Holly Fuong
Ph.D. 2021
Dissertation: Social animals detecting danger: how social relations influence anti-predator behavior in a noisy forest
The risk of death by predation has been a
major driver of group living in many prey animals. Animals must adapt
to temporal and spatial variation in predation risk and would benefit
from using relevant and reliable sources of information both from
conspecifics and heterospecifics to better learn about danger. Research
on the effects of group living on antipredator strategy has focused
largely on group size. However, sociality is often more complex than
simple amalgamations of individuals. Those living in groups are likely
exposed to unequal levels of predation risk; some are exposed to more
danger than others because of factors related to their age, sex, and
spatial or social positioning. An individual’s antipredator strategy
should reflect its perceived safety levels.
I studied antipredator strategies in blue monkeys (Cercopithecus mitis stuhlmanni)
in the Kakamega Forest, Kenya. Blue monkeys are arboreal guenons that
live in matrilineally-based social groups and form differentiated
social relationships. These social relationships could affect how
monkeys respond to variable predation risk. Blue monkeys live in dense,
biodiverse rain forests and are preyed upon by both aerial and
terrestrial predators. They have a well-developed acoustic
communication repertoire and have been known to associate with other
primates to reduce predation risk (Cords 1987). I conducted five
playback experiments and two sets of observational studies, and used
data gathered on social interactions among adult females to further our
understanding of how group living affects antipredator strategies. I
also used 14 years of social interaction data to explore the
heritability of social tendencies.
In the first chapter, I present a
comprehensive literature review of the connections between group living
and antipredator behavior. I describe the effects of group size on
antipredator behavior and how research on sociality has shifted towards
focusing on individuals’ specific relationships and social
connectivity. I then describe several ways in which social connectivity
has been shown to influence antipredator behavior. I conclude with
future directions and then introduce the dissertation.
In the second chapter, I focus on
heterospecific eavesdropping. I identified the extent to which blue
monkey adult females respond to playbacks of alarm and social calls of
two syntopic non-predatory bird species—black-faced rufous warblers
(Bathmocercus rufus) and joyful greenbuls (Chlorocichla laetissima).
Blue monkeys responded differentially depending on both call type and
species. I then evaluated differential responses to conspecific and
heterospecific callers, hypothesizing that conspecific signals would
trigger stronger anti-predator responses because conspecifics are more
relevant signals of risk. I conducted a playback experiment in which
adult females were presented simultaneously with one alarm or social
call from both conspecifics and warblers (4 combinations of alarm and
social calls), or ambient rain forest sound (control). Subjects did not
differentiate their responses to simultaneous calls according to the
type of playback stimulus. These findings suggest that blue monkeys do
not differentiate their responses to alarm calls according to caller
relevance. Heterogeneous results among different response variables
also highlight the importance of examining multiple modes of
antipredator behavior.
Next, I examine how an individual’s social
connectivity influences its antipredator strategy, hypothesizing that
more socially connected individuals would benefit from the proximity of
more and closely bonded groupmates in enhancing predator avoidance. In
Chapter 3, I evaluate the effects of social connectivity on acute
antipredator responses, antipredator vigilance, and responses to
signals related to various levels of predator-related threat. I first
assessed how social connectivity affects the rate at which adult
females exhibit acute antipredator responses (such as diving down in
trees, climbing up trees, or alarm calling) and the proportion of
responses that are major (lasting >30 s), statistically controlling
for age, the presence of an infant, and 2-month “seasons”. I predicted
that more socially connected individuals would exhibit less frequent
acute antipredator responses because they would be better-informed
about risk and therefore would exhibit fewer false alarms. I For the
same reasons, I also predicted that they would exhibit more major (vs.
minor) responses because false alarms are more likely to involve
shorter responses (Cords 1987). Contrary to predictions, however, more
closely connected individuals exhibited higher rates of acute
antipredator responses, which might reflect their enhanced ability to
learn about danger from surrounding groupmates, allowing them to detect
more potential threats. There was no evidence that social connectivity
was associated with the proportion of responses that lasted >30 s. I
also found that the rate of acute antipredator responses and the
proportion of responses that lasted >30 s varied with season. I then
conducted 90-s focal vigilance follows, to assess how long females
exhibit antipredator vigilance after controlling for other social and
microhabitat factors (e.g., surrounding vegetation density), which can
influence conspecific monitoring and exposure to potential predators. I
predicted that more well-connected individuals would exhibit lower
levels of antipredator vigilance in the absence of any imminent threats
and after controlling for other social and spatial factors. More
closely connected individuals who were in the spatial center of their
social group did spend less time vigilant, but social connectivity was
not associated with vigilance times when subjects were at the group’s
edge, where exposure to predators and thus predation risk should be
highest and antipredator vigilance should generally be higher. In the
spatial center of the group, more closely connected individuals should
be in a better position to observe their social partners’ antipredator
behavior. Microhabitat also influenced antipredator vigilance in
multiple ways, which highlights the spatial variation of perceived
predation risk in a complex environment. Lastly, I conducted a playback
experiment where I examined responses to signals from conspecifics and
heterospecifics that are associated with different levels of threat. I
predicted that more poorly connected individuals would respond strongly
to all signals that might be associated with predators because they
must identify personally whether danger is real, whereas more
well-connected individuals would have more differentiated responses
because they should be near social partners more frequently and can
rely on their partners’ antipredator reactions to assess risk levels.
However, although subjects did respond more to direct cues of the
predator’s presence (its own calls) than to indirect cues of its
presence (alarm calls by conspecifics and heterospecifics), there was
no evidence that social connectivity affected responses to playbacks.
As expected, stimulus type did affect responses—calls from predators
(vs. alarm calls or social calls from non-predators) elicited increased
looking responses from subjects, which suggests that stimuli that
directly signal predator presence will elicit antipredator behavior
regardless of the listener’s social connectivity. Overall, social
connectivity seems to play a limited role in blue monkeys’ antipredator
strategy but there was some evidence that more well-connected
individuals were less vigilant when surrounded by groupmates.
The ability to distinguish alarm calls by
individual callers has not been well-studied, but animals might benefit
from making such distinctions if callers vary in how reliably they
signal danger. For decades, researchers have tested whether animals can
discriminate callers using the habituation-dishabituation paradigm.
After habituating subjects by repeatedly presenting calls of
one individual, A, they examine whether subjects dishabituate when they
hear the calls of a different individual, B (test stimulus). In Chapter
4, I first review studies that used this paradigm to evaluate whether
animals discriminate between conspecific callers and then report on two
playback experiments which tested whether wild blue monkeys
(Cercopithecus mitis) are capable of such discrimination. My review
revealed much methodological variation, particularly in the habituation
phase and criteria, statistical analysis, and controls. In experiments,
I contrasted two methods of habituation, either presenting a fixed
number of stimuli (set after pilot observations) or evaluating
responses during the series before progressing to the test. Afterwards,
I conducted Wilcoxon signed-rank tests to assess habituation
statistically. In the first experiment where I played back a fixed
number and rate of calls, it was statistically unclear whether subjects
habituated to caller A, despite preliminary observations and similar
studies that suggested that the experimental design would be
appropriate. Because there was not strong evidence that subjects
habituated, I did not evaluate statistically whether subjects
differentiated between callers in the full dataset. However, in the
second experiment where I assessed habituation during the trial,
subjects did habituate to caller A and there was weak support that they
dishabituated to caller B, which suggests that caller discrimination
may occur. From my experiences, I propose an improved design for
studies using the habituation-dishabituation paradigm.
Lastly, I explore the mechanisms that drive
phenotypic variation in social tendencies (and in turn, social
connectivity) in adult females. For natural selection to occur, there
must be variation in traits, differentiated fitness benefits based on
phenotypes, and heredity or a genetic basis underlying phenotypic
variation. The previous chapters highlight the variation in and some of
the benefits of social connectivity. In Chapter 5, I conducted an
exploratory analysis to examine what factors account for phenotypic
variance. Using animal models, I found that bothenvironmental and
additive genetic variance accounted for some of the phenotypic variance
seen in traits associated with social tendencies (using social
connectivity as a proxy). Variance in the social environment (i.e.,
environmental variance) played a large role in shaping observed
phenotypic variation in social connectivity. However, all six of the
social network measures examined were weakly heritable, which suggests
that there is also a genetic basis for behavioral variation, allowing
selection to occur.
This dissertation emphasizes the importance of
examining both antipredator behavior and sociality using multiple
experiments, observations, and measures, while also considering the
importance of study species and habitat complexity. The relationship
between antipredator behavior and social connectivity is not
straightforward and can vary greatly between study systems. Although
many of my predictions were not supported, I did find evidence that
blue monkeys are receptive to heterospecifics, vary their acute
antipredator responses and vigilance based on social relationships with
conspecifics, adjust their antipredator vigilance according to spatial
positioning, and potentially discriminate between alarm callers. The
findings presented here expand our knowledge of how animals learn about
predation risk by being attentive to conspecifics and heterospecifics.
Publications
Fuong, H., Maldonado-Chaparro, A. & Blumstein, D.T.
2015. Are social attributes associated with alarm calling propensity?
Behavioral Ecology 26: 587-592.
Fuong, H., Keeley, K.N., Bulut, Y. & Blumstein, D.T.
2014. Heterospecific alarm call eavesdropping in non-vocal, white-bellied, copper-striped
skinks (Emoia cyanura).
Animal Behaviour 95: 129-135.