ZooChat Journal Club

Given the volume of news reported on this site, I've long wondered why ZooChatters don't tend to debate or even recognize advances in zoo research. This "Journal Club" is my attempt to remedy that: a thread dedicated to discussing papers members find important, relevant, or just plain interesting.

As a general guideline, I think we should stick to papers recently published by peer-reviewed journals, eg. Zoo Biology, Conservation Biology and the Journal of Applied Animal Welfare Science. Given the interdisciplinary nature of zoo research, I won't dictate a field of discussion, but we could possibly split different topics into different threads down the line.

Below are brief overviews of some recent research that might generate discussion. Links are provided to the first two papers, which are freely available, but the rest require login/payment. There's not much I can do about that unfortunately, but all the abstracts are online (check Google Scholar). If anyone wants more info on a paper they can't access, feel free to drop me a PM.

Finally, if any ZooChatters want to support zoo-based science, this is a list of projects looking for crowdfunding: Experiment.


Zoo Biology (vol. 35, no. 5):

1) "Husbandry and enclosure influences on penguin behavior and conservation breeding", Marshall et al. [https://www.researchgate.net/profil...n_breeding/links/57a4484908ae3f4529291702.pdf]
More evidence that size matters from this multi-zoo comparison, which identified correlates of good welfare and breeding success in Humboldt penguins. Breeding success was influenced by social factors (group size and age), but pool-use (a proxy for health and natural behaviour) was significantly predicted by land area and enclosure size. A relationship between pool-use and pool area per penguin was described as near-significant (p=0.085*). These trends did not level off, suggesting that none of the five zoos provided large enough enclosures and minimum standards should be raised. A couple of similar papers were recently published in the Journal of Zoo and Aquarium Research [The effect of the zoo setting on the behavioural diversity of captive gentoo penguins and the implications for their educational potential | Collins | Journal of Zoo and Aquarium Research, King Penguins in Zoos: Relating Breeding Success to Husbandry Practices | Schweizer | Journal of Zoo and Aquarium Research].

2) "Hair plucking, stress, and urinary cortisol among captive bonobos (Pan paniscus)", Brand et al. [https://www.researchgate.net/profil...n_paniscus/links/57bcb8e808aedf5f75eaa54b.pdf]
The first study to investigate the relationship between hair-plucking (suggested to be stress-induced) and cortisol (a hormone involved in the stress response) in a great ape. This is important, because most research uses either behavioural or physiological stress indicators, rather than testing whether both give congruent results. In this case, a significant positive correlation was observed between cortisol levels and hair-plucking in female, but not male, bonobos at the Columbus Zoo (n=13**).

3) "Plumage variation and social partner choice in the greater flamingo (Phoenicopterus roseus)", Freeman et al.
Interesting correlations identified between colouration and social relationships in greater flamingos at Disney's Animal Kingdom. Males with a preferred social partner were redder than males without, and there was evidence for assortative pairing based on plumage colour. Some important research being carried out on flamingos at the moment. Watch this space.


Journal of Applied Animal Welfare Science (vol. 19, no. 4):

4) "Environmental enrichment effect on fecal glucocorticoid metabolites and captive maned wolf (Chrysocyon brachyurus) behavior", Martín et al.
Examined the effect of different types of enrichment (intraspecific, interspecific, and foraging) on maned wolves at the Belo Horizonte Zoo, Brazil. This study also used both physiological and behavioural stress indicators, but only three wolves were included and no consistent patterns were identified.

5) "Environmental enrichments for a group of captive macaws: low interaction does not mean low behavioral changes", Reimer et al.
Study assessing how different enrichments influenced the behaviour of 16 macaws (14 Ara ararauna, two A. macao) at the Bosque dos Jequitibás Zoo in Brazil. Enrichments the macaws interacted with least resulted in as many behavioural changes as those they reacted with most, suggesting low interaction doesn't mean an enrichment has failed.


Applied Animal Behaviour Science (vol. 184):

6) "A comparison of nocturnal primate behavior in exhibits illuminated with red and blue light", Fuller et al.
A must-read for anyone with an opinion on nocturnal houses and the welfare implications of indoor-only exhibits. Nocturnal strepsirrhines kept under blue light during the dark phase (often used to create a "moonlit" effect) spent less time active than those under red light. Levels of melatonin (a hormone that controls sleep-wake cycles) were also significantly lower for an aye-aye in the blue condition. The authors therefore concluded red (and possibly also white) light is better for animal welfare.


Visitor Studies (vol. 19, no. 2):

7) "Visitors' perceptions of the conservation education role of zoos and aquariums: implications for the provision of learning experiences", Ballantyne & Packer.
Some fascinating insights into the average zoo visitor from this questionnaire-based study, carried out at 13 zoos/aquariums in four countries. Spending time with friends and family was the primary impetus for most visits, but education was the second highest priority. Visitor satisfaction was shaped most strongly by animal welfare concerns, in particular seeing animals that were well cared for and exhibited naturalistically. In terms of the role of zoos, 76% of respondents believed conservation education should be at least as important as providing a fun day out, whilst 81% thought it was at least as important as exhibiting rare, endangered, or exotic animals. Interestingly, 79% of visitors attended zoos at least once a year. These are just a few highlights; I'd recommend any ZooChatter who can to read the paper in its entirety.



*P-values are a measure of statistical significance, with smaller values indicating more significant results. They describe the probability of obtaining a result equal to, or more extreme than, your observed result if the effect you’re testing for is not present. In other words, they're the likelihood of getting a false positive, so a p-value of 0.085 means a false positive would be expected in 8.5% of cases. By convention, p-values <0.05 (false positives expected in <5% of cases) are considered statistically significant, hence the authors described p=0.085 as "near-significant".***

**N is the sample size. In this case, n=13 means 13 chimps were included in the study. In general, larger sample sizes are better, but what constitutes an adequate sample size (and, indeed, a sample) is context-dependent. This is particularly relevant to zoo research, where there are often practical constraints on sample size and, from an ethics perspective, one of the “3Rs” is Reduction.***

***No patronization intended!

 

I'm planning to update this thread within the next month or so, but until then here's an open-access paper on meerkat welfare. Three variables – smaller group size, smaller enclosure size, and greater visitor exposure – were associated with higher stress levels, measured using faecal glucocorticoid metabolites (glucocorticoids are hormones released as part of the stress response). Oddly, the authors don't mention a previous study on the visitor effect in meerkats (Sherwen et al. 2014), which used behavioural welfare indicators and found no effect.

Group size and visitor numbers predict faecal glucocorticoid concentrations in zoo meerkats | Open Science

For the less inclined, there's also a newspaper article outlining the research. I have to say, I think the responses from the zoo professionals here are appalling (as quoted, at any rate).

Simples: how zoos can help stressed meerkats

 

Annoyingly I can't read all of the news article without subscribing; but the results are interesting. Visitor pressure and more room to move and hide make perfect sense to me and are, I suspect, staple results in many species kept in captivity. Even domestic species which undergo heavy human interaction can show increased stress.

The group size was interesting in how more meerkats (up to a point) actually lowered the stress levels. But again its not surprise when you think about it as they are a pack species with a group mentality.


I can't read the keeper comments and the newspaper might have cherrypicked; that said its also not abnormal that a species which has generally bred and survived well in captivity would get some push back from keepers when their method/standard enclosures are brought up in a negative light (esp if earlier research showed no or less stress).

 

There is a large and growing body of evidence that visitors negatively impact animal welfare in zoos, although studies tend to be poorly designed and taxonomically biased. For reviews, see:

1) Hosey, G. R. (2000). Zoo animals and their human audiences: What is the visitor effect?. Animal Welfare, 9(4), 343-358.

2) Davey, G. (2007). Visitors' effects on the welfare of animals in the zoo: A review. Journal of Applied Animal Welfare Science, 10(2), 169-183.

3) Fernandez, E. J., Tamborski, M. A., Pickens, S. R., & Timberlake, W. (2009). Animal–visitor interactions in the modern zoo: Conflicts and interventions. Applied Animal Behaviour Science, 120(1), 1-8.

Absolutely. If I recall correctly, six is the magic number for meerkats; wild groups of <6 are unlikely to survive.

Here is the relevant part of the article:

Amy Plowman, director of conservation at Paignton Zoo, said: “Physiological stress is part of being an animal and not to be confused with distress. Often it’s not feasible to keep bigger groups because if individuals don’t get on this causes more stress.”

Benjamin Mee, chief executive of Dartmoor Zoo, said: “They get very stressed when they’re on their own. They need to be in a group of at least two.”

 

I can see the line between stress and distress being a massive sticking point of debate and also something that could be very hard to determine the difference between with regard to animals. At least when one is talking about build up of stress and more modest levels - the extreme ends are often easy to identify for those used to working with animals, but by that point much of the damage is done and recovery is much harder.

 

I would argue that the difference between stress (which can be positive, neutral or negative) and distress (which is necessarily negative) is largely temporal. Given that distress is generally defined as chronic stress and this was a longitudinal study carried out over a long period, I consider the distinction deeply misleading (again, as quoted).

Perhaps, but Dartmoor's exhibit couldn't hold (m)any more than two.

 

I saw this paper recently and thought it would be of interest - American minks kept in sterile exhibits with less enrichment mate less than those that are given an enriching enclosure. Interestingly, housing conditions did not seem to affect the fertility or willingness to mate by the female mink.

Environmentally Enriched Male Mink Gain More Copulations than Stereotypic, Barren-Reared Competitors

 

I saw this very interesting piece of research about visitor reactions to carcass feeding in three carnivorous mammals (Tasmanian devil, spotted hyena and African painted dog) at ABQ BioPark Zoo in Albuquerque. The response was very positive - visitors stay longer at the exhibit when a carcass is present, report feeling comfortable and at ease when watching a carcass feeding and also exhibit positive attitudes toward animal care and welfare when watching such feedings.

The actual paper seems to be only available behind a paywall, but it is available in thesis format from before it was actually published:
https://digital.lib.washington.edu/...19/Roth_washington_0250O_14597.pdf?sequence=1

 

I and other ZooChatters have often raised concerns about hippo welfare in zoos. This paper, based on a survey of American holders, basically argues the same: that husbandry, facility design, and research need to catch up with welfare standards established for other megafauna. Hopefully it spurs the industry to improve.

https://www.sciencedirect.com/science/article/pii/S0376635717303340

 

Thanks Giant Panda! Before reading the survey I never realised the welfare issues that result from locking hippos in their holding pens at night.

 

A review of research output in AZA zoos. I think the journal standard comes through, unfortunately - there was no evidence publications are an effective proxy for conservation and I would've liked more systematic recommendations for improvements. Still, it's worth a read.

EDIT: Link didn't work, so here's a citation:

Loh, T. L., Larson, E. R., David, S. R., de Souza, L. S., Gericke, R., Gryzbek, M., ... & Knapp, C. R. (2018). Quantifying the contribution of zoos and aquariums to peer-reviewed scientific research. FACETS, 3(1), 287-299.

 

A new comparative analysis has been published on carnivore welfare in zoos, with data collected at the San Diego Zoo and the Safari Park. Commonly used in evolutionary biology, comparative analyses identify correlations between different variables. In this study, "Results suggested that generalist species have higher behavioral diversity and offspring production in zoos compared with their specialist counterparts. In addition, increased minimum distance from the public decreased pacing and increased offspring production, while increased maximum distance from the public and large enclosure size decreased infant mortality." Previous comparative analyses have reported similar results. Obviously correlation doesn't necessarily mean causation, but I've long argued that this is an underused tool in zoo research.

https://www.tandfonline.com/doi/abs/10.1080/10888705.2018.1455582

Miller, L. J., Ivy, J. A., Vicino, G. A., & Schork, I. G. (2018). Impacts of natural history and exhibit factors on carnivore welfare. Journal of Applied Animal Welfare Science, 1-9.


Here are some previous multi-species comparative analyses which focused on zoo animal welfare:

Clubb, R., & Mason, G. (2003). Animal welfare: captivity effects on wide-ranging carnivores. Nature, 425(6957), 473-474.

Clubb, R., & Mason, G. J. (2007). Natural behavioural biology as a risk factor in carnivore welfare: How analysing species differences could help zoos improve enclosures. Applied Animal Behaviour Science, 102(3), 303-328.

Kroshko, J., Clubb, R., Harper, L., Mellor, E., Moehrenschlager, A., & Mason, G. (2016). Stereotypic route tracing in captive Carnivora is predicted by species-typical home range sizes and hunting styles. Animal Behaviour, 117, 197-209.

Müller, D. W., Lackey, L. B., Streich, W. J., Fickel, J., Hatt, J. M., & Clauss, M. (2010). Mating system, feeding type and ex situ conservation effort determine life expectancy in captive ruminants. Proceedings of the Royal Society of London B: Biological Sciences, rspb20102275.

Pomerantz, O., Meiri, S., & Terkel, J. (2013). Socio-ecological factors correlate with levels of stereotypic behavior in zoo-housed primates. Behavioural Processes, 98, 85-91.

 

It's almost as if Howletts know what they are doing

 

Researchers from the Clinic for Zoo Animals, Exotic Pets and Wildlife at the University of Zurich have evaluated the data from 150,000 births of 100 different species of carnivore mammal kept in zoos and have found that, for 80% of the species, the births in captivity occurred at the same time as the wild breeding season. Previously it had been unknown whether birthing seasonality remained the same in zoos because of year-round food abundance and heated indoor quarters but it seems that, by and large, it is a fixed characteristic of these animals.

The carnivores with the strongest seasonality were the red wolf, European mink, yellow-throated marten, wolverine, red panda and Canadian lynx, which all had very precise optimum breeding times. The jaguar, spotted hyaena and bush dog, by contrast, bred at any time of year. The study showed a clear link between the species' native range and their breeding behaviour - the further from the equator the carnivore lived, the more seasonal its reproduction. The only exception to this was the sea otter which breeds year-round despite its temperate/sub-polar habitat; this is likely because its natural food supply is available year-round.

An article about the findings of the study is included below:
UZH - Raubtiere im Zoo gebären zur gleichen Jahreszeit wie in der Natur

This is the abstract for the paper, although I cannot find the full paper publicly available anywhere:
http://journals.sagepub.com/doi/abs/10.1177/0748730418773620

 

This research is from last year, but I haven't seen it before and thought it might be of interest considering the discussion it has generated from elsewhere on the forum.

Aardvarks are often kept in small indoor-only enclosures despite their size and roaming distances (in part because they are perceived as thermophilic - needing high temperatures to thrive); this leads to a tendency towards obesity and compromised welfare. Despite his, wild aardvarks may be active outside their burrows at temperatures of 2 degrees Celsius and this suggests there may be wild aardvark populations suited for outdoor keeping under European climatic conditions. By computing climate matches between source areas in Africa and target areas in Europe the researchers found that the Free State, a province in South Africa, had the best climate similarity. The scientists recommend the import of animals from these parts of Africa to be kept in outdoor enclosures for the animal's welfare.

A PDF of the article is included below:
https://www.researchgate.net/profil...-Zoological-Gardens-in-the-European-Union.pdf

 

The journal Animals is publishing a special issue on zoo animal welfare. All the papers are open-access.

Animals

 

I just found this piece of research from last year; I think it is interesting and relevant enough to warrant posting here, considering its importance to conservation.

Research done at Chester Zoo, the Mitsinjo Association Captive Breeding Centre in Madagascar and Mangabe (a wild site in Madagascar) on golden mantellas Mantella aurantiaca found that the calls of Chester's frogs were statistically different from either the wild or Madagascan captive population (which has been in captivity for only one generation). The frogs at Chester Zoo reacted strongly only to calls from within Chester's own population, while the wild frogs had a similar reaction to calls independent of their source. This could have a negative effect on any future reintroduction projects, as it could result in the released frogs mating exclusively among themselves and lead to two genetically separated populations.

The paper does suggest that pre-release training associated with a soft release programme could help reshape the calls of captive animals to increase their chances of breeding in the wild.

The full paper is included below:
Neglecting the call of the wild: Captive frogs like the sound of their own voice

 

Some recent research from Slimbridge WWT has found that flamingos change their enclosure usage and behaviour during the night - the flamingos had higher rates of foraging at certain points during the night and had a more even enclosure usage when compared to daylight hours. The findings suggest that flamingos use different water depths at different times of day. Flamingos increased nocturnal foraging in their pool during the breeding season.

The research found that the enclosure for these flamingos (the 270-strong flock of greater flamingos) is large enough and has enough variation in land and water areas that the flamingos can follow daily activity patterns similar to wild birds.
The differences in enclosure use between night and day should be considered when designing enclosures for these birds.

The abstract for this research paper is included below:
https://onlinelibrary.wiley.com/doi/abs/10.1002/zoo.21440

 

The Journal of Applied Animal Welfare Science has published selected papers from the Fourth Global Animal Welfare Congress (May 2017), held by WAZA and Detroit Zoo's Center for Zoo and Aquarium Animal Welfare and Ethics. Once again, I find myself in near-total agreement with Kagan et al. ('What Is the Future for Zoos and Aquariums?'). For anyone after a general intro, 'Advances in Applied Zoo Animal Welfare Science' is also recommended.

https://www.tandfonline.com/toc/haaw20/21/sup1?nav=tocList