Dyer Lab: Integrative Behavioral Biology
Research Interests
Overview
I am interested
in mechanisms, function, and phylogeny of animal behavior. Behavior
fascinates me in part because of the important role that it plays in mediating
the interactions of animals with their environment. Furthermore,
as one who is interested in how organisms work and why they have the features
that they do, I am fascinated by the flexibility and subtlety of behavioral
adaptations, and by the intellectual and methodological challenges that
arise in studying them. The fitness-relevant design features of behavioral
traits often are hard to specify in comparison with those of morphological
or physiological traits. The mysteries of behavior can reveal themselves,
however, through a blend of careful experimental manipulation and comparative
observations.
I have worked primarily with honey bees (Apis), long an important
model system for studies of learning, visual behavior, communication, and
sociality. Bees remain highly attractive as model organisms for both
mechanistic and evolutionary approaches to behavior. Their behavior
is amenable to experimental manipulations designed to elucidate underlying
mechanisms that are difficult to study with more direct neuroscientific
techniques. Also, comparative studies of different Apis species,
which I have pursued in India and Thailand, allow insights into both evolutionary
and mechanistic questions that are not possible with a single species.
Through my own work, I have experienced the truth of Karl von Frisch's
characterization of the honey bee as a "magic well" of scientific discovery:
"the more you draw from it, the more there is to draw." This aphorism
could apply to any well-studied model organism. What makes it true
for bees is the intrinsic fascination of unraveling their unique behavioral
capacities as well as the potential for exploring issues that transcend
the biology of the organism.
My research interests all concern behaviors involved in the use of space--orientation,
navigation, communication (of spatial locations), and foraging. These
interests are described below. Bibliographic citations refer to papers
listed here.
Specific Topics
Navigation and Spatial
Cognition
Most animals routinely face the challenge of orienting themselves in
space, and studies of spatial orientation have long played an important
role in psychology and behavioral biology. Honey bees are especially
intriguing because they navigate over enormous distances with astonishing
flexibility, though equipped with vision far feebler and brains far smaller
than ours. Foraging honey bees travel up to 10 km from their nest
in search of food, and so they frequently face the problem of steering
a course to a familiar goal (e.g., a feeding site or the nest) that is
not directly in view. Solving this problem requires the animal to
use environmental features detectable at the starting point and along the
way, which in turn requires that it be informed of the spatial relationship
between these features and the route to the unseen goal. For insects
and many vertebrates, landmarks and celestial
cues (the sun and patterns of polarized sky light) provide the most
important sources of navigational information. A major focus of my
research in recent years has been on what bees learn about these two navigational
references and how they learn it (reviewed by Dyer 1994, 1996). The
work has mainly addressed questions about the sensory and learning mechanisms
underlying the behavior. However, the results have also led to new
perspectives on the adaptive design of these mechanisms.
Landmarks
An ability to use landmarks for long-distance navigation implies that
the animal can link together visual images recorded in successively encountered
parts of the terrain. How faithfully does the insect's spatial memory
represent the geometrical relationships among routes that the bee has traveled?
About 10 years ago, the flexibility with which honey bees and other insects
orient to familiar landmarks led James Gould to suggest that the underlying
spatial representation approximates the computational sophistication of
human mental maps, and confers upon the bee a human-like ability to calculate
novel shortcut routes among separately visited sites. In experiments
designed to test this hypothesis, however, I found that bees orienting
to landmarks are constrained to follow routes along which they can see
familiar sequences of landmarks. Thus, at best, they store one or
more "route maps" in memory, and do not encode the spatial relationships
among separately traveled routes (Dyer 1991a).
In other experiments I have investigated the flexibility with which
bees can use these route maps. For example, bees can compensate for
displacements from a familiar route, adjusting their response to familiar
landmarks seen from a new vantage point, and responding appropriately to
familiar landmarks encountered in an unfamiliar context (Dyer et al. 1993;
Dyer submitted). Also bees that change nesting sites with a reproductive
swarm reorient quickly to a new nest site, but remember how to get to feeding
sites they have visited from the old nest (Dyer 1993a); they also remember
where the old nest is, and can return there if deprived of the new nest
(Robinson and Dyer 1993). Thus, they rapidly reorganize their responses
to familiar landmarks, but retain their ability to use them in the original
way.
The experiments discussed so far have all dealt with the "contents"
of spatial memory in thoroughly experienced bees. An exciting line
of work being pursued by one of my former graduate students, Elizabeth
Capaldi, considers the acquisition of spatial memory by naive bees.
Her experiments examine what young bees learn about landmarks in their
environment during the orientation flights that they do prior to beginning
their lives as foragers. During orientation flights, which are also
performed by experienced bees that have moved with their colony to a new
terrain, bees explore the surrounding environment for only 5-10 min.
As an assay of landmark learning, we study the homing ability of bees that
have been displaced from the nest after a single orientation flight.
From release sites up to 150 m away, bees depart directly toward the nest
even though it is not in view. Thus, during their brief exploration
of the environment, the bees evidently started to assemble route maps extending
modest distances from the nest.
Go to:
Celestial cues
The sun has crossed the sky roughly 200 billion times since bilaterally
symmetrical animals arose on earth, so it is hardly surprising that many
diverse creatures have evolved the ability to use this highly reliable
feature of the environment for orientation. What is intriguing, however,
is that many animals, including honey bees, learn the pattern of solar
movement relative to earth-bound features, which allows them to use the
sun as a true compass. Sun compensation entails integrating visual
information about the sun's changing direction with temporal information
from the circadian pacemaker. In my Ph.D. work I showed that bees
learn the sun's course in relation to landmarks seen during the flight.
They can use their memory of this relationship to perform their communicative
dances when they have flown under a cloud cover (Dyer and Gould 1981; Dyer
1987a). In Apis mellifera, dances are normally performed on
the vertical combs in the darkness of the nest. The dancer indicates
the direction of food relative to the sun in the orientation of her body
relative to gravity. On cloudy days, a bee determines her flight
direction relative to the sun by retrieving a time-linked memory of the
sun's position relative to landmarks seen during
the flight.
In studies with an Asian honey bee, Apis florea (Dyer 1985a),
I found that dancers could also learn the sun's course relative to a second
set of landmarks, those visible while dancing on the nest. This species
nests in the open rather than in enclosed cavities, and dances are normally
oriented directly to celestial cues. Dancers in this species cannot use
gravity, and so the ability to orient dances to landmarks probably plays
a crucial role in their communication system. Initially, I thought
that this ability was restricted to this species, but Elizabeth Capaldi
and I (1995) recently discovered that A. mellifera can also use landmarks
as a reference for dance communication (although it should rarely need
to use this ability). This discovery opens the way for experiments
using the dance to explore the sensory and learning mechanisms underlying
orientation to landmarks, just as it has long been used to study orientation
to celestial cues.
In work with another former graduate student, Jeffrey Dickinson (Dyer
and Dickinson 1994, 1996; Dickinson and Dyer 1996), I have explored an
astonishing feature of sun-compass learning that was first described in
the 1950s: animals that have been exposed only to a portion of the
sun's course behave as if they can estimate its position at times of day
(and night; Dyer 1985b) when they have never seen it. We designed
an experiment to test various computational models that had been proposed
to account for this ability. We observed the dances of partially
experienced bees that flew to a familiar feeding site at times of day when
they had never seen the sun. The sky was cloudy during the experiment,
so the bees were forced to rely upon an estimate of its position rather
than a directly measured or previously memorized position. Our data
led us to reject all of the previous models. Each had predicted that
the bees should estimate unknown positions of the sun by fitting a specific
linear function to the set of time-linked positions that they had experienced.
Our partially experienced bees seemed to be innately informed about the
actual non-linear pattern of the sun's azimuthal movement over time (specifically,
the slow rate of change in the morning and afternoon and the rapid rate
of change at midday). The innate sun-azimuth function initially only
approximates the actual pattern of solar movement, but becomes more accurate
as bees obtain additional flight experience.
The bee's ability to estimate unknown portions of the sun's course raises
questions about how the bee's brain integrates spatial and temporal information,
and how individually acquired information is integrated with innately specified
information. We have begun to explore various new modeling approaches,
including connectionist neural networks, to understand this phenomenon
(Dickinson and Dyer 1996). One insight of this work has been that
the bee's innate representation of the sun's course may have been designed
to allow rapid learning of the actual pattern of solar movement at the
season and latitude where they find themselves living.
Go to:
Sequential Information Gathering in Machines and
Animals (SIGMA)
For the past 40 years or so, computer scientists have strived to endow
machines with an "artificial intelligence" approaching the natural intelligence
of organisms. In spite of all this effort, it remains clear that organisms
far surpass machines in the flexibility and fluidity of their responses
to the environment. Recently I have begun a collaboration with a psychologist
(John Henderson) and a computer scientist (Sridhar Mahadevan) to study
decision-making in three model systems: insects, humans and robots. Our
aim is investigate general principles of decision-making, and thereby to
gain insights both into the biology of decision-making in organisms and
into how decision-making algorithms used in machines might be made more
flexible. The Power Point presentation available at the link below gives
an overview of the intriguing research question raised by the problem of
sequential decision-making. More details about this collaborative, interdisciplinary
research program can be found on the SIGMA
Lab and the MSU IGERT Program
web pages.
Power Point
presentation on Sequential Decision Making in Cognitive Science
Evolution of Dance Communication and Visual Orientation
Through comparative studies of three Asian Apis species plus
A.
mellifera, I have studied the evolutionary history and adaptive design
of the dance language, which successful foragers use to communicate the
location of food. By taking comparative study of this particularly
tractable behavior to the deepest level possible, I hope to expose both
the potentialities and the limitations of phylogenetic analyses of behavioral
evolution. My thesis work in India challenged previous suggestions that
the dances of different modern species reflect a historical progression
in the complexity of the bees' direction code. I found instead a
deep dichotomy between A. florea, the species previously thought
to represent the primitive state, and the other Apis species (Dyer 1985a;
in prep. a). Given the phylogenetic relationships among the species,
it is now ambiguous whether the distinctive elements of A. florea's
dance should be viewed as derived rather than ancestral (Dyer 1991b).
In other work in Thailand (Dyer and Seeley 1991a), I have studied
the adaptive design of the distance code of the dance language, specifically
focusing on interspecific differences known as "dialects."
We found, in contrast to the traditional view, that interspecific similarities
and differences could not be explained by similarities or differences in
flight range or habitat. Thus, either there is no relationship between
dialect and these ecological variables, or the relationship is more
subtle than was previously supposed.
Another project that I hope to develop in the future is an evolutionary
study of the structural and physiological bases of visual resolution and
sensitivity in the bees' compound eye. This project would build upon
my discovery (Dyer 1985b) that Apis dorsata can forage (and dance)
by moonlight as well as by daylight. Such visual flexibility is unknown
in the other Apis species and is exceedingly rare in insects generally
(insects are usually either diurnal or nocturnal, but not both).
By studying correlations between behavior and eye structure in a phylogenetic
context, I hope to understand how a common visual ground plan can
(or cannot) be modified in a group of closely related insects.
Go to:
HOME
Comparative Ecology: Foraging, Energetics,
and Pollination Biology
When I originally learned about the Asian honey bees, I became intrigued
by the differences among the species in worker body size (the largest is
5 times the mass of the smallest), in colony size (ranging from 7,000 to
40,000) and in nest architecture (some species nest in enclosed cavities
as does the familiar European honey bee Apis mellifera; others nest
in the open on combs protected by a blanket of worker bees). I expected
these differences to have major implications for the energetic economy
of workers and colonies, and perhaps to shed light on the evolutionary
forces that shaped the differences.
During my post-doctoral work with Thomas Seeley (Dyer and Seeley 1987,
1991a,b), I carried out field studies in Thailand comparing worker physiology
and colony organization in three Asian honey bee species with the western
honey bee Apis mellifera. We had assumed that the scaling
of physiological traits (e.g., metabolic rate, body temperature, flight
speed, flight range) with size would impose important constraints on the
performance of workers, and hence on the acquisition and use of resources
by colonies. We found instead that the scaling relationships
themselves diverge among different species in a way that is not correlated
with size. Two of the species have relatively high-powered, high-tempo
workers, and two have relatively low-powered, low-tempo workers.
Thus, normally robust scaling relationships appear to have been modified
within the genus Apis, or at least have not imposed a strict constraint
on worker physiology. Furthermore, we found that worker energetic
performance correlates with nesting behavior: the high-tempo bees
nest in enclosed cavities and the low-tempo bees nest in the open.
We proposed that honey bees as a group have evolved two divergent adaptive
syndromes associated with the differing demands that open-nesting and cavity-nesting
place on colony demography. These divergent syndromes and their functional
significance would have remained hidden without both a comparative perspective
and careful studies of worker biology.
A graduate student, Puja Batra, has begun to move beyond studies of
the bees themselves to consider their impact on the plants that they pollinate.
According to a study by David Roubik of the Smithsonian Tropical Research
Institute, the 3-4 species of honey bees found in any given locality probably
have a disproportionate effect on the transfer of pollen. This may
be because of traits that result from the extraordinarily efficiency with
which the dance language allows foragers to recruit their nestmates to
food: very large flight ranges, large colony sizes, high densities
of colonies. Conceivably, A. dorsata's unusual ability to
forage during both night and day further enhances its effect on plant reproduction.
Puja is interested in the implications of these behavioral abilities for
forest conservation. On the one hand, some plant populations in Asia
may be more dependent on this one small but dominant group of insect pollinators
than is commonly the case in neotropical forests, and hence more vulnerable
should the bee populations decline through disease or human exploitation.
On the other hand, the large foraging ranges of honey bee colonies, combined
with the flexibility of their nesting behavior, may mitigate the effects
of forest fragmentation on plant reproduction, at least in comparison with
the neotropics, where the limited flight range and narrow nesting preferences
of many pollinators may reproductively doom trees in isolated forest patches.
Go to:
HOME