An Observational Study of Maladaptive Behaviors in Avian and Human Populations due to Urban Environments












By: Sabrina Bronni, Malcolm Davis, Jennifer Semaan, and Alexis Tangalos










LB 144 Biology I: Cell and Organismal Biology Section 009

Wednesday 7:00 p.m. - 10:00 p.m.

Professor: Dr. Douglas B. Luckie

TA: Anthony Watkins LA: Mellissa Ungkulde and Kaleb Howard

October 19, 2016

https://msu.edu/~bronnisa/

https://youtu.be/5QtxZ6rJLQU

Introduction

Finalized by: Alexis Tangalos

     Daily interactions with humans can alter an animal's responses to threatening situations (Lima and Dill 1990). These alterations can dull an animal's instinctive response to reach safety, thus affecting the rate of survival for a specific set of animals (Olsson et al. 2002) In an urban environment, such as Michigan State University, where nature is integrated into the campus, the animals that inhabit the campus often become accustomed to interacting with humans, causing them to not react to stimuli as they would in a more natural environment (McDonnell et al. 1997). The birds that live on Michigan State University's campus are constantly in close proximity to college students, causing them to have become accustomed to certain human interactions which delay their reactions to potential predators, lowering their chance of survival (Olsson et al. 2002). Whereas, the birds that inhabit Fenner Nature Center, in an off campus rural environment, are not constantly in close proximity to humans, thus they react more quickly to potential predators, such as humans (McFarland 1993). Studies have been done on this same topic involving different animals. One such study was done using squirrels observing the differences between two populations; one that were regularly exposed to humans versus another that lived in a more natural environment, with less human interaction and exposure (Mccleery 2009). The probable cause of some birds taking more risks versus birds that will be cautious could be the temperaments of the birds. Research shows that there may be a genetic framework that correlates to certain personality traits, such as risk-taking or being more likely to avoid harm (Budaev and Zhuikov 1998; Elliot and Thrash 2002).
     The avian and human populations of Michigan State University, an urban environment, tend to exhibit more risk taking behaviors than their rural counterparts because of exposure to stimuli repeatedly (Bradley et al. 1993; Fischer et al. 2003; Metcalf et al. 2000). An urban environment as defined in this experiment is any area in which more than 15,000 people live and even more travel through on a day-to-day basis. Michigan State University's campus houses around 15,195 students and has around 37,988 undergraduate students enrolled, and because of this it classifies as an urban environment. These "risk taking behaviors" can be defined as how long it takes for an organism to return to an area that which had previously been deemed unsafe, or a verbal outburst against another member of the population. This brashness of behavior, and ignorance of danger, can often be explained by habituation, an overall decrease in reactions to repeated stimuli (Bradley et al. 1993; Fischer et al. 2003; Metcalf et al. 2000). In these urban environments innovative ways of finding adequate resources and nesting areas are required, and to a certain extent this behavioral alteration can affect future physiology (Atwell et al. 2012); only organisms able utilize the new innovations will survive and pass on their genes. Some variation though, is due to innate boldness (Wilson et al. 1994), and genetic markers such as DAT1, DRD2 which affect serotonin pathways related to harm avoidance (Blumstein 2006; Cummings 2000). This enhanced risk taking ability, that arose at one point due to random genetic variation, that some birds have to ignore danger signals for a bit in order to try and obtain new resources, would normally lead to death of the specimen. In the more urban environment of Michigan State University though, this unique variation leads to the birds enhanced survival. This is because the staff of the university stock bird feeders around campus with various types of bird seed; the birds bold enough to fly out into an open area are rewarded with a continuous source of food all year, thus increasing their odds of survival. As result, the innately bolder birds pass on their genetic disposition for bold actions and aid in the habituation of the other birds by offering an example of how best to survive. Despite evidence of interspecific differences and habituation being a simple explanation for urban behavior, and there being extensive literature detailing intraspecific behavior in survival, few studies have addressed the former topics (Blumstein 2006; Evans et al. 2010).
     Certain genes, DAT1 and DRD2, have been associated with temperaments that exhibit risk taking behaviors, in humans. (Cummings 2000). The DAT1 and DRD2 genes that relate to harm avoidance in humans utilize serotonin pathways as a control mechanism to reduce dangerous behaviors (Cummings 2000). There is a study being done on a gene similar to the DAT1 and DRD2 in humans on birds. The serotonin pathways have 5-HT receptors that are complex in both birds and humans (Parent 1980). This can show the correlation between humans and birds and whether they exhibit harm avoidance behaviors or not. Based on this it is possible to see that there are similarities in the way the squirrels in Mccleery's study reacted, the rural squirrels being more likely to show harm avoidance behaviors than the squirrels that live in urban environments, and the way the birds of Michigan State University may react. The overall importance of investigating the effects Michigan State University has on the bird population, is to see if it creates adaptations with a negative impact on the bird's survival, causing them more harm in the long run.
     Many animal behavior studies have focused on observing how different organisms interact and have become accustomed to human interaction. In one such study, urban populations of birds, that resided in environments like college campuses, were compared to rural populations of birds that resided in open fields and forests (Evans et al. 2010). The purpose of this observational study was to understand how birds have adapted to the presence of humans, and have become more domesticated as a result. The research conducted in the Evans study also measured the FID, or distance that a human could be away from the bird before it would fly away to safety (Evans et al. 2010). If the birds got closer to a speaker, then it was assumed that the bird had a more aggressive or bolder response (Searcy et al. 2006). The methods from this study inspired the experiment that will be performed, which will show that urban populations of birds have slowly become more comfortable around humans altering their behavioral patterns and communication methods. Previous studies, that the Evans article methods were based on, have been done that examined how boldness or risk taking behaviors occur in response to human interactions and commotions (Blumstein et al. 2003; Blumstein 2006). This study focuses specifically in regards to visual communication and how the birds watch others before deciding if it was safe to return. This idea comes from how birds responded to and showed boldness when returning to a speaker (Nowicki et al. 2002). By observing how the birds of Michigan State University react to everyday human life compared to birds that live off campus, we predict that similar conclusions can be made, based on the previous studies.
     Adaptation is a significant aspect of natural animal behavior and communication. In this study, the relationship between Avian behavior and urban environments is examined. Factors such as noise pollution and public disturbance, play an important role in a bird's acclimation to what would normally be considered aversive stimuli within its habitat (Blumstein 2006). Areas with prominent human disturbance consist of species of birds that have dulled "fight or flight" responses to disruptive stimuli, reducing their natural anti-predator behaviors (Mccleery 2009). As a result, the Michigan State University birds will develop a bolder nature and take more risks, increasing exposure to predators, and potentially raising their mortality rates (Sih et al. 2003). The predicted result associated with this information is that the communication affiliated with this behavior will recur in future generations, affecting their ability to thrive. In order for the animals to survive in an urban area with different types of stimuli, it is crucial that the birds alter their behavior so that they increase their chances of survival (Evans et al. 2010). With this information, we hypothesize that the birds at Michigan State University will associate food and safety with the bird feeders, increasing the amount of risks taken and altering the natural order of the environment. This will result in fewer cautious birds that would normally have the best chances of survival, and create a new system of communication based on the new order of what is considered a danger.

Methods

Finalized by: Malcolm Davis

     Four types of observational periods will take place in order to track how a specific and very structured human environment affects communication signals within bird and human populations in regards to risk taking. Risk taking behaviors are to be defined as how long it takes for an organism to return to an area that which had previously been deemed unsafe in birds, or a verbal outburst against another member of the population in humans for the scope of this study. The first will be held on the campus of Michigan State University concerning the birds located at the feeders behind Holmes Hall. The second will concern the birds of Fenner Nature Park. These two observational periods involve collecting data for the birds behavior and establishing whether or not harm avoidance is exhibited. After these two trials, human testing of risk taking will be measured. Two trials will occur, one at Michigan State University regarding its student population, and another at Fenner Nature Park with the residents of East Lansing. These trials will be observing human behavioral responses to aversive stimuli to observe if habituation occurs to threats within an urban environment.
     The bird feeders that will be observed at Michigan State University, the first observational period, consists of an undisturbed feeder in an area without human activity which is maintained by the university outside of Holmes Hall that will serve as a control, and a disturbed feeder located in an area located within a central location surrounded by walking paths resulting in large amounts of human activity. Each feeder will be observed three days a week from 12:15 pm to 12:45 pm. The birds' responses will be measured in regards to three different sets of conditions; the first trial will be a control and the undisturbed feeder will be monitored, the second trial will consist of "normal" campus activity, a type of control for human interactions, in which the everyday behavior of the birds will be recorded at the disturbed feeder, and the third trial will contain of specific and obvious traces of human activity meant to disturb the peace and observing how drastically the birds behavior has been altered and how long it takes the birds to return to the feeder. "Normal" campus activity is what foot traffic happens around the feeders on a day to day basis without intervention from the experimenters. Examples of the intentional outbursts of activity are a loud phone call, clapping, or the bike racks being rattled. The behavior of the birds as they land at, when they leave, and how long it takes them to return to the feeders will be recorded via an iPhone camera. Afterwards, the footage will be reviewed and these specifics will be cataloged into a data table and compared to the notes of the researcher from that time period.
     The second observational period will take place at Fenner Nature Center and will consist of procedures nearly identical to that of the bird study that will take place at the Michigan State University feeders. To be consistent, the feeders will be observed three days a week, each time being from 12:15 - 12:45 pm, using the three different sets of conditions that were applied to the Michigan State feeders. The first trial will involve observing a control - a replicated undisturbed feeder - because there will not be a feeder that remains undisturbed. This will be the feeder that is in the most secluded area of Fenner Nature Center. The second trial will be identical to the trial that is to be performed at the Michigan State University bird feeders. The Fenner Nature Center trial will involve performing the "normal" activities that were listed previously, and the behavior of the birds in this environment will be also recorded. Lastly, intentional disturbance will be conducted on the feeder for trial three. The responses of the birds will be recorded via an iPhone camera and the specific behaviors of the birds will be documented in notes taken by the researchers.
     The same experiment will then be attempted on the human population of Michigan State University in much the same way. Three trials will occur; one a control at Holmes Hall cafe which has a steady stream of students and is quiet and is a low stress environment, the second on the Shaw Lane without any intervention by the researchers, and the third in which there will be intentional disturbances to the natural state of things of Shaw Lane; the intentional disturbance will be a biker traveling through busy sidewalks without regard for the flow of traffic. This will be to see in what ways the students of Michigan State University have habituated to "university life"; in essence to see how Michigan State University has altered their behavior.
     A similar experiment will then be done on a human population outside of Michigan State University. The site of the observations will occur at the Fenner Nature Center in the East Lansing area. There will be three sets of conditions observed, similar to the experiment on the humans of Michigan State University. The first trial will be the control, which will occur in the quietest area of the park where the researchers will observe people and take notes on their actions. The second trial will occur in a busier environment in the park where more people are located, a more central location where there is a lot of foot traffic. In this location the researchers will observe people's behaviors with no interventions. The final trial will include a disturbance created by a third party, such as riding a bicycle down a busy sidewalk, and the researchers will observe the reactions. The goal of this experiment was to understand the ways in which humans that live in a non-campus environment react to scenarios differently than those that live on Michigan State University's campus.
     After all the data has been collected the statistical significance of the data will be calculated. Because there are three variables that will be observed, the control, "normal" activity, and intentional disturbed activity, a one-way ANOVA test will be used within each population to prove statistical significance. If the p-value is less than or equal to the set significance level, the data is considered statistically significant; this is what will be used to gauge if the data is significant across the two populations, bird and human respectively. Each of the variables will be compared in singularity to its corresponding variable from the other population using a t-test for significance; i.e the control with birds at Michigan State University will be compared to the control for birds at Fenner Nature Center and this pattern will be followed with all variables both bird and human. The data will be normalized to midigate the influence of sample size discrepancies. The significance level, or alpha, for this study will be equal to 0.05, meaning that the probability of observing the differences seen in the data by chance is 5%.

Results

Finalized by: Jennifer Semaan

Michigan State University Birds

     We predict that the birds that inhabit Michigan State University will show more risk-taking behaviors in comparison to the birds of Fenner Nature Center (McDonnell et al. 1997). Risk taking behavior is defined as birds returning to the feeder quickly after intentional disruption. These results will be compared to a control, which will consist of everyday campus life and a control at the undisturbed feeder (Figure 1). This bar graph shows the time, in minutes, it takes for the birds of Michigan State University to return to the disturbed feeder when there is a disruptive stimulus. We predict that the birds of Michigan State University that are observed at the disturbed feeder will return to the feeder quicker than the birds of Fenner Nature Center, because the birds of Michigan State University have grown accustomed to living in an urban environment where there are constant disruptive behaviors performed by humans (McDonnell et al. 1997). We anticipate the birds of Fenner Nature Center will take more time to return to the feeder because they are not as exposed to human behaviors, and will thus exhibit harm avoidance defined as taking more time to return to the feeder after a potential threat, the disruptive human behaviors (McFarland 1993). There will be an ANOVA test run on the results in Figure 1 to detect the statistical significance of the data.

Fenner Nature Center Birds

     We predict that the subsequent birds, birds after a singular initial bird returns, returning to the Fenner Nature Center feeder will display increased harm avoidance behavior in comparison to the birds at Michigan State University because they are not accustomed to human activity (Mccleery 2009)(Figure 2). It is predicted that the consecutive birds will return to the feeder after receiving a signal from an initial bird that returns first. The harm avoidance behavior is defined as an interval of time taken for all birds to return to the feeder. The time taken for the consecutive birds to return to the feeder shows the relationship that avian communication plays between rural versus urban areas. The first birds return is predicted to have an effect on the behavior in the consecutive birds as a way to gauge the threat level of an area (Mccleery 2009). Birds that inhabit a rural environment exhibit what is considered 'normal' behavioral responses to aversive stimuli (Metcalf et al. 2000).

Michigan State University Humans

     We predict that the urban human population of Michigan State University will exhibit less harm avoidance behavior and will display more risk-taking behaviors in comparison to the rural human population outside of Michigan State University, because they have habituated to the nuances of campus (Bradley et al. 1993; Fischer et al. 2003) (Figure 3). The harm avoidance behavior will be measured by the number and type of reactions that occur in response to a stimulus. We predict that the humans of Michigan State University will not react to a biker speeding down the sidewalk because they consider it "normal" behavior on a college campus (Bradley et al. 1993); what is considered "normal" overtime is because of habituation (Bradley et al. 1993). This predicted reaction type shows that the humans living in Michigan State University's campus will not consider stimuli like a reckless biker as a dangerous stimulus, and will not seek to avoid it.

Fenner Nature Center Humans

     We predict that the humans observed at Fenner Nature Center will exhibit less risk-taking behavior than the humans observed at Michigan State University when exposed to the threatening stimuli of an unorganized biker, because the humans at Fenner Nature Center will will not know how to respond and shy from confrontation because they are not familiar with the experience which is common on campus (Bradley et al. 1993; Fischer et al. 2003). The risk taking behavior for this portion of the observational study will be considered a violent verbal outburst; this would be the observed human directly fronting the run-away biker with its outburst as a form of threat or warning. We predict that the humans of Fenner Nature Center will instead try to warn the biker calmly or be so startled they simply jump out of the way. This is because of how humans handle social confrontation and the breaking of social norms (Newell and Stutman 1988); the humans of Fenner Nature Center are not used to wild bikers and so feel their claims of the biker being a threat are legitimate, which most often leads to a quick and calm confrontation (Newell and Stutman 1988). The different types of response humans perform after the biker passes will be recorded and sorted into four categories and shown in a bar graph (Figure 4). These categories are violent verbal outburst, glaring, fleeing, and no response. The data will be collected over three days and then averaged. Whichever response receives the highest average will be considered as that populations, the Humans of Fenner Nature Center, social norm. An ANOVA test will be run on the data to determine the statistical significance of the data collected.


References


Finalized by: Alexis Tangalos

Atwell, J. W., G.C. Cardoso, D.J. Whittaker, S. Campbell-Nelson, K.W. Robertson, and E.D.      Ketterson. 2012. Boldness behavior and stress physiology in a novel urban environment      suggest rapid correlated evolutionary adaptation. Behavioral Ecology 23: 960-969.

Blumstein, D.T. 2003. Flight-initiation distance in birds is dependent on intruder starting      distance. Journal of Wildlife Management 4: 852-857.

Blumstein, D.T. 2006. Developing an evolutionary ecology of fear: how life history and      natural history traits affect disturbance tolerance in birds. Animal Behavior 71: 389-399.

Bradley, M. M., P.J. Lang, and B.N. Cuthbert. 1993. Emotion, novelty, and the startle reflex:      Habituation in humans. Behavioural Neuroscience 6: 970-980.

Budaev, S. V. and Zhuikov, A. Y. 1998. Avoidance learning and 'personality' in the guppy      (Poecilia reticulata). Journal of Comparative Psychology 112: 92-94.

Cummings, D. E., R. Gade-Andavolu, N. Gonzalez, S. Wu, D. Muhleman, H. Blake, M.B.      Mann, G. Dietz, G. Saucier, and J.P. MacMurray. 2000. A multivariate analysis of 59      candidate genes in personality traits: the temperament and character inventory. Clinical      Genetics 58: 375-385.

Elliot, A. J. and Thrash, T. M. 2002. Approach-avoidance motivation in personality: approach      and avoidance temperaments and goals. J. Personality Soc. Psychology 82: 804-818.

Evans, J., K. Boudreau, and J. Hyman. 2010. Behavioural Syndromes in Urban and Rural      Populations. Behavioral Ecology 23: 960-969.

Fischer, H., C. I. Wright, P. J. Whalen, S. C. McInerney, L. M. Shin, and S. L. Rauch. 2003.      Brain habituation during repeated exposure to fearful and neutral faces: A functional MRI      study. Brain Research Bulletin 5: 387-392.

McFarland, D. 1985. Animal behaviour: psychobiology, ethology and evolution. Animal      Behavior and Etiology 45: 576-579.

Mccleery, R. A. 2009. Changes in fox squirrel anti-predator behaviors across the urban-rural      gradient. Landscape Ecology 24: 483-493.

McDonnell, M.J., S.T.A. Pickett, P. Groffman, P. Bohlen, R. V. Pouyat, W. C. Zipperer, R. W.      Parmelee, M. M. Carreiro, and K. Medley. 1997. Ecosystem processes along an urban-to-      rural gradient. Urban Ecosystems 1: 21-36.

Metcalf, B. M., S.J.J.F. Davis, and P.G. Ladd. 2000. Adaptation of Behaviour by Two Bird      Species as a Result of Habituation to Humans. Australian Bird Watcher 18: 306-312.

Newell, S. and Stutman, R.K. 1988. The Social Confrontation Episode. Communication      Monographs 3: 266-285.

Nowiki, S., W.A. Seary, T. Krueger, and M. Hughes. 2002. Individual variation in response to      simulated territorial challenge among territory-holding song sparrows. Avian Biology 33:      253-259.

Osslon, O., J.S. Brown, and H.G. Smith. 2002. Long- and short-term state-dependent foraging      under predation risk: an indication of habitat quality. Animal Behavior 65: 981-989.

Parent, A. 1980. Comparative anatomy of the Serotoninergic Systems. Journal de Physioloige      77: 147-156.

Searcy, W.A, R. C. Anderson, and S. Nowicki. 2006. Bird song as a signal of aggressive intent.      Behavioral Ecology and Sociobiology 2: 234-241.

Sih, A., L.B. Kats, and E.F. Maurer. 2003. Behavioural correlations across situations and the      evolution of antipredator behaviour in a sunfish-salamander system. Animal Behavior 65:      29-44.

Wilson, D. S., A.B. Clark, K. Coleman, and T. Dearstyne. 1994. Shyness and Boldness in      humans and other animals. Trends in Ecology and Evolution 9: 442-446.

Figures


Finalized By: Sabrina Bronni
msu bird time photo msubird time_zpsdp1xepud.png

     Figure 1. Time Taken for Subsequent Birds of Michigan State University to Return after Intentional Stimuli is presented. This bar graph shows the time, in seconds, it takes for the subsequent birds of Michigan State University to return to the disturbed feeder after there is a disruptive stimuli and an initial bird has returned. The x-axis shows the trial numbers in which the intentional disturbance, a person clapping till all the birds have been scared from the feeder, is presented and the y-axis shows the amount of time taken for the birds to return. The time taken for the subsequent bird to return to the feeder after the intentional disturbance was observed to be 37 seconds for Trial 1, 27 seconds for Trial 2, and 33 seconds for Trial 3. The percent error for each trial has been calculated and is represented by the error bars. Although percent error is shown, statistical significance has not been performed. An ANOVA test will be conducted to allow for comparison between the 3 trials. From this, we predict that the birds at Michigan State University will have a significantly faster return time to the feeder (Evans et al. 2010; McDonnell et al. 1997).



time data photo RealRawTimeGraph_zpsviqkvopj.png

     Figure 2. Comparison of Number of Consecutive Birds that Returned to the Feeder after Intentional Stimuli at Michigan State University and the Fenner Nature Center. Each bar on the x axis represents each trial observed at Fenner Nature Center and at Michigan State University. The y axis represents the time taken for consecutive Birds at both Fenner Nature Center and Michigan State University that returned to the feeder after the 'Intentional Disturbance’ is presented. The intentional disturbance is defined as clapping loudly at the feeders. The labeling of the birds as 'subsequent' refers to the observation that the birds returned to the feeder after an initial bird returns, providing the assumption that it is safe for other birds to return. The average time for the subsequent birds at Michigan State University to return to the feeder is calculated to 32.33 seconds. Fenner Nature Center had an average time of 71.33 seconds. Although the graph displays raw data, no statistical tests have been conducted. A T-test will be used to calculate significance across the two location, and an ANOVA test will be used to calculate significance within populations. Based on the data shown, it is predicted that the birds at Michigan State University will have a significantly faster return time than the birds at Fenner Nature Center because they have adapted to their habitats and do not see aversive stimuli as significantly threating (Metcalf et al. 2000).



intentional response photo RealIntentionalResponsegraph_zpshjqbvduy.png

     Figure 3. Total Number of Responses to threatening Stimuli by the Humans at Michigan State University and Michigan State University. The bar graph above represents the raw data collected at both locations. The x-axis displays the number of responses for each type of response. The four different observed response types are no response, fleeing, glaring, and violent verbal outbursts. No response is defined as people ignoring the frightening stimulus. Glaring is defined as an individual narrowing their eyes at the biker. The fleeing response is described as moving out of the way of the bike. Lastly, the violent verbal outbursts is defined as yelling or shouting at the biker. Based on the raw data, Michigan State University has a larger number of individuals exhibiting no response and glaring whereas Fenner Nature Center has a larger number of Individuals fleeing from the stimuli. Percent error has been calculated, shown by the error bars, but the data has not been normalized. The data must be normalized in order to account for sample size variation. The sample size variation is due to the fact that the sample size at Fenner Nature Center is so much smaller that the sample size at Michigan State. When comparing across the two different locations, a T-test will be used. An ANOVA test will be used when comparing the trials within each of the two locations. Based on the collected data we predict that there will be statistical significance for all responses, both within and across the two locations (Bradley et al. 1993; Fischer et al.2003).


Social Norm photo Real Social Norm_zps9webuhkx.png

     Figure 4. Average of Responses to Threatening Stimuli by the Humans of Fenner Nature Center and Michigan State University. The response of the humans of both Michigan State University and Fenner Nature Center to the threatening stimuli of a wild biker was recorded and averaged for the data collected. The x axis represents the four response categories;no response, fleeing, glaring, and violent verbal outburst. The y axis represents the average number of individuals that respond in each category. No response will be ignoring the stimuli, glaring will be considered as a narrowing of the eyes directed at the biker, fleeing will be considered jumping away from the bike, and violent verbal outbursts will be considered shouts at the biker. After collecting the data, the number of responses was averaged. The social norm at Michigan State University has been observed as exhibiting no response when presented with threatening stimuli. Fenner nature center has a social norm of fleeing when presented with a threatening stimuli. As of now, there is no error calculated, but it is expected due to the fact that these responses are based on judgement. Statistical significance has not been established, but is also expected. A T-test will be used to compare between each response type at each location. It is predicted that fleeing will be the most popular response because the humans of Fenner Nature Center will not be used to the biker and will jump out of the way to avoid harm and they will be too startled to confront the situation (Bradley et al. 1993; Fischer et al. 2003; Newell and Stutman 1988).


     Figure 5. Peace J.A.M.S Documentary Video. This is a documentary covering everything currently discovered through this observational study along with background information from the sources within the references section. It contains clips of the researchers talking, both the Michigan State University and Fenner Nature Center feeders, and clips of the biker and Holmes Hall cafeteria with voice overs. It ends with a researcher discussing the purpose of the experiment and some of the results currently discovered.

Appendix