Angela R. Freeman PhD - Neuroscientist and Behavioral Ecologist
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what are the mechanisms involved in communication?

Current research of social signals

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olfaction and reproduction
​ of Pouched rats
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Richardson's ground squirrels
​Neurobiology and signaling

 Other Collaborations

C/o Gerry Carter
neuroscience of cooperation in vampire bats
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Ontogeny of oxytocin and vasopressin systems

 
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giant african pouched rat olfaction

why are pouched rats excellent 'sniffers'?

In January 2017 I started working as a postdoctoral fellow at Cornell with Dr. Alex Ophir. My work here focuses on the olfactory capabilities and social signals of the giant pouched rat (Cricteomys ansorgei).
In addition to behavioral work, with our collaborator Dr. Michael Sheehan (Cornell), we are examining genetic and genomic aspects of olfaction in this species.
My main questions have been: what are the signals these pouched rats send and receive, what are the indicators of discrimination ability, what role do these potential signals play in mating?
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Pouched rats are used as biodetectors, so understanding what might support olfactory behavior is important for producing effective animals for landmine and tuberculosis detection. However, we actually know very little about the reproduction and olfaction in this species, and it turns out the pouched rat is fairly unique in both of these areas.
So far, we have found that male pouched rats are most likely to scent mark (with urine) in unfamiliar environments, which may advertise to other individuals (Freeman and Ophir, 2018, Journal of Mammalogy).
Furthermore, we have determined that male pouched rats that are highly masculinized show an enhanced preference for reproductively available females (based on interest in female scent) (Freeman, Sheehan, and Ophir, 2019, Animal Behaviour).

Pouched rats are not only incredible olfactory specialists, they also have a very unique reproductive biology. Pouched rat females have vaginas that can reversibly close throughout adulthood. When they open, their 'scent profile' changes to ones that males find irresistible. We conducted repeated metabolomic assays on females when they were closed and after they recently opened, and saw that the profiles became extremely similar after opening.
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Pouched rat females change their 'scent profile' when their vagina opens. Left, closed and open-vagina females. Right, same 'closed' females after opening.
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It turns out that these 'closed' or 'non-patent' (as a technical term) females also differ in their reproductive organ size. Non-patent/closed females have smaller uterine horns and cervices compared to patent females. This corresponds to their external genital morphology, shown in our Animal Behaviour paper in 2019.

We suspect patency shifts are driven by the social environment, but we only have some pieces of this puzzle. In February of 2018, a female with a reliable estrus cycle died from old age in our colony. When she did, 7 non-patent females opened within a month. These non-patent females had been closed for up to 3 years, were of different ages, were not related, and were all on the same diet and exposed to the same light and temperature. We are exploring what this suppression cue from cycling females might be, and working currently to understand the neural and physiological mechanisms of patency shifts in the pouched rats.

 

Richardson's ground squirrel Neurobiology

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As part of my dissertation work, I have been exploring the neural mechanisms of communication and social behaviour of Richardson's ground squirrels (Urocitellus richardsonii) under the supervision of Dr. Heather Caldwell (Kent State) and Dr. Jim Hare (U of Manitoba).

Richardson's ground squirrels are a moderately social, colonial rodent native to the prairies. Our study population was located in Winnipeg, Manitoba, at the Assiniboine Park Zoo.

We conducted research which investigated the neural mechanisms of alarm call perception, as well as production and social behaviour. We found that central vasopressin administration altered squirrel behaviour, making males more vigilant and more likely to escape potential predators, as well as changing aggressive behaviors (Freeman, Hare, Anderson and Caldwell, 2018, Behavioral Neuroscience). Regions important for social behavior and communication contain receptors for vasopressin and oxytocin in this species, though the levels are highly variable among individuals (Freeman, Hare, Caldwell, 2019, Journal of Neuroscience Research​).


More recently, Liz Aulino (Kent State), Heather Caldwell, Alex Ophir and I conducted a meta-analysis which examined vasopressin and oxytocin receptor binding patterns across species (Freeman et al. 2020, Journal of Neuroendocrinology). We showed that some brain regions have highly correlated binding patterns, such as the OTR binding patterns in the BNST and Central Amygdala. Nearly all rodents studied to date have OTR in the BNST - a region known for its role in a broad range of social behaviors.
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V1aR ('g') and OTR ('h') radioimmunoassay and Right, Cresyl violet (in Richardson's ground squirrels). From Freeman et al. 2019.
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OTR binding in the BNST is shared in all rodents studied thus far (except Guinea Pigs). From Freeman et al. 2020
We are also interested in which brain regions are activated from different types of alarm calls; our preliminary research shows that high threat vocalizations (i.e. chirps) elicit different activation patterns in the Medial amygdala and superior colliculus compared to whistle-receivers and controls.

I have also worked on a number of glucocorticoid-related projects, including one where we demonstrated partial heritability of the stress response in ground squirrels (Bairos-Novak, Ryan, Freeman, Anderson, Hare, 2016, Current Zoology).

Future research plans

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Making social assessments - how do you decide who is your 'kin'?
Following the theme of social signalling, my future work with ground squirrels plans to compare the social assessment strategies ground squirrels use. 
Social ground squirrels, such as the Richardson's ground squirrel above, use alarm calls to warn kin and other colony members of potential predatory threats. But how does a squirrel decide if 'kin' is 'kin'? (I use the quotation marks here, because in some cases selective affiliation towards the in-group is not actually related to true kinship - often it is based on only familiarity among individuals living together. Much like in humans, actual genetic relatedness is not required for these relationships and selective behavior).

Ground squirrels vary across species in the types of strategies they employ in making complex social assessments. Richardson's ground squirrels, for example, use some sort of genetic information to identify kin (Davis, 1982). In Belding's ground squirrels, however, littermates are treated as 'kin', but as adults, individuals can use some additional information (genetic or phenotype matching) to include additional genetic kin as part of their in-group/kin group. In Columbian ground squirrels, littermates are treated as 'kin', however, in later life indirect familiarization can lead to the concept of a larger 'in-group'. This lead to the following questions: Why are the kin-recognition or in-group assessment strategies different among these closely related species? Do these different strategies share a common mechanism (e.g. neural or physiological)? If we can change the strategies used, does this impact fitness? Why do these age-dependent social signal processing differences exist? 

Who run the world? Squirrels.
There are a lot of ground squirrels across the Western US and central Canada.
In addition to these social assessments of who is kin or in-group, squirrels have remarkable plasticity in their alarm call system. The responses to alarm calls are learned in the early juvenile life stage, however, even later in life individuals can reassess specific calls and respond accordingly. In Richardson's ground squirrels, individuals can remember the past reliability of a caller and respond accordingly - reducing trust in those who frequently emit alarm calls without a predator present.
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Age-dependent plasticity in communication
Much like the kin-recognition strategies above, there is age-dependent plasticity in the reception of acoustic signals. Logically, as an adult squirrel, it might be adaptive to ignore juvenile callers. Juveniles are still learning associations of predators and calls, and they might be more likely to call at potential threats that are not actual concerns. By being selective, adults could afford more time to foraging, and potentially, improve their chances of survival and future reproduction. Adults also have lower predation risk. However, if the caller is correct and a predator is near, ignoring the warning could be deadly. Depending on the overall costs, it might be more adaptive to simply respond to most calls and not attend to the age of the caller. This might increase false alarms, but would reduce missed detection. Juveniles, given that they might still be learning associations, should attend to all calls, in particular because they are at greatest risk for predation. Indeed, this is what is observed in Belding's and California ground squirrels - where adults respond more strongly to adult calls and less to juvenile calls (Belding's), or older squirrels tend to be less reactive overall (California).
However, in other species, Columbians and Richardson's - adults and sub-adults respond similarly. Why might age-dependent signal assessment exist in some species but not others? Are these mechanisms shared (e.g. do all juveniles have increased glucocorticoids increasing reactivity but also learning)? When do these differences disappear (if age differences exist)? Are these differences more ubiquitous across all ground squirrels? When might it be adaptive to choose one strategy over another?

 Other Collaborations

 

Vasopressin and oxytocin receptors and bat cooperation

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Dr. Gerry Carter's website
Left: Desmodus rotundus brain (whole)
Right: Desmodus rotundus brain (being sliced coronally; shown is the start of the ventral hippocampus)
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In collaboration with Dr. Gerry Carter (Ohio State), Dr. Alex Ophir (Cornell) and Dr. Rachel Page at the Smithsonian Tropical Research Institute, I travelled to Panama in 2017 and 2019 to collect tissue to examine the neural basis of cooperation in bats. Currently we are slicing bat brains prior to localization of oxytocin and vasopressin 1a receptors, which should help us elucidate the evolution of these potential mechanisms in the Phyllostomidae family.
 

Ontogeny of the vasopressin and oxytocin systems in prairie voles

An ongoing collaboration with Liz Aulino, Heather Caldwell, Alex Ophir, and Jesus Madrid is examining how the oxytocin and vasopressin systems might change in the development in the prairie vole. These neural systems are highly plastic, and in mice, recent work by Aulino has shown early sex differences in development of the vasopressin system.
This project is ongoing, and in its early stages.

Previous research projects

Infrasonic communication by indian peafowl

For my masters work, I was supervised by Dr. Jim Hare at the University of Manitoba. We recorded peacocks displaying and noted that there seemed to be low frequency components in the train-shaking displays. We then played back these components using a rotary-based subwoofer that was installed in an old Manitoba Hydro van, creating a resonance chamber to propagate the infrasonic signal. 
We determined that both males and females can perceive this infrasound and respond by becoming alert, and walking and/or running. Males responded to infrasonic signals by vocalizing, but did not respond to the 'audible' (i.e. >20Hz) versions of those signals (Freeman and Hare, 2015, Animal Behaviour).

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Fear and maternal investment by song sparrows

In 2009, I assisted Aija White (supervised by Dr. Liana Zanette, Western) with her thesis project investigating maternal investment by song sparrows and the perception of fear. We spent nearly all of a glorious summer in the Gulf Islands nest searching, setting up videos to record predation events, mist-netting, and setting up playback units on breeding territories.
The work determined that perceived predator risk reduced offspring investment, perhaps as a way to shift investment to a following year (Zanette, White, Allen, Clinchy, 2011, Science).
Pictured: Song sparrow nestlings, Gulf islands sunset.
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landscape ecology of northern flying squirrels

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Flying squirrel after release
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Radiocollared female flying squirrel
I spent two field seasons working with Dr. Matt Smith (supervised by Dr. Graham Forbes University of New Brunswick) assisting on his dissertation work examining landscape use by northern flying squirrels. We trapped, translocated, radio tagged and released a number of squirrels to determine how they cross different landscapes. The research showed that squirrels strongly preferred forested routes (Smith, Forbes, Betts, 2013, Biological Conservation), and homed best when connectivity within the landscape was high (Smith et al. 2011, Landscape Ecology). 

Other field jobs

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In addition I have worked and volunteered as a bird bander in both Canada and the US.
Left: Olive warbler, banded in Arizona
Right: Saw-whet banding with master bander David Lamble

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