Thank you, Dr. Clapp. In the examples you note above, it would suggest that one of the factors most important for training as enrichment (if it is, in fact, enriching) is simply some form of social interaction and/or habituation. So that would be an important factor to control for, such as using response-contingent food delivery/attention (i.e., the animal is required to engage in a targeted behavior) vs. response-noncontingent food delivery/attention (FT/VT schedule or the like). I would suspect that habituation/sensitization in the form of handling and the ability of engaging with trainers/keepers/caretakers would play a significant role in producing an enriching effect, rather than the actual training task. But, again, that's an empirical question, and one worth investigating!

I would imagine that a laboratory scenario, or agricultural setting, like you suggested, could be ideal for testing this. Neuroscientists and other animal researchers have become increasingly more interested in environmental enrichment, since it's also been correlated with results such as increased neurogenesis activity/speed (references, anyone?) So not only could this generate some great research, but also be NSF/NIH funding-worthy! I myself would be very interested in working with 'the brain folks' on this kind of research (I'm still trying to work my way into using assays and other physiological measures that be correlated with behavioral welfare indices!) Good stuff.

Hi Eduardo,

Zebunke et al. investigated the impact of a learning task on HRV in pigs, using a design without human handling. I do not completely agree with their conclusion but the references they cite could be interesting to you (better wound healing, changes in brain opioid receptors). Regarding neurogenesis, I included a link that might be a starting point (although it's focusing on an Alzheimer mouse model).

Regards,

Steffi

http://www.ncbi.nlm.nih.gov/pubmed/19118549

Hi Eduardo.

What a great subject!  I am not aware of any studies on the following, but anecdotally, I have seen training increase the self-confidence of anxious animals.  Such animals are initially difficult to train because positive reinforcement training requires that an animal do something in order to be rewarded.  Anxious animals tend to freeze when they are put into situations that demand that they act, so it's difficult (comparatively speaking) to get them to do something for which they can be rewarded.  In other words, training for them is initially not enriching --- it's stressful.  Once they figure out the rules of the game, though, they become eager to participate, because while they are participating, they have some control over what happens in their lives.  Performing a behavior becomes a way of demanding a treat.  Such control improves the welfare of all animals, but it has seemed to me that it is especially beneficial for those with anxious personalities.  I'd guess this effect would occur even with Skinner box training, but it would certainly fit in with the cognitive bias testing mentioned above.  I would expect cognitive bias to become more positive as an anxious animal gains more confidence.  Anyway, I'd love to see this hypothesis explored scientifically.

In essence, training teaches an animal to think about controlling its environment, so an animal that has learned trial-and-error is probably more likely to benefit from other enrichment tools (e.g., foraging devices) or to find ways to enrich itself.  An animal that has learned to think in this way could be able to benefit from more complicated enrichment devices that would take up more of its time.  I would expect that the brain changes seen in animals in enriched environments would be even more obvious in animals enriched through training.

For the period of time it is being trained, an animal does not experience the boredom of confinement.  Making human interactions positive reduces stress and provides some social stimuli for isolated animals.  These factors combined (and probably others that don't come immediately to mind) should help reduce stereotypies.  It would be easy to check something of that type.

I think there are all sorts of ways to explore training as enrichment.  If you are training husbandry behaviors, you would be killing two birds with one stone (so to speak) --- or maybe even three birds, because husbandry-trained animals reduce handler stress, too.  Best of luck to you in your endeavors.

Wendy 

Hi Eduardo,

This is directly related to my primary research interest in human-animal interaction and relationships (primary with nonhuman primates). I know you've done some related work in the area of visitor effects (which I've referenced extensively). I'm glad you raised this issue here and that others are looking into it in more detail.

Looking at the conversation so far, it seems there are actually two questions being asked. First, whether training (such as PRT or task training) is enriching in the sense of wellbeing/welfare similar to other forms of enrichment (like environmental/behavioral enrichment). Second, whether training is beneficial, for example in the form of neurogenesis or other benefits that are beyond the scope of wellbeing/welfare.

I'm not familiar with the second, but in regards to the first I'm pretty sure there is very limited empirical investigation beyond the studies you've mentioned and a few similar (looking at behavior change, reduced anxiety/aggression, post-training interactions with humans or conspecifics, etc). All of the outcome variables that you suggest could very well be used as indicators, although there would be need to control for other variables that also impact the outcomes (for example, training + novel environmental manipulation, training + food, changes in social composition or interactions, presence/absence of humans, familiarity of humans, etc). Also, some indicators are only valuable after there is already a problem (such as abnormal behavior). So while they might be good indicators for interventions, they clearly cannot be used to evaluate the enrichment potential of training/interactions in all cases.

Based on my reading of the recent literature and my personal experience with my own research, I'd argue that (as you suggest above and others have as well) it is not the training, but the positive interaction and relationship that provide the positive outcomes, in line with predictions of the human-animal relationship model (e.g., Hosey 2008).

One of the easiest ways to test this prediction is to compare training interactions with other types of positive interaction (e.g., non-structured, non-task-oriented). Kim Baker and Mary Jensvold (refs below) have looked at positive non-training interactions between humans and chimpanzees. Research with gorillas (admittedly case studies vs. sizeable samples), suggest that PRT does not necessarily provide benefits over and above other forms of positive interaction (see two refs below). Other research suggests that unstructured, positive interactions (rather than training) provide positive welfare benefits - whether they are the same as enrichment is still open for debate. I have a book chapter forthcoming that touches on this. I can't post it publicly, but if you send me an email I'll send you a draft copy).

I'll stop now because I can talk forever on this topic. As a final suggestion, I'd suggest contacting Geoff Hosey directly (I'm sure you're already familiar with him). Keep me posted - I'm very interested to see whether you come up with some novel research directions.

Baker KC. Benefits of positive human interaction for socially housed chimpanzees. Anim Welfare. 2004;13(2):239-45.

Carrasco L, Colell M, Calvo M, Abell MT, Velasco M, Posada S. Benefits of training/play therapy in a group of captive lowland gorillas (Gorilla gorilla gorilla). Anim Welfare. 2009;18:9-19.

Jensvold MLA. Chimpanzee (Pan troglodytes) responses to caregiver use of chimpanzee behaviors. Zoo Biol. 2008;27:345-59.

Jensvold MLA, Buckner JC, Stadtner GB. Caregiver-chimpanzee interactions with species-specific behaviors. Interaction Studies. 2010;11(3):396-409

Pizzutto CS, Nichi M, Ramiro Corrêa SH, Ades C, DeBarros Vaz Guimarães MA. Reduction of abrormal behavior in a gorilla (Gorilla gorilla gorilla) through social interaction with human beings. Laboratory Primate Newsletter. 2007;46(3):6-10.

Such a great topic! I am currently initiating a project in Costa Rica that will examine this question. There are captive populations of wild-born primates and raccoons displaying stereotypies. The center was originally designed for rescue and release, but due to new legal guidelines these animals cannot be released. My idea is to use training not only as a form of enrichment but to also reduce animal stress. Much of the care at these types of rehabilitation/rescue centers is administered by inexperienced volunteers. While I was there, there were multiple negative and stressful animal-human encounters during feeds and enclosure maintence. My hope is that basic training can prevent negative human-animal interactions and also act as a form of enrichment. we have a wealth of behavioral data on the animals so far and will try to make a comparative behavioral study after the implementation of a training program. If anyone has any advice I would greatly appreciate it.

I have no doubts that training (or caretakers-animal relationship) has in most cases a positive effect on animal welfare. A related question should be what is the effect of no interactions-training when some facilities such as marine parks and zoos are closed to the public in winter months.

For those interested in the combination of training + enrichment, we've just our paper in Zoo Biology on training penguins to enrichment items come out in Early View. You can see the pre-print on my page: Fernandez, EJ, Kinley, RC, & Timberlake, W. (2019). Training penguins to interact with enrichment devices for lasting effects. Zoo Biology.

Very interesting question - I have more experience in Animal Studies from a Literature point of view, but am interested to see any more answers to the question