People Watching: the study of urban wildlife is a two-way street

My eyes are instinctively drawn to a black, blue, and snow white flurry of movement. A reflex hammer to my naturalist’s knee. The subject of my fascination springs a brisk two-footed hop-scotch, just ahead along a ribbon of green separating parking lot from bustling sidewalk in downtown Calgary. The throng of oncoming foot-traffic ignore the avian specimen to their left -the black-billed magpie (Pica hudsonia), preoccupied with foraging among decaying fruit fallen from the crab-apple canopy overhead, is similarly unperturbed by susurrations of the passing shoe-lace express. Like the crab-apple tree, I am a transplant to Calgary and a recent one at that. This naiveté to the local flora and fauna causes me to fixate on what can be fairly characterized as an exceedingly common sight in cities throughout this magpie’s westerly range. By contrast, the surrounding citizenry afford this tri-coloured bird no more consideration than they would a rock dove. Although…to be fair I can also often be found scanning the wonderfully colour polymorphic flocks of this archetypical urbanite.

Abreast of the magpie now, I stop. Mirroring me, feathers settle excepting those tousled by the autumn breeze, a gust redoubled by constructed concrete corridors. I glance down to lock, for two heartbeats, with discriminating eyes at the end of curious and straining neck…thump…thump…then the magpie is airborne, trailing raucous cry and pennants of blue-green iridescence. Reverie shatters as I realize my rapidly vanishing feathered friend is not alone in its unease at my behaviour. Fellow pedestrians – the same the magpie saw fit to ignore moments before I indignantly note – have begun casting sideways glances…ever a hazard of being an urban biologist. Onwards then to the next green ribbon.

Cities are a mirage. At the utterance of urban, all can conjure an image in their mind’s eye. Grasp at defining characteristics however, and details vanish into intangibility. This is because the features of urban landscapes around the world differ dramatically based on culture, climate, socio-economics, industry, and history. These factors operate at fine-scales, generating remarkable heterogeneity even within cities. However, one feature inextricable from the essence of what is urban is this ecosystem’s engineer, humans. As such, urban ecologists have long been interested in wildlife responses to human exposure. Weaver et al. 2018’s recent publication is yet another chapter in that saga.

A) Intra-specific comparison of flight initiation distances (mean ±95% CI) for 20 avian species measured both in rural and urban habitats. Carrete & Tella 2011

In this Landscape and Urban Planning article, researchers from the University of Arizona  compare behaviours of captive house finches (Haemorhous mexicanus) in response to human exposure and observed that urban and suburban birds displayed reduced anxiety-like behaviour (bill wiping), when compared to their rural fellows. This is aligned with many other studies that report urban wildlife are less responsive to human exposure, something most commonly assessed in free-living wildlife by measuring how close a human observer can approach before an animal flees (a.k.a. flight initiation distance  or FID for short).

Differences between urban and rural populations can be substantive, with one researcher demonstrating that FIDs can be 7x higher in rural fox squirrels than their urban counterparts! These sciurid city slickers also spent less time after human encounters engaging in anti-predator behaviour (i.e. belligerently flagging tails and chattering teeth… the squirrel equivalent of trash-talk of which I have often been the target). Reductions in FID are commonly reported among urban wildlife, and may not be all that surprising since most encounters between pedestrian foot-traffic and wildlife residing in cities are likely benign. Time spent foraging instead of needlessly depleting energy reserves fleeing non-harmful stimuli offers an apparent advantage.

However, while reigning in FID might be adaptive, it is unclear whether trends towards human-tolerance could represent true urban evolutionary change. Habituation, the ability for individuals to adjust their behaviour based on prior experience, likely features prominently in these patterns; a point driven home by the same fox squirrel research above, in which naïve urban juveniles had much larger FIDs, and engaged in more belligerent behaviour directed towards humans, than wise-to-the-world grey-tails. An individual squirrel may learn from

B) Variability in FID versus relative brain size of 21 avian species in rural habitats (fill: white – species near absent from cities, grey – city < rural, black – city > rural). Carrete & Tella 2011

frequent false alarms that frenetically fleeing up the nearest tree at every passing human might be an over-reaction. But this hard-won experience is not passed onto offspring. Without some heritable FID trait, evolution towards reduced FID in urban environments could not occur. At an inter-specific scale, it is apparent that not all are equal in their behavioural plasticity to human approach. This may signal that heritable host traits could underlie a species’ habituative capacity. There is also evidence both within and between European bird species, that reductions in FID might signal true urban evolutionary change.

Although FID is a common metric used to assess animal behaviour, it often fails to discern the subtleties of wildlife responses to human exposure. Urban wildlife are monitoring not just proximity but also your behaviour, they respond accordingly. For example, although urban squirrels may have shorter FIDs than their rural counterparts, Bateman and Fleming (2014) demonstrate that just how short depends on YOUR behaviour.

Proportions of urban eastern grey squirrels in each of four approach treatments that either fled or did not flee an approaching pedestrian – Bateman and Fleming 2014

Walk on a squirrel adjacent sidewalk, mind your own business, and you and your furred fellow urbanite will be copacetic. Walk off a path tangential to a squirrel while glancing its way however, and this will send the squirrel running. This is because you have just rudely violated a rudimentary ‘Human Code of Conduct’*, unknowingly imposed on you by the squirrel. This silent agreement is that you refrain from eye-contact and remain walking a straight-line path on those concrete highways built in miniature. The squirrel has a catalog of expected human behaviour and you, my friend, just went rogue. Needless to say, in pursuit of my research on urban eastern grey stress physiology and intestinal microbiomes (more on that in a later post), I have become a behavioural outlier in the mind of many a squirrel.

‘Red-Yellow-Black’ – has mastered the art of reading humans. She can often be found sunning herself in the middle of busy walkways or on the tops of trash cans awaiting meal delivery…a behavioural and body mass outlier both.

I have put Bateman and Fleming’s findings to the test more than once, albeit with some twists. In the spring of 2017, I found myself hand delivering peanut-butter-ball goodies to specific squirrels identifiable by colour-coded ear-tags (part of an experimental manipulation**). Stop on a path near a squirrel, glance their way and soon they’ll be scrambling up the nearest tree, chattering all the way. However, stop on a path near a squirrel, glance their way, and hold out your hand…and many will come bounding towards you – a behaviour sure to confound any FID trial. This response was not universal though, and I soon learned the eager customers (eager from the onset) from those more aloof.

Sketch by Bronwyn Robinson (insta: @wynnierobins) – Artist & avian research tech extraordinaire.

Food seeking from humans is undoubtedly (like FID) heavily influenced by habituation, and indeed, in my experience juveniles were near impossible recipients of experimental treatments. However, over the course of this 2-week experiment, the reticence of many squirrels quickly faded, while others treated me with redoubled wariness. It is unclear to me what might underlie these inter-individual differences. Like FID, there is evidence that not all species are equally adept at reading human cues. Human infants show more acuity in interpreting directive gazes than some of our closest primate relatives; domesticated species (dogs, goatshorses etc.) often more reliably read human cues than human habituated wildlife (Asian elephants, chimpanzees, foxes etc.). Rather than simply avoiding interruptions to foraging by reducing FIDs, a refined ability to read human cues in cities may also allow wildlife to occasionally win high calorie meals – a scene no doubt playing out daily in city parks the world around.

While the magpie I encountered on the streets of Calgary was a new sight for me, my stopping and gawking was likely unexpected and disconcerting for the magpie. The momentary inspection before flight might have been to size me up for a meal – not two blocks away, I spied a man tossing seeds to a roiling mass of squirrels, pigeons, and yes, magpies. The bird I startled paid no heed of other passersby, because they were unknowingly adhering to the unvoiced accord, between bird and human, to ignore one another along their morning commute. Just as urban biologists have begun closer observation of the wildlife colonizing the ecosystems we’ve engineered, many wildlife in cities are making a careful study of us. If fitness on an urban landscapes is tied to an ability to read human behaviour, is it possible that some urban wildlife are evolving a refined ability to people watch? Regardless, the study of urban wildlife is a two-way street.

 

* A comparable ‘Large Rumbling Beasty Code of Conduct’ cached away deep in the urban squirrel psyche might explain their relative success at road crossing, and ambivalence to cars during roadside foraging.

** PSA: This was done with a permit for the purpose of research. Please do not feed wildlife, it does more harm than good.

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