BDIgest Saturday, 14 April 2018

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.



Cheetah with a hare kill. Photo credit: Pete Laver 2003 (CC BY-NC-SA 2.0)

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.

Lead author, Anne Hilborn, in the field. Photo credit: Pete Laver 2003 (CC BY-NC-SA 2.0)
Authors, Anne Hilborn and Marcella Kelly. Photo credit: Pete Laver 2003 (CC BY-NC-SA 2.0)
After pushing the field vehicle out for the umpteenth time. Photo credit: Pete Laver 2003 (CC BY-NC-SA 2.0)
Cheetah mother with cubs. Photo credit: Pete Laver 2003 (CC BY-NC-SA 2.0)
Kleptoparasitism. Photo credit: Pete Laver 2003 (CC BY-NC-SA 2.0)
Kleptoparasitism writ large. Photo credit: Pete Laver 2003 (CC BY-NC-SA 2.0)
Food coma. Photo credit: Pete Laver 2003 (CC BY-NC-SA 2.0)
Photo credit: Pete Laver 2003 (CC BY-NC-SA 2.0)





Orange-fin anemonefish (Amphiprion chrysopterus). Public domain: US National Park Service.

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).





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.





Variable harlequin frog (Atelopus varius). Photo credit: Brian Gratwicke (CC BY 2.0)

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. 





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



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.





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.

“Tiger tragedy” 2017 by Pieter Cronje. Oil on stretched canvas, 46 cm x 46 cm
“Tiger tragedy” 2017. Oil on stretched canvas, 46 cm x 46 cm.
Pieter says: “During 2017, I had the opportunity to train police in Punjab, India, on how to respond to violence against women. The police invited me to visit a nature reserve (Tiger Reserve) in what they refer to as Kipling country. This is the area of India which inspired the English author Rudyard Kipling to write the Jungle Book. They originally took me to a zoo to see tigers which really saddened and frustrated me. After some discussion they agreed to take me to see the real thing. After one night on the train I was fortunate to see three tigers in the wild. Unfortunately, most of the tigers nowadays are in cages. This picture shows the fear and majesty of the tiger kept in a broken cage. Sadly, this is a highly threatened species in high demand from Chinese traditional healers for tiger bones. They also use the skins for a dancing ceremony in Tibet, although the Dalai Lama requested the local Tibetan people not to use tiger skins. The tradition was taken over by the Chinese staying in Tibet as a sign of power and wealth. Also represented is the Emperor of India Butterfly, also known as Kaiser-I-Hind, Teinopalpus imperialis, is also a highly endangered species due to habitat destruction and butterfly collectors.”
Pieter says: “As a human rights lawyer, I also always challenge people about the destruction of the earth and the decline of species and what they can do about it. I work with law enforcement agencies all over the world and focus on human rights related issues such as human trafficking and domestic violence; but I also talk about the environment to my learners and this is always an important part of every workshop to law enforcement officials. For the past few years my paintings have become a social commentary after my visits to some of these places.”
Have a look at a selection of Pieter’s paintings by visiting





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Pete Laver
Editor, BDIgest





Biodiversity and Development Institute