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  • Writer's pictureAndrew MacIntosh

Expanding Zooentropy

The first official international invitee of the Zooentropy project was Dr. Lance Miller, VP of Conservation Science and Animal Welfare Research at the Chicago Zoological Society (Brookfield Zoo).


Animal Welfare Scientist Dr. Lance Miller crouching next to a kangaroo at Chicago's Brookfield Zoo
Dr. Lance Miller with kangaroo at Brookfield Zoo in Chicago

I originally came to know of Miller through his published work on behavioral diversity. More in that in a moment.


I spent the week that turned February into March with Miller, in Kyoto and my hometown of Inuyama. I already shared a post promoting the event we held at Kyoto City Zoo on zoo animal welfare science in the US and Japan, organized by my good friend and colleague Dr. Yumi Yamanashi at Kyoto City Zoo.


That event, by the way, was excellent. We were at capacity with 30 on site participants and 280 online. The event was consecutively interpreted between English and Japanese, so there was a certain pace that inevitably led to a lot of unanswered audience questions (sorry!). But the ability for the speakers to reach participants in two languages was well worth it.

As an aside, the quality of interpretation was outstanding. We had Kimiko Woo interpret the invited talks. She is a professional interpreter provided by the Interpretation Service group at Japan Convention Services, Inc. Amazingly, Kyoto University Wildlife Research Center doctoral candidate Annegret Naito-Leiderbach interpreted the Q&A and ensuing discussion. And nailed it! Wow.


Animal Rights versus Animal Welfare Science


In his talk, Miller gave some insight into how animal welfare works at zoos in the US, and the role that bodies such as the AZA (Association of Zoos and Aquariums) play. He began with a timely distinction between animal rights and animal ethics.

Rights are a matter of philosophy. Miller noted that one might fall on a continuum, where folks at one end argue that no animal should be held captive for any reason and those on the other end have zero issue with it. He figures that people who work at zoos fall somewhere in the middle.

If I might riff on this a little bit. I think it’s also possible to binarize this argument to some degree with the fundamental question of whether or not you think it’s ethical for humans to keep animals in places like zoos. Then again, maybe your answer to that question is, “it depends”. I won’t comment too much on this here, but know that there is a growing number of people who are at least uncomfortable with the idea of animals as entertainment.


We can, of course, go back and forth on whether zoos are strictly entertainment focused, or whether they achieve their other stated missions of conducting scientific research, educating the public about biodiversity and the challenges it faces in our modern world, and directing resources toward conservation of endangered species. But I’ll save that for another time. One thing is for certain: zoos are far from the worst offenders when it comes to treating their animals with dignity.


There’s an interesting movement called the Nonhuman Rights Project that is aiming to litigate in the US on behalf of some nonhuman animals, like apes and elephants, particularly those living in what for a human we might call heinously unethical conditions.


The documentary “Unlocking the Cage” by Chris Hegedus and D A Pennebaker follows American lawyer and author Steven M. Wise and his team in their case to get some ex-biomedical and ex-entertainment chimpanzees rights under the state of New York law.


Poster from Hegedus and Pennebaker's documentary "Unlocking the Cage" showing a pensive-looking chimpanzee depicted in a courtroom
Poster from Hegedus and Pennebaker's documentary "Unlocking the Cage"

Now, they’re taking on California in an effort to grant rights to an elephant named “Mabu”, after a failed attempt to do the same in New York for the ironically named elephant, “Happy”.

That’s deviating from the point somewhat, but it’s important to keep in mind that people may have vastly different views on the issue of animal rights, what they might be, and whether or not animals deserve them.

To guide us back into the distinction between animal rights and animal welfare, it might be useful to note that some of the earlier thinking about how to provide animals with quality welfare rested on what were called ‘the five freedoms of animal welfare’. These included an animal’s freedom from hunger and thirst, freedom from pain, injury or disease, freedom from discomfort, freedom from fear and distress, and freedom to express naturalistic behavior.


The five freedoms were originally drafted to support livestock husbandry in the 1960’s, and were formalized in 1979 by the Farm Animal Welfare Council.


While still influential, the five freedoms are not what we might call exhaustive guidelines for how best to care for the animals in our facilities. Miller was among the welfare scientists to come up with an alternative set of guiding principles, which they termed ‘the five opportunities to thrive’.


I’ve pasted the full version of them at the bottom of this post, because I think they are a great take away from this post, but for now, let’s just say that instead of focusing on what shouldn’t be taken away from animals in our care the five opportunities to thrive focus on creating environments in which animals can flourish well beyond some minimal standards of care elicited by the five freedoms.

Now, we can aim to measure the extent of flourishing in zoo animals, and that gets us to the key distinction between animal welfare and animal rights: animal welfare is an applied science, and given the right tools, welfare can be objectively measured. Miller highlighted health, physiology and behavior as cornerstones of animal welfare assessment, but in fact there are other ways to think about and measure welfare as well.


The key point is that different markers can be used to help us place individual animals along a welfare gradient, from poor to excellent welfare. With enough data, benchmarks can be determined to ensure that all animals at places like zoos reach a sufficient level of welfare.

As an example, Miller introduced the Cetacean Welfare Study, a multi-institutional initiative he was leading to assess the welfare of cetaceans at accredited zoos and aquariums in the US. The scale of that project is quite incredible and, according to Miller, unprecedented.


Miller and his colleagues published a series of articles from this work as a special section in the journal PLoS ONE, which is open access so anyone can read their results free of cost. The overarching goal of this work was to provide the aforementioned benchmarks so that any institution housing cetaceans can assess the welfare of their own animals using these criteria.

Behavioral Diversity for Animal Welfare Assessment


And just to return to something a little more specific, although he didn’t spend much time on it during the zoo event, Miller’s work on behavioral diversity as a tool to assess animal welfare is one of the reasons I brought him to Japan. Zooentropy is my attempt to understand behavioral complexity in the context of animal welfare, and behavioral diversity is one component of that.


In Miller’s view, the diversity of behavior an animal displays might offer a window into the extent to which it is capable of expressing its natural habits. Where environments offer all of the required stimulation, we may see a fuller range of such species-typical behaviors emerge. On the other hand, where environments fail to stimulate the animals in all the necessary ways, behavioral diversity may also be truncated and favor repetitive patterns instead.


Miller recently published a review and call-to-action on behavioral diversity for animal welfare assessment in the Journal Animals in 2020. In other studies, he has also shown that behavioral diversity correlates with rates of stereotypical behavior and/or physiological stress in dolphins, chimpanzees, and cheetahs (Paywall).


His model of behavioral diversity is based on Shannon’s Diversity Index, a common index used in a lot of different contexts. This is based on behavior sampling and measures the level of unpredictability observed in a sample of different kinds of behavior. In other words, if you sample an animal’s behavior and observe the same 3 behaviors over and over again, at more or less the same frequency, then behavioral diversity is low. If instead you observe 10 behaviors, and they occur at wildly different frequencies, then behavioral diversity will be high.


Table 2 from Miller et al (2020) in the MDPI journal Animals. The table shows the range of Shannon's Diversity Index estimates across species of zoo-housed animal that have been studied to date (citations to original papers are not included)
Table 2 from Miller et al (2020) published in the MDPI journal Animals. The table shows the range of Shannon's Diversity Index estimates across species of zoo-housed animal that have been studied to date (citations to original papers are not included)

With Zooentropy, I am also interested in Shannon Entropy, among other metrics, but in my case using behavioral time series rather than static samples of behavior. That said, some of the principles overlap, in that behaviorally diverse time series are likely to produce high-entropy sequences, as long as there is not a high degree of autocorrelation within them.


Regardless, it’s all about adding to the toolbox and learning how these different potential welfare indicators relate to each other, and to other more broadly accepted indicators of animal welfare at places like zoos and aquariums. That’s a key goal I have with the Zooentropy project and through the Zooentropy Network! So stay tuned…

Science at Zoos and Aquariums in Japan


Meanwhile, the second speaker at our Kyoto City Zoo event - Dr. Wataru Anzai, keeper at Hiroshima City’s Asa Zoological Park - provided a detailed summary of zoo-based research in Japan.

Anzai and his colleagues summarized the results of a survey of research conducted at Japanese zoos over the last 60 years! This reminded me of the “Twenty-Five Years of Zoo Biologyarticle published in the journal Zoo Biology (Paywall) in 2008. Anzai and co’s study will be my new go-to guide when designing activities for the Zoo biology class I teach at Kyoto University.

The major takeaways of this survey were that, although research at zoos has diversified in the past 30 years and the number of scientific publications is steadily on the rise, most zoos are not participating in such knowledge generation and dissemination (especially among aquariums) and focus on animal welfare is sparse.


That is exactly why we thought an event like this, featuring a well-known zoo animal welfare scientist from the USA and an up-and-coming cast of motivated young scientists in Japan led by Wataru Anzai and Yumi Yamanashi, would have a lot of value for the zoo community in Japan.


Anzai noted in his talk that JAZA - Japan Association of Zoos and Aquariums - does not (as of March 2023) have a committee set up to oversee and provide recommendations for animal welfare.


Moreover, one of Anzai’s coauthors, Tomoya Kako from the Port of Nagoya Public Aquarium, found in a survey of zoos and aquariums in Japan that although 64% of them employ staff with graduate degrees, only 11% have research departments and most staff in those departments are also keepers, curators or educators, which leaves them little time for scientific study.


In that sense, Kyoto City Zoo is one of a very select few that actually has a dedicated research department that staffs full time researchers. I would hazard that they also wear many hats at the zoo and assist in various other activities, but that puts Kyoto City Zoo at the front of the push to increase the visibility of Japanese zoos as drivers of zoo-related research advances.


I’ve been happy to have the opportunity to work with them, particularly Yumi Yamanashi, toward doing some welfare science related work. But the next steps for us will be to pin down some ideas and collaborators and apply for funds to continue pushing animal welfare science forward in Japan.

The WAZA 2023 Animal Welfare Goal


There are more than 300 zoos in Japan, around half of which are members of JAZA. Now, the World Association of Zoos and Aquariums has mandated that all WAZA members must have in place a welfare assessment protocol by the end of 2023. See the WAZA 2023 Animal Welfare Goal for details.


It would be great if institutions in Japan also make this a goal of their own in the near future, for the benefit of the many individual animals of countless species exhibited across the country.


We hope that the event we held in Kyoto will help us get there.


Lance Miller and Wataru Anzai listen to an audience member's question being read out by event organizer Yumi Yamanashi
Chicago Zoological Society's Lance Miller and Hiroshima City Asa Zoological Park's Wataru Anzai during discussions at our Kyoto City Zoo event on Animal Welfare Science in the US and Japan


The Five Opportunities to Thrive

(from Lance Miller and co. while at the San Diego Zoo)


1. Opportunity for a well-balanced diet: fresh water and a suitable, species-specific diet will be provided in a way that ensures full health and vigor, both behaviorally and physically.

2. Opportunity to self-maintain: an appropriate environment including shelter and species-specific substrates that encourage opportunities to self-maintain.

3. Opportunity for optimal health: rapid diagnosis and treatment of injury or disease, while providing supportive environments that increase the likelihood of healthy individuals.

4. Opportunity to express species-specific behavior: quality spaces and appropriate social groupings will be provided that encourage species-specific behaviors at natural frequencies and of appropriate diversity, while meeting social and developmental needs.

5. Opportunities for choice and control: providing conditions in which animals can exercise control and make choices to avoid suffering and distress, and make behavior meaningful.

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