16) moving more forcefully as scientists into the realms of policy-making and politics.

And so … the conversation continues …

DOI: 10.1093/biosci/bix125 (2017 letter)
DOI: 10.1093/biosci/biy006 (2018 follow-up – economic growth)
DOI: 10.1093/biosci/biy007 (2018 follow-up – new global ethic)
DOI: 10.1093/biosci/biy008 (2018 follow-up – political power)
DOI: 10.1093/biosci/biy009 (2018 response to all)

Ed: This series of letters is sobering and somewhat depressing. A lot of the recommended steps would appear to be beyond our individual control as they fall into either POLICY or THE MARKET. We should remember though that in most cases, policy and the market are the collective outcomes of a multitude of individual behaviours and decisions (e.g. votes, or purchases). Some of our most effective lobbying may be to lobby the people directly around us – friends, family, colleagues, neighbours – people who at the very least might give us the chance to be heard.

Popular literature

6

Are scientific papers obsolete?

The Atlantic produced an interesting article about scientific papers and how they may be obsolete in the digital age. The article focuses heavily on the idea of creating computational essays instead – digital files that include data, algorithms, traditional text, and interactive components. Two competing models are introduced – a pay-to-play version from Stephen Wolfram, and an open-source alternative, Jupyter.

7

Don’t you dare touch that thermostat

Scientific American discusses the Atlantic Meridional Overturning Circulation (AMOC), which plays a vital role in how heat gets distributed around the planet. Previously, in this digest, we have looked at climate oscillations such as El Niño Southern Oscillation (ENSO), the Indian Ocean Dipole (IOD), and the North Atlantic Oscillation (NAO) (see here). AMOC could have even bigger impacts on humankind, and it appears that there is now evidence that AMOC is undergoing some change – specifically a slowing down of the currents. The links between climate change, melting Arctic ice, resulting changes in water density in the North Atlantic, and ultimately changes to AMOC, all make for grim but important reading.

Conservation Art this week

A new prison uniform … striped, and orange?

The featured conservation artist this week is Pieter Cronje. He is a human rights lawyer with a master’s degree in Human Rights Law, with Environmental Law as one of his subjects. He was born In Oudtshoorn, South Africa. He started drawing and painting when he was in high school. He also studied history of art and spent many hours at the arts faculty of the University of the North West in Potchefstroom while he was doing his military service. As a human rights lawyer he has traveled to many countries which have both serious human rights issues and environmental issues. Environmental issues were always part of his inspiration and are depicted in many of his paintings. Pieter’s contribution to the Virtual Museum has been massive; he has submitted 27,000 records from 22 countries.

If you like what you’ve seen here and want to receive weekly digests via email of recent biodiversity and development research, then go ahead and sign up below. If you know of any recent papers, projects, or issues worth sharing, feel free to get in touch.

Thanks,
Pete Laver
Editor, BDIgest
pnlaver(at)gmail(dot)com

This week, we take a look at a fascinating study on a migratory bird and how the authors teased out potential drivers of population trends. We also see an interesting experimental study about our tendency to redistribute wealth and our capacity for tolerating inequality. Finally, we look at three methods papers – one that tackles pseudoreplication, and two that address remote sensing.

1

Birds of a feather don’t necessarily flock together

In a remarkable study reported (with commentary) in PNAS, we learned this week about “migratory connectivity” – a strong association between geographically-distinct breeding and nonbreeding areas. Kramer et al. (2018) determine the cause of population declines in one distinct breeding population of golden-winged warblers, by bringing together several lines of evidence. They used migratory data (70 individuals with geolocators), long-term (since 1966) citizen science population trend data, and land cover data for nonbreeding sites for two congeners, blue-winged and golden-winged warblers. These species are ecologically similar and migrate between approximately similar regions. This setup provided a good phylogenetic control. The breeding population of golden-winged warblers from the Appalachian Region appears to be in decline, while the other breeding populations of this species and breeding populations of the blue-winged warbler appear relatively stable. The blue-winged warblers exhibit weak migratory connectivity, with somewhat distinct breeding populations mixing in their nonbreeding area. The golden-winged warblers, by contrast, exhibit strong migratory connectivity with distinct breeding populations using distinct nonbreeding areas. The only declining population, from the Appalachian breeding site, was also the only population of either species to over-winter in northern South America, where it appears that habitat degradation (forest loss) may be linked to the population decline.

DOI: 10.1073/pnas.1718985115
With commentary:
DOI: 10.1073/pnas.1802174115

Ed: This study is quite unique in its breadth, depth, and use of phylogenetic controls. Deploying enough geolocators and recapturing 70 of the tagged birds after a year is phenomenal and provided a rich dataset on migratory movements in these two species. Having Breeding Bird Survey data going back to 1966 also provided a clear picture of population trends for both species, which, in turn, represented a neat phylogenetic control.

2

A little bit of Robin Hood doesn’t go enough of the way

Why do we struggle with inequality? Bechtel et al. (2018) try to answer that question using an experimental game played by a large number of German and United States study subjects (nearly 5000, in total). All participants were placed in random “pairings” whereby both participants recieved a “payout”. The pair partners were unknown to each other. The distribution of the winnings were such that the participant won either USD 25 (versus USD 75, i.e. disadvantageous inequality within the pair), USD 50 (versus USD 50, i.e. equality within the pair), or USD 75 (versus USD 25, i.e. advantageous inequality). Each participant was allowed to give to or take from their partner any sum they pleased. In general, participants tried to redistribute the winnings more equitably when they were in either inequality pairing: participants who received USD 25 took money from their USD 75 partners, and USD 75 participants gave money to their USD 25 partners. Even though the difference in winnings in the inequality pairings was USD 50, participants only gave/took USD 10 to/from their partners (on average). This would suggest that people try to apply some redistribution of wealth, but are generally quite comfortable with retaining relatively large inequalities – even when the starting point for both partners in a pair was essentially a luck-based lottery winning.

DOI: 10.1073/pnas.1720457115

Ed: Even though the dollar values in this study were somewhat trivial, this study still gives important insight into human behaviour with regard to tolerance of inequality and redistribution of wealth. Some of the study strengths include a very large sample of participants (who were representative of the adult voting public), and a “survey instrument” that allowed participants to both donate to and take from their partners.

3

Crying fowl over pseudoreplication

Individual variation in physiological responses to stressors, and individual variation in metabolism of circulating stress hormones are both relatively under-appreciated aspects of non-invasive hormone monitoring. Coppes et al. (2018) address this issue in an extensive study of faecal glucocorticoid metabolites in the capercaillie in Germany. The authors modeled (as the “full” model) the variability in the faecal glucocorticoids using several environmental parameters and animal sex (as fixed effects), and controlled for the individual variability using a random effect for animal ID. The authors then compared this model to a “naive” model that assumed each sample was independent and thus allowed for pseudoreplication (treating non-independent samples from the same animal as independent samples). The full and naive models differed in which parameters were considered significant and differed in how much variance was explained.

DOI: 10.1111/1365-2664.13140

Ed: Although treating repeated measures from individuals is an important step in analysis, as the authors highlight, the broader issue that this study exposes, is the problem of pseudoreplication. By removing the random effect for individual ID in the “naive” model, the authors were actually incorrectly increasing the effective sample size by assuming that the multiple samples from a given individual all contained unique information. Naturally, this would change how much variance could be explained by the model, and it could allow additional variables to be selected as significant, simply by inflating the sample size. The important take-home message here might be that researchers need to think clearly about pseudoreplication during study design (incorporating sufficient spatial or temporal separation in sampling to reduce pseudoreplication) and during statistical analysis (for example by using a random effect in a random effects or hierarchical model).

4

Sixth sense

Remote sensing offers the promise of being able to monitor biological populations in areas that are difficult or dangerous to reach, with ease, speed, and costs that might outperform traditional human observers. However, to date, remote sensing has mostly been used successfully when counting large animals across a relatively small spatial scale when the background substrate is relatively homogeneous. As this review in Methods in Ecology and Evolution shows, there are still a number of obstacles to overcome before remote sensing can play a larger role in monitoring biological populations. Some of these obstacles include the cost of high-resolution data, and the ability to automate the organism detection and counting process, which is currently still subject to error.

DOI: 10.1111/2041-210X.12973

Ed: This is a field ripe for further development and improvement, both in counting animal populations and plant populations (not addressed in the review).

5

Drones for clones

As an example of one of the scenarios where remote sensing may prove helpful in counting animal populations, Hodgson et al. (2018) performed rigorous ground-truthing for drone-based remote-sensing of a seabird colony. The authors created replicas of seabirds of known number so that they could compare the accuracy of ground-based counts by human observers with counts based on drone imagery processed manually or with a semi-automated process. The drone-based counts were more accurate than the ground-based counts.

DOI: 10.1111/2041-210X.12974

Ed: This study demonstrates an important aspect to any remote sensing study – the need for rigorous ground-truthing. The drone method appeared to work well in this contrived example, but, it should be noted that the background substrate – beach sand – was homogeneous and the replica birds on nests represented large detection targets. If a drone-based count is going to work for any animal population – this would probably be it.

Every dog has its … picture painted

This week’s conservation art profile:

Depicting 4454 wild dogs all individually hand painted. Caitlin O’Gorman’s representation of what is left in the wild. Oil on canvas. 2m x 1.8m

Caitlin grew up mostly in Ireland, and completed her final years of schooling in KwaZulu-Natal. She has sketched and painted for as long as she can remember. Our lives are full of accidental stories which take us in unexpected directions. One of the happiest accidents in Caitlin’s life was discovering the Michaelis School of Fine Art at the University of Cape Town. In 2018, she is in her fourth and final year as an undergraduate, and a key component of the year is a display of what drives and inspires the people in her class. For Caitlin it is conservation and therefore, she plans to work in collaboration with the Landmark Foundation to discover the inspiration for her project. Watch this space.

From Caitlin:

I am a fine art student currently in my fourth and final year of studying. I have always had a strong passion for wildlife and my art has resulted in always taking the shape of that subjectivity. In my practice in recent years, I attempt to convey to the viewers the emotions that I feel about wildlife and it’s current state. Although there is a lot of good happening with wildlife conservation, there is dramatic negative activity happening and I attempt to portray this human-wildlife co-existence in a way that challenges the viewer and engages them with a more emotive and connected response. As a visual representation of statistical information, I hope to allow the viewer to truly see the stats rather than read, and in turn to draw the viewer in to empathize with the subject.

If you like what you’ve seen here and want to receive weekly digests via email of recent biodiversity and development research, then go ahead and sign up below. If you know of any recent papers, projects, or issues worth sharing, feel free to get in touch.

Thanks,
Pete Laver
Editor, BDIgest
pnlaver(at)gmail(dot)com