#22: Mini-episode 3 - Puppy whines and maternal care, impacts of housing on shelter dog stress

Summary

In this conversation, I discuss two research papers related to dog behavior. The first paper explores the influence of puppy whines on maternal behavior in dogs. The study found that puppy whines trigger maternal care - with stronger maternal care in response to the mother's own puppies.  The second paper examines the impact of different enrichment interventions on the stress levels of dogs in a shelter. The study suggests that housing dogs with conspecifics may be beneficial in reducing stress. However, the results are not clear cut and I discuss the limitations and challenges in interpreting this study.

Takeaways

• Puppy whines can influence maternal behavior in dogs, and mothers can identify their own puppies based on the acoustics of their whines.
• Housing dogs with conspecifics may help reduce stress levels in shelter dogs.
• Individual variation in shelter dogs is important to consider.
• Interpreting results in stress-related studies is complex - I discuss some of the important points to consider.

Chapters

00:00 The Influence of Puppy Whines on Maternal Behavior in Dogs
10:19 Enrichment Interventions and Stress Levels in Shelter Dogs

References

Massenet, M., Philippe, R., Pisanski, K., Arnaud, V., Barluet de Beauchesne, L., Reynaud, K., ... & Reby, D. (2024). Puppy whines mediate maternal behavior in domestic dogs. Proceedings of the National Academy of Sciences, 121(22), e2316818121.

Corsetti, S., Natoli, E., Palme, R., & Viggiano, E. (2023). Intraspecific interactions decrease stress affecting welfare in shelter dogs: A comparison of four different housing conditions. Animals, 13(11), 1828.

If you'd like to learn more or contact Dr. Spaulding, you can do so through our website www.sciencemattersllc.com.

For more information, please check out my website and social media links below!

• https://sciencemattersllc.com/
• Facebook
• Instagram

Transcript

Kristina (00:01.074)

For this episode, the first paper that I'm going to cover is by Massinet and colleagues. And I chose this one kind of just because I think it's sort of fun and interesting, but it does also have some potential applications in certain situations regarding puppy raising. And so this is a paper about puppy whines and how they influence maternal behavior.

So I talk a lot about the importance of prevention and early intervention when it comes to behavior issues in dogs. And in order for us to do this effectively, we need a much better understanding of early development. So like I said, this study examined the behaviors between the puppies, specifically the wines from the puppies and the mothers.

Kristina (01:17.49)

So as I said, this study examined the influence of puppy whines on the behavior of the mother. And this will give us an additional step towards understanding puppy behavior and development. We do already know that poor maternal care in a variety of different species can decrease stress resilience.

Kristina (01:41.234)

can decrease stress resilience later on in life. So I think it is important to understand more about maternal care in dogs.

Kristina (01:55.858)

This is a very in -depth study and they did an acoustic analysis on 4 ,400 wines from 220 puppies in 40 different litters with 16 mothers and these were done in beagles.

Kristina (02:16.402)

So what they found was that wines vary both within and between litters. And that means that different litters of puppies have different characteristics to their wines. So basically AI was able to analyze the wines of individual puppies and correctly place them into the correct litter.

purely based on the acoustics of their wine at above chance levels. I do want to mention that it was still far from perfect. The success rate was below 40%. But it's still above chance. So they're picking up on something there. And that suggests that mothers are identifying, likely identifying their own puppies based on acoustics.

common to the entire litter. But there's probably other things going on as well. I would be very surprised if scent doesn't play a role. So that was one of the things they did. One of the other things they did that has some very interesting results is that they played back the vocalizations to the mothers by placing speakers just outside of the nest. So these were the vocalizations of her own puppies, but then they also

played some other vocalizations as well. So when mothers heard the vocalizations of their own puppies, they responded 94 % of the time, very high. And the playback elicited behaviors such as providing maternal care, sniffing, looking at their puppies, sniffing or looking at the speakers, as well as some stress -related behaviors.

And in 16 % of the trials, the mothers actually carried the loudspeaker into the nest, which I think is especially notable given that these are beagles and not necessarily genetically prone to retrieving, though that is a whole other can of worms that we will not get into right now.

Kristina (04:34.034)

What they also did is they modified the actual recordings of the puppies to synthetically generate wines that had been modified in a few different ways. And using this method, they found that mothers responded more to synthetic wines that were generated from their own puppies than wines that were from puppies of other litters. So basically they...

They took the mom's own puppies and they modified their wines and then they played them back to her. But they also took other mother's puppies and modified those wines and played them back. And the mothers responded more to the modified versions of their own puppies, which indicates that they're still picking up on something, even though it's been modified, that indicates that that is their their puppy.

that is making that sound. And this effect, the difference in the behavior from the mother was particularly strong when it came to carrying the loudspeaker into her nest. She was much more likely to do that when it was modifications of the vocalizations of her own puppies.

If they changed the wines so that they were outside of the litter's normal range, sort of made them sound weird basically, you did not see as much of an increase in maternal care and the same was true with wines from other litters that had not been modified, you did not see as much of an increase in maternal care.

They also found that in most cases the wines of the smaller puppies were higher pitched.

Kristina (06:34.642)

They also found that in most cases the wines of the smaller puppies were higher pitched and so they then did some more synthesis.

synthesizing and they created wines that were supposed to mimic high -pitched wines from the mother's own litter.

and they found that when they did that, so you maybe take a puppy that isn't the smallest puppy and you change it to make that puppy's vocalization higher pitched, when they did that it stimulated an increased amount of interaction from the mom compared to puppies that were not as high pitched. But this effect didn't work if they were modifying the wine from a different litter.

Kristina (07:33.81)

So I thought that was just really interesting, right? It's some in -depth knowledge on what kinds of cues might be stimulating maternal care in mothers. And I do think there are some potential applications of this. So for example, if you are...

helping to care take a litter of puppies and you're not seeing a lot of engagement or maternal care from the mother, one of the things that might be worth investigating is what's going on with the puppies themselves and how much are they vocalizing? Or maybe there's one puppy that's not doing as well. Is that puppy vocalizing less than the other puppies?

And is there something we can do to change that? So maybe something as simple as recording that puppy's vocalizations and then, or even the vocalizations of the entire litter and then playing that back may increase maternal care. I certainly don't think that's going to be the only explanation, but it is a potential avenue for intervention.

Kristina (08:49.906)

It also suggests that if you are trying to foster puppies to a new mom from another litter, so you have a foster mom, that it may be beneficial to record the foster mom's biological litter and play back those sounds when the new pups are introduced, and that may help trigger maternal care to those new puppies. Now, please understand that this was not tested in the study. This is...

something that I am, this is a prediction that I am making, so we don't know for sure that it would help, but it might be something that's worth trying, especially if you feel like you're having a hard time getting that mother to engage with the puppies.

So that is the first paper. And I'm just going to cover, I'm going to try just covering two papers because my episodes are supposed to be many episodes, but they were starting to run a little bit long.

Kristina (09:51.506)

So the second paper for this mini episode is coming from Corsetti and colleagues. And this is looking at how different enrichment interventions in a shelter impact the stress level of the dogs. This was a study that was conducted in Italy. And I did not know this until reading this study, but apparently there is a law in Italy.

that require shelters to be no -kill, which means dogs can have very, very long stays in shelters. So they looked at 10 dogs. They were all intact males. And they had all been in the shelter for one to two years, being housed in five to 10 foot kennels, or excuse me, five by 10 foot kennels that had an indoor and an outdoor porch.

portion and are never being walked. So right off the bat, right, we have major concerns about the welfare and well -being of these dogs that have been living in that environment for at least a year. So what they did then is they took each of those 10 dogs and put them in four different conditions. So they,

They all spent time in each condition and they observed their behavior while in that condition.

and then they counterbalanced the order so they didn't go through all the conditions in the same order. So they had the baseline condition where they were in that five by 10 foot kennel. They were able to smell and hear other dogs, but they could not see them because the sides of the kennels up to a certain height were solid. The second condition was that they were alone in an enriched cage.

Kristina (11:51.794)

And so this cage was a little bit bigger. It was 10 by 10 feet, roughly. And they were able to see other dogs. They also had what they referred to as a dog basket, which I'm assuming is a dog bed, a slightly raised platform that they could stand on that allowed them to see other dogs, toys, bones, and scented cloth. And there was also an area within that kennel, that small area that had dirt and grass.

The third condition was when they were housed with two con specifics. So this is again, a 10 by 10 foot kennel, where again, they can see other dogs. And they're also has with two spayed females. And then the last condition was human interaction. Here they were in that normal baseline kennel. So the one that was five by 10 feet, and they could not see other dogs.

but they had regular daily interaction with someone in an outdoor enclosure that involved play or petting, depending on which the dog preferred. And that interaction lasted for two hours a day. In order to get to the outdoor enclosure, they did have to be walked down the row of kennels where they're being barked at by other dogs. And...

It also involved handling and leashing the dogs, which they were not used to because they had just been living in these kennels without really being routinely taken out of the kennels. So each dog was in each condition for 10 days. And then they observed each dog for a total of an hour a day to try and determine if there were any behavior changes. So I understand an hour is not a lot of time, but we have to work within the realistic constraints.

of what people are able to do, right? So observing eight hours of each dog a day is probably not realistic for 10 dogs that are in four conditions that are 10 days each. In addition to behavioral observation, they also collected cortisol levels, specifically fecal cortisol levels, and they took at least three samples per dog per condition.

Kristina (14:13.362)

So cortisol can be collected in a number of different ways. And one of those is through the feces. And then, and they chose this because it's non -invasive. It's not as timely because obviously they're not, you know, defecating immediately after, for example, interaction with people, but really they were trying to look at.

across 10 days of having these different enrichments what was the effect. So I think that this is an appropriate way to try and assess cortisol levels. So what did they find? First of all they found that displacement behaviors were more common when the dogs were alone than when they were housed with two females.

And very few dogs showed, well I shouldn't say very few, I mean there's only 10 in the sample, but only two dogs showed stereotypical behavior during the study, but both of those dogs showed that stereotypical behavior while they were in that baseline alone condition. In terms of observed behaviors, there were no other behavioral differences between the four conditions.

They looked at sort of all what they called olfactory investigation. So I'm assuming that that means how much time the dogs are spending sniffing around their cages. They spent more time doing that when they were in the enriched cages. And remember that the enriched cages had specifically scented cloth as well as earth and grass.

Also, the highest cortisol levels occurred when the dogs were alone in their cage and when they had regular human interaction. And then after that, it was the enriched condition. So the highest was alone in the cage and regular human interaction. And they had the lowest levels of cortisol when they were with conspecifics.

Kristina (16:33.138)

But the primary difference in the cortisol levels was between...

Kristina (16:49.906)

So they found that the dogs had the highest cortisol levels in the human interaction condition and the lowest cortisol levels in the condition when they were housed with two other females.

It is worth noting, and this is actually not unusual at all, that the fecal cortisol levels and the displacement behaviors were not correlated. So basically what that means is that there was no relationship between the concentration of cortisol or the levels of cortisol and the types of behaviors we were seeing in the dogs. It's not uncommon to see this.

Kristina (17:38.674)

It's not uncommon to see this and it just basically speaks to the challenge of trying to assess stress.

and the fact that there's a lot of individual variation in the stress -related behaviors that dogs display. And on that note, they did specifically say in this study as well that the levels of individual variation were very high. And so that does make interpretation of the study a little bit more challenging. So just to give you an example,

One of the dogs in the study had their highest cortisol levels when they were alone and the lowest cortisol levels when they were getting daily human interactions. Another dog had the exact opposite. So that dog had the lowest cortisol levels when he was housed alone and the highest cortisol levels when he was getting daily human interaction. So,

It just, it's important to understand that when we're talking about these results, we're talking about averages. And although that can be helpful, it does.

It is not... I'm trying to think of how to phrase this clearly.

Kristina (19:20.466)

While that can be helpful, it's important to remember that not all dogs are going to display that exact pattern. Having said that, in most dogs, the cortisol was highest in the condition with humans. So that's taking the average, but also if you look at each individual pattern, you see that that's true for most of the individual dogs.

So the authors conclude that the most effective enrichment approach when it comes to decreasing stress in shelter dogs, at least dogs in this shelter, was being housed with two conspecifics. But again, it's important to note that that is clearly not the case for certain individuals, right? So, GOB,

did have the highest levels of stress. Excuse me, I'm sorry, that's incorrect. But he had the highest levels of stress when alone. Levels of stress with enriched females were, and this is based on cortisol, by the way, were sort of moderate, but then they were much lower when he was getting daily human interaction. And it just depends on the dog. So,

there was another dog, so R2, for example, had the lowest levels of stress in the alone condition, and all the other conditions were higher levels of stress. So this is just a reminder again, that it's really important to pay attention to the individual response as well. And I think it's important to note that being housed with conspecifics, having access to social interaction,

That is absolutely a form of enrichment. It might not be what we always think of when we think of enrichment, but it definitely is a type of enrichment. And even though this study found that interaction with humans was the highest stress level, and we're going to talk about that in a second, other studies have shown that human contact is important for decreasing stress. So,

Kristina (21:46.386)

Just to put it simply, this is complicated and we haven't worked out all the different things that are involved here.

I do want to note too when you look at the con -specific condition versus the human interaction condition, when they're being housed with other dogs, they had 24 -7 contact with those other dogs. And I'm not sure you can really compare two hours a day interacting with humans with 24 -7 contact interacting with other dogs. So that is a limitation of this study.

There's also a possibility that one of the things that's going on with the dogs and the human interaction group is that, or the human interaction condition rather, is that they're getting that interaction, but then it's been being taken away and that might have an impact. And also, as I mentioned before, in order to have that human interaction in this study, these dogs are being walked through a gauntlet of barking dogs.

that are being handled, which they're not used to, and they're being taken into areas outside of their familiar home cage. So it's really hard for me to be convinced that this is clean data, right? There's a lot of noise in this data. There's a lot of other things coming in. What is it that's actually driving up those cortisol levels? Because cortisol, I mean stress,

is a response to change. And so there's a lot of change going on with those dogs. Now, there's also change in having two new dogs come into your kennel. That is absolutely a change as well. But once they're there and the dogs adjust, then things are going to be relatively consistent, as opposed to the human interaction condition, where they're having this big event every day. And the event itself might be challenging. It's also really important to note,

Kristina (23:43.626)

that cortisol level, even though it's associated with stress, it does not actually tell us anything about the animal's valence. So what that means is it tells us that the animals are experiencing stress, which is a response to change. It doesn't tell us if that is good stress or bad stress. So simply looking at cortisol is really not enough to tell us about the well -being of the animals. That is where

behavior can come into play. And with that, we showed that displacement behaviors were more common when dogs were alone than when they were with the females. None of the other conditions had differences. So the results of this study are not super clear cut. That's not uncommon. Again, that's why we need to have multiple papers to really draw strong conclusions. But they do.

Certainly they indicate that being kept alone in an unenriched cage is probably not the best option, which I don't think is surprising to any of us. But they do indicate that housing dogs with other dogs may be beneficial. Again, with the understanding that that's not going to be the right option for every dog. So those are your studies for this month. I hope you guys find this helpful. And if you have any questions or comments, please feel free to contact me.

using the information listed in the show notes. Thanks everyone.