AMER. ZOOL.. 18:765-778(1978).
Aggressive Social Organization in Nectarivorous Birds
LARRY L. WOLF
Department of Biology, Syracuse University,
Syracuse, New York 13210
SYNOPSIS. I argue that a net benefit model of aggressive social organization is consonant
with observed variation between territorial and dominance systems. For nectarivores net
benefits are associated with obtaining nectar. Costs are time and energy associated with
aggression and possible risks of injury. The fitness criterion probably varies across situations and may be long or short-term. An important problem for behaviorists is to understand the position in a time hierarchy at which particular social interactions are important.
INTRODUCTION
Many organisms use limited resources, or
resources that vary in quality. Thus, competition often is an important component
of interactions within and between species.
Competitive interactions can take several
forms, generally referred to as exploitative
and interference (Miller, 1967, 1969).
Exploitative competition results from use
of resources by other individuals; interference competition involves preventing
other individuals from gaining access to
the resources. The two forms of competition are often contrasted with an intuitive
model that suggests individuals normally
experiencing unpredictable levels or high
levels of available resources will be exploitation competitors while individuals experiencing resource limitation will be interference competitors (Pianka, 1970; Gill,
1974).
Nectarivorous birds exhibit both types of
competitive interactions in feeding situations with the type of interaction varying
intraspecifically at different times (Gill and
Wolf, 1975; Wolf, 1975; Feinsinger and
Colwell, 1978; Gill, 1978). The variation
may occur between seasons (Stiles, 1973),
between years (Carpenter and MacMillen
1976a), within a season across days (Wolf
and Gill, in preparation), or even within
days (Gill and Wolf, 1975). This flexibility
of competitive interaction and the ease of
studying nectar feeding birds in the wild
makes them ideal candidates for examining the determinants of the overt character
of competitive interactions.
FORMS OF AGGRESSIVE SOCIAL ORGANIZATION
Both types of competitive interaction
may select for aggression (Brown, 1964)
although the spatial and temporal characteristics may vary between types. For
nectar-feeding birds the first question in
any particular situation is whether to be
aggressive or not and if aggressive what
form, length, and timing of aggression to
employ. Nectarivores show three general
types of aggressive interactions in relation
to their food that differ primarily in spatial
fixation, resource orientation, and distance
from a reference point at which the aggression is initiated (Fig. 1). These have
been termed territoriality, dominance, and
individual distance. As with most categorizations this division subverts the essential
continuity of the three types.
Individual distance is primarily short
distance spacing behavior that maintains
an exclusive area, the individual space,
J. Bradbury, J. Brown, F. R. Hainsworth, F. B. Gill, around the individual. It is individualand I. Bernstein provided helpful comments on an oriented and reflects the willingness of the
earlier draft of this paper. T. Mercier helped with
bibliographic and technical details. Supported in part individual to allow intruders closer than
by a grant from NSF (DEB75/07670 AO1) and by some specified distance. Although it often
Syracuse University.
is considered to be species specific (Wilson,
765
766
LARRY L. WOLF
NON-SPATIAL RESOURCE-ORIENTED
FIG. 1. Schematic representation of the relationships
among territoriality, dominance interactions and individual distance. The importance of each variable is
represented by distance for that side of the triangle.
For example, both dominance and territoriality are
resource oriented and are close to that side of the
triangle. The cross-hatched areas are intermediate
types of behavior that would be hard to categorize.
1975) the area defended may vary seasonally, and with the sex and direction of
approach of the intruder (Mailer, 1956a;
Me Bride el al., 1963). A large individual
distance that is spatially fixed could be
called a territory. Variable expression of
the individual distance especially in the
vicinity of different resources might be
considered a form of dominance interaction rather than an inviolate individual
distance. The essential distinction is that
individual distance is individual centered,
moves with the individual, and has limited
relation to resource distribution. However,
it would be interesting to see if individual
distance varied as a function of resource
proximity.
It the individual distance became more
and more resource oriented it would be
increasingly difficult to discriminate it
from dominance interactions. In chicken
flocks the peck order (= dominance
hierarchy) is largely related to control of
space by an individual (McBride, 1968). In
this sense, the resource for which the aggression is manifested is the space around
the individual so that dominance and individual distance are closely intertwined conceptually.
Dominance is the potential ability of the
individual to control access to resources,
including space, and it can specify situations where there is a probability of aggressive encounters. Dominance is resource
oriented and hence spatially variable. The
distance to which the second individual is
allowed to approach can vary more for
dominance interactions than for territoriality or for individual distance.
As the outcomes of dominance encounters become predictable they approach a
dominance hierarchy. As they become less
predictable the hierarchy breaks clown, but
the hierarchy of which individuals have
potential access to resources may persist. It
is important to uncouple the underlying
conceptual base from the overt behavioral
interactions that are potentially an outcome of the stimulus situation. The essence of a dominance hierarchy is that it is
a formalized attempt by the investigator to
rank individuals in relation to their priority of access to resources that may continually shift in location (Syme, 1974; Richards.
1974).
Dominance has been called an intervening variable since it can be used to classify
some predictable interaction between the
internal state of the organism, its external
environment, and its aggressive interactions (Hinde, 1970; Richards, 1974).
Hinde argues that an intervening variable
is useful only when it is correlated with
measured overt behavior responses. As the
direct relation between a stimulus and response are uncoupled the correlation deteriorates and dominance presumably
loses utility as an intervening variable
(Syme, 1974).
Multiple inputs may inlluence the probability of a particular behavior pattern.
Thus, aggression (or its converse, subordination; Rowell, 1966) is only one possibleresponse in many competitive situations
and the degree to which the response is
controlled by a multibranched hierarchy
(Dawkins, 1976) reduces the correlation
between stimulus and response. Just as
knowing whether a bird is hungry may be
insufficient to predict a response when
food and water are ottered simultaneously
(Nibiy, 1975), so predicting the outcome ot
AGGRESSIVE SOCIAL ORGANIZATION1
a competitive interaction for food may also
W depend on how recently each has eaten or
whether there is a receptive mate nearby.
This additional complexity does not diminish the importance of dominance as an
intervening variable, but it does introduce
difficulty in understanding its relative importance in a particular situation (McFarland, 1977; Sibly and McFarland, 1976).
Territoriality is defined in the threedimensional system of Figure 1 nearer extremes of sp; rial fixity and resource
orientation with a fixed distance to another
individual before aggression is initiated.
The figure indicates that none of these
need be 100%, but the combination distinguishes territoriality from other forms of
aggression. Territorial boundaries for
birds can vary within days (Wolf, 1975) or
seasons (Weeden, 1965; Root, 1967;
Stefanski, 1967). However, the aggressive
behavior is clearly related to displacing
others from a particular area (Odum and
Kuenzler, 1955), although the defense
generally is not of the area but of some set
of resources in it (Wolf, 1970; Wolfe/ at.,
1976). This can lead to the interesting
situation where only a subset of the resources in an area are used by an intruder.
If these differ from those used by the
resident, the intruder may be permitted
within the territory (Wolf et at., 1976).
Territoriality can shift toward dominance interactions in several ways. Some
birds, such as the Stellar's Jay (Cyrmocitta
stclleri) and the Bicolored An third (Gymnopithys tricolor), have fixed areas within
which they are dominant, but do not assert
dominance with equal probability
throughout the area (Brown, 1963; Willis,
1967). A territory boundary then is associated with the probability of winning
encounters rather than an all or none
effect. A logical position for the boundary
would be where the proportions of wins
statistically exceeds 50%, although this location may vary with different intruders.
Territoriality also may become a spatially
fixed probability of initiating an encounter.
Territoriality could also be viewed as an
expanded individual distance, and Marler
(19566) suggested the gradual establish-
767
ment of a territory in the spring by the
Chaffinch (Fringilla coelebs) is via increasing
individual distance through time coupled
with increased site fixation. The major
difference between territories and individual distance is the degree of site fixation
and the distance at which the intruder is
chased. Even the distance criterion can
vary. In the nest territories of colonial
birds, territory size may be the distance
that the nesting birds can reach without
leaving the nest (Wallace and Mahan,
1975).
Organisms can change the form of the
overt aggressive social organization
through time. Sufficient time between observations permits relatively unambiguous
distinctions among the categories, but
more frequent observations increase the
probability of seeing intermediate forms of
social organization. Redwing Blackbirds
(Agelaius phoeniceus) gradually spend more
time on their nesting territory and defend
it with increasing persistence as the time of
breeding approaches (Orians, 1961).
Bronzy Sunbirds {Nectarinia kilimensis) may
defend a (lower patch for 30-45 minutes,
and then disappear from less than an hour
to several hours only to reappear and
reestablish exclusive use for an hour or
less. (Wolf and Gill, in preparation). The
birds are territorial when present, but they
exhibit dominance interactions when absent. The length of time in each behavioral
type varies so that the social organization
depends on the time scale of interest to the
investigator.
Aggressive social organization can vary
considerably relative to variations in resource characteristics. Spatially fixed resources may be defended, leading to territoriality; spatial variation in availability of
the resources can lead to dominance interactions; and defending space around
the individual is individual distance. Of
more interest here is that with the same
spatial resource characteristics the social
organization may vary across time within a
fixed area. These variations are principally
along the territoriality-dominance axis that
reflects aggression over resource use
rather than space around the individual
(Fig. 1).
768
LARRY L. WOLF
COST: BENEFIT MODEL
A formal approach to examining variation in aggressive behavior related to resource use is essentially an economic
costrbenefit model of aggressive behavior.
This paper deals with the role that nectarivores have played and can play in our
understanding of the economics of aggressive behavior, particularly associated with
food.
Very generally we can ask: How should
an organism act under specific conditions?
A benefit/cost model assumes that it is
possible to specify benefits and costs of
alternative acts and that natural selection
has molded individual behavior to maximize individual fitness (McFarland, 1977).
Organisms that respond appropriately
will have higher relative fitness than
could have been achieved by alternative
behaviors. To the extent that the ability to
respond is genetically controlled, selection
molds how individuals respond based on
their available information. While this may
sound as if the organisms assess different
potential outcomes, selection will result in
more genetic representation in future generations ot those individuals that respond
appropriately than those that do not. For
example, a male that was highly aggressive
toward females and mated less often than
other males may leave fewer offspring
than if it were less aggressive. The level of
aggiession in the context of the mating
season and the presence of a female would
be molded by natural selection.
A formal statement of an economic
model of aggressive behavior is that a
particular act will occur if the individual's
projected net benefits exceed those of possible alternatives, including non-aggression:
B,-C,>Bi-C,
(1)
where B,, B h Q, and Cj are the benefits
and costs per time unit of acts i and j . This
model can also be used to predict the
winner of aggressive encounters where the
winner generally will be the individual with
the higher net payoff.
This model concentrates not on the absolute value of the net benefit for a particular activity, but rather on differences in
net benefits of alternatives. This is what
natural selection should operate on since
fitness is a relative value. In most cases it is
realistic to suppose that there is a lower
limit to acceptable net benefits (usually
assumed to be zero). Organisms should
continually test (in an evolutionary sense)
the results of possible experiments against
alternatives. Presumably natural selection
favors genes that lead to better alternatives. Generally these will also be ones with
positive net benefits simply because alternatives with negative net benefits have
been eliminated from the population, except for short term negative solutions.
The conditions under which this model
predicts an evolutionarily stable strategy
(ESS) (Maynard Smith and Price, 1973)
can be specified by:
or if
E,(I) = EKJ), then E3(I) > Ej(J)
That is, if the expected payoff of playing
strategy i against another individual playing i exceeds that of playing j against i then
no individual mutant that plays j can successfully invade the population. However,
if the two strategies are equal against i,
then no mutant will be able to invade if i
played against] yields a higher payoff than
j played against j . In many situations the
ESS is a mixed strategy.
The payoff matrix in most natural situations continually changes since the net
benefits of being aggressive change. The
variance in the payoff values for particular
types of interactions should be important
determinants of the selective pressure
producing variation or plasticity of behavioral response to particular stimulus
situations. This is similar to the war of
attrition, but with the benefit or penalty
functions changing among situations
rather than with time during situations. In
each case the individuals continually respond to shifting net benefits.
Most aggressive contests are asymmetric
in what Parker (1974) calls Resource
Holding Potential (RHP) or whether the
individual is the resource holder or the
attacker. In most asymmetric contests the
AGGRESSIVE SOCIAL ORGANIZATION
predicted winner is the one with more to
gain or the one with the higher RHP.
However, Maynard Smith and Parker
(1976) note that some asymmetric contests
may have paradoxical outcomes since the
individual with the higher RHP gives way
and this is an ESS. They list three situations where a paradoxical outcome seems
possible: 1) when there is a very high
probability of severe injury relative to the
potential gain; 2) when precise information exists about a cue to an asymmetry;
and 3) when RHP varies and available cues
are not good pi edictors of the outcome of
possible escalations of the contest. However, they note that the paradoxical
strategies have :i low probability of occuring in natural situations, primarily because
it is also an ESS to respond in the standard
way to the inequality sign. Thus, we expect
most or all asymmetric contests in nature
to be settled according to the direction of
the net benefit inequality sign.
One obvious difficulty with this view is
that it assumes perfect assessment of alternatives. While selection ought to be toward
perfecting such responses, there are clear
constraints on realizing the optimal condition. There may be a limited constraint
produced by historical inertia; organisms
may not have had time or genetic variability available to evolve the appropriate responses. This seems somewhat unlikely in
the case of nectar-feeding birds that depend heavily on a particular energy source
and whose small size presumably means
strong fitness penalities for poor choices
(Brown rial., 1978).
A more important constraint is due to
environmental variability. The value of a
response is projected net benefits, not past
net benefits (Dawkins and Carlisle, 1976)
and the predictability of the environment
can strongly influence the appropriateness
of a response. While in the short term one
response may provide the maximum net
benefit, it is the summed lifetime net
benefit that is critical (and even beyond if
we consider influences on subsequent generations). In general, as the variance of
environmental conditions increases, a response that minimizes the variance among
the fitness values of short term responses
769
will out-compete responses that always
seek to maximize the short term outcome
(Templeton and Rothman, 1974; Stearns,
1976). This is because the maximization is
a boom or bust strategy for which the
failure probability approaches one while
the more conservative strategy reduces the
probability of total failure (Lewontin and
Cohen, 1969). We might expect in most
natural situations organisms would show
responses that appropriately reduce the
variation of short term fitness values, but at
particular times this would appear not to
be the optimal strategy that produces
maximal fitness in the short term.
Darlington (1977) argues that environmental variation coupled with the cost of
allelic substitutions is also likely to provide
what appear to be imperfectly adapted
organisms. The overt appearance of organisms faced with this problem and those
minimizing the probability of doing badly
will be hard to discriminate in nature, but
the underlying mechanisms are quite different. The important conclusion is that
we may be searching for sets of "best"
behaviors for particular situations while
the organisms are always behaving in ways
that are somewhat off the peak. If the
constraint is genetic cost then we should
still be able to identify individuals that are
doing better in the short term. If the
constraint is that the long term maximization differs from that of short term responses we may incorrectly identify individuals that are responding "best."
Most simple optimality models assume a
single global maximum, but as the number
of factors affecting a behavioral decision
increases, the possibility increases of a
series of local maxima. Since local maxima
imply local minima, it may be difficult for
an organism to move between maxima
even though there may be adjacent maxima with absolutely higher net benefits. A
potentially significant additional problem
is that of stochastic influences on behavioral events. The role of stochastic
events in determining the overt behavioral
act is virtually unrecognized, and, by
definition, the role of such events will vary
among situations.
In the remainder of this paper I will-
770
LARRY L. W O L F
I'ABLK I. Predicted forms of aggressive social organization, either territoriality (T) or non-territoriality (XT =
dominance interactions) as a function of the net benefits
inequality among the txi'o possible Joints.
Non-territorial net benefit
Territorial
net benefit
>0
<0
>0
T,NT
NT
<0
T
T,NT
consider only territoriality and dominance.
The prediction of which will be used in a
particular situation is shown in Table I.
This table indicates that predictions are
easy when net benefits for one alternative
are plus while they are negative for the
other. However, the model predicts that
either form of aggressive social organization is possible when the net benefits for
each have the same sign. In this case it will
be possible to predict which of the two
alternatives should occur only by working
out the actual net benefits. This is probably
more important when the alternatives both
have positive net benefits. A social organization with negative net benefits cannot be
stable for very long. However, as Verner
(1977) has recently reemphasized, fitness is
a relative value and net benefits for an
individual in fitness terms may include
reductions of fitness for other individuals.
Holding a territory when costs exceed
benefits could increase fitness because of
reduced net benefits to excluded individuals.
the floral nectar that serves as the primary
energy source for the birds (Wolf el «/.,
1976; Feinsinger, 1976; Carpenter and
MacMillen, 1976/;). Quantifying benefits
then depends on being able to measure the
actual uptake of energy from flowers visited. An important alternative is to measure benefits as changes in foraging time
(Wolf, rta!., 1975; Gill, 1978).
The principal energetic constituent of
nectar is carbohydrate that is assimilated at
essentially 100% efficiency at concentrations normally encountered by feeding
birds (Hainsworth 1974). How rapidly
calories can be extracted from a flower
varies as a function of the volume content
of the flower, the "fit" between the flower
and bird morphologies, and the sugar concentration (Wolf, el «/., 1972, 1976; Wolf
and Wolf 1976). The benefits derived from
conspecific flowers should be viewed in
relation to available nectar per flower (Figure 2). The general form of the curve
Mocltonio globro
s
e
COMPONENTS OF BENEFITS AND COSTS
It is important to recognize that benefits
and costs are defined relative to which
measurements are made (McFarland,
1976). The relative benefit of food, while it
may be constant in terms of calories or
nutrients, nonetheless may vary depending on whether the individual is hungry or
on the size of the individual (Sibly and
McFarland, 1976). For nonbreeding nectarivores, we assume as a first approximation of fitness that benefits relate directly to
energy and time expenditures as they
influence survival (Schoener, 1971; (iill,
1978) and that benefits are derived from
2
3
100
4
TIME FEEDING (sec)
Mocleonio
Fuchsio
0
94
302
510
719
92 7
2072
0
24
74
124
174
224
4974
INTAKE(>il/flower)
FIG. 2. The relationship between energetic benefits
and the nectar volume per flower or the time spent at
a Hower (determined by the volume taken). The data
are for the hummingbird, Panlerpe insignis, feeding at
two flower species. The benefits are calculated from
equations in WolfV* al. (1976) assuming 1009c assimilation and costs onlv associated with extrac ting energy
from the flower.
AGGRESSIVE SOCIAL ORGANIZATION
suggests that the rate of increase in benefit
is less at high initial volumes than at low
initial volumes and differs considerably
among bird-flower combinations. Additional costs of moving between flowers,
plants, and between foraging locations and
perches will reduce these benefits. If costs
differ between territorial and nonterritorial responses the benefits for similar volume intakes will also differ. In general we might expect higher flight costs in
non-territorial situations. However, residency on a home range could reduce the
differential.
In Figure 3 these benefits are translated
into foraging time budgets in which we
assume that a hypothetical 15 g sunbird
breaks even energetically over a 24-hour
period. We predict that the time budget is
especially sensitive to variations in energetic benefits at low volumes and relatively
insensitive to similar variations at higher
volumes. Evidence from foraging records
of two male Malachite Sunbirds (Nectarinia
famosa) supports this relationship (Wolf,
1975). This means that the direction of the
inequality sign in equation (1) could differ
in the same situation depending on the
units of the benefits.
NECTAR OBTAINED PER FLOWER 1^1)
FIG. 3. The general relationship between foraging
time and nectar obtained per flower assuming 100%
assimilation of carbohydrate from the nectar and a
neutral 24-hour energy budget; see Wolf el al. (1975)
for further details.
771
Most models of aggressive behavior
utilizing an energetic base consider benefits from the average of a set of resources,
but nectarivores can modify their behavior
to increase their benefits above the average
(Gill and Wolf, 1977; Kamil, 1978; Pyke,
19786; Gass, 1978). The ability to differentially exploit patches of differing quality should be counted among potential
benefits. Most of the behavioral adjustments are available equally to territorial
and non-territorial individuals, but nectar
resources are not instantly renewed so
foraging creates depleted patches. If all
flowers in an area are not visited during a
foraging bout, remembering locations of
depleted (or full) patches could also bias
the reward above the average. However,
the usefulness of this memory system depends on how closely the individual's
memory of patch distribution approaches
reality. Memory would predict reality better when no other individuals feed in the
same area, as in the perfect territorial
system. Benefits from use of memory
should be greatest for territorial individuals, except for situations where foraging
beats do not overlap independently of aggression ( = traplining; Feinsinger, 1976).
Aggression costs can be summarized as
either metabolic or time associated with
aggression and risk factors, such as the
possibility of injury or the probability of
being taken by a predator (Stamps, 1977).
The latter might increase with activity.
Aggression costs might also include some
non-aggression. The cost of territorial defense should include time spent monitoring the territory (Carpenter and MacMillen, 19766).
The costs of aggression in territorial
nectarivores depend on the rate of invasion of intruders (Schoener, 1971), which
could be a function of territory area and/or
resource quality if population size is constant. For nonbreeding sunbirds in East
Africa the rate of invasion can be estimated
for territorial individuals by the chasing
rate. For non-territorial individuals it can
be estimated from bird feeding activity per
unit time. At Leonotis flowers in the Rift
Valley the rate of chasing was negatively
related to the square root of territory size
772
LARRY L. WOLF
(Gill and Wolf, unpublished). Territory tions. Nonbreeding territoriality in neesize also decreased with flower density so tarivores probably is a relatively short term
that average number of flowers per terri- response in which day to day survival is
tory remained essentially constant (Gill and critical. During the breeding season the
Wolf, 1975). Thus, chase rates were a added reproductive constraints make the
positive function of flower density, an ob- problem longer term if short term negative
vious cue to the feeding birds (Gill and net benefits are acceptable for longer term
Wolf, unpublished). In a hedge of Aloe gain (Wolf and Wolf, 1976). Intermediate
secundiflora near Gilgil, Kenya, the rate of between these two time scales will be one
chasing by territorial sunbirds per m2 of associated with seasonal blooming patterns
territory was a positive function of flowers of flowers. Territoriality might be advanper m2 (Wolf and Gill, in preparation). tageous if, at times when nonterritoriality
The relationship to average nectar vol- would have a higher net benefit, it assures
umes was negative suggesting that intrud- the attacker/holder asymmetry when the
ers tended to reduce nectar voJumes. In net benefits are reversed. Thus, it appears
nonterritorial situations minutes of bird the solution to the relative importance of
feeding per m2 hour was positively related time scales may vary depending on the
to flower density and negatively related to importance of the short term perturbaavailable nectar volumes. Again, the birds tions to the net benefit inequalities.
seemed to invade an area in relation to
flower density. Nectar volumes seemed to
play little role, but were reduced by heavy Net benefits
use.
With costs and benefits identified, the
Once the sources of benefits and costs shape of the net benefit curve as a function
are identified the next step is to pick an of nectar per flower is the difference beindex of fitness for the situation (Schoener, tween the two functions. If we hold number
1971). Although others are possible many of intruders per unit time and the distance
authors use maximizing rate of net energy of each chase constant, then costs should
accumulation as a fitness index for short remain constant relative to benefits for
term time scales (see Pyke et ai, 1977). We both territorial and nonterritorial indimight anticipate that a bird attempts to viduals. The cost of nonterritorial aggresminimize total feeding time or total costs sion should be minimal. Figure 4A indiover a time interval. Pyke (1978r/) showed cates the costs ot nonterritoriality as
that territory size in Golden-winged Sun- slightly greater than zero, but constant
birds (Nertnrinia reichenoxui) conformed over all nectar availabilities. The costs of
most closely to a cost minimization criter- territorial behavior should also be constant
ion. It is possible the birds will not act in a under the assumptions, but the added cost
short term optimal fashion in order to of aggression will make the value higher
satisfy a longer term fitness function. Sev- than for nonterritorial individuals.
eral kinds of relatively sedentary orThe benefit functions will take apganisms, including spiders and lions, have proximately the same shape as in Figure 2.
relatively inflexible territory sizes that However, they will be displaced from their
seem to reflect the size required when food original position because of the effects of
is least available (Reichert, in preparation; the two behavior types on the resource.
Schaller, 1972). This may maximize the Territoriality may raise the benefits by
probability of acquiring sufficient re- some amount that reflects the reduced
sources at times of low food availability.
total utilization, but it also increases the
The time scale problem is not all or total energy required by the resident
nothing for each possible unit of time. It is (Wolf et ai, 1975; Carpenter and Macessentially a hierarchical problem (Daw- Millen, 1976«). If nectar levels are
kins, 1976) in which succeedingly larger sufficiently high at the start, the influence
time scales reduce the flexibility of re- of territoriality could shift the upper porsponse to locally shifting short term condi- tion to the left. If the levels are initially low
AGGRESSIVE SOCIAL ORGANIZATION
the lower portion of the curve could be
shifted to the right, thus altering the general shape of the curve slightly. For nonterritorial birds the effect of intruders is'lo
reduce the level of available energy per
flower through exploitation competition,
This will shift the benefit curve to the
right, the distance effecting the level of
intruder pressure.
The net benefits of the two alternatives
are shown in Figure 4B. Assuming the
organisms select the better alternative, we
can predict the range of nectar volumes
over which each alternative should be cho-
NECTAR VOLUME PER FLOWER
NT,.
35 +
/'y''
'
1
FIG. 4. A. Hypothetical relationship between benefits
and costs of social organization types and available
nectar volumes per flower. Intruder pressure is assumed to be constant. T B and NTB are the benefits of
territoriality and nonterritoriality, respectively; T c
and NTC are the costs of territoriality and nonterritoriality, respectively. The benefits of territoriality include the costs of feeding at the flowers and are
slight modifications of the relationship shown in Figure 2. See text for further details of position of the
benefit and cost curves. B. The net benefits of the
territorial and non-territorial social organizations.
These are derived by calculating the difference between the benefit and cost curves in A. The arrows
indicate the upper and lower thresholds of territoriality.
773
sen. In Figure 4 there is a middle range of
resource values under which territoriality
should occur; at high and very low values
the organism should be nonterritorial.
However, at the low levels of available
nectar both alternatives have negative net
benefits and the system should be unstable
over long periods of time.
The influence of the feedback relation
between nectar volumes at the time of
decision and the shift of the benefit curves
for territorial birds is complexly related to
intruder pressure and nectar production
rates. There is a threshold level of nectar
availability per flower below which foraging time is sufficiently high in relation to
nectar production rates that nectar volumes gradually decline; above this
threshold the requirements of the birds
are sufficiently low that nectar volumes
increase. The effect in both cases is to
gradually shift along the net benefit function with the direction of shift depending
on the starting volumes in relation to the
threshold value. If nectar volumes increased enough during the course of a clay
and the threshold was exceeded, territorial
birds should become nonterritorial. Birds
that begin at sufficiently high nectar volumes should be nonterritorial, but again
the effect is to continually reduce the levels
if use exceeds nectar production rates.
Thus, the birds may gradually move toward the origin and cross into the territoriality region.
The actual shapes of the benefit and
costs curves will change with the particular
situation, and very likely in relation to the
available nectar per flower. This will make
the curves more complicated and can have
differential effects on the curves for the
two alternatives. Higher intruder pressure
at higher resource levels will shift the
benefit curve for nonterritorial individuals
farther to the right, but only at the upper
portion thus straightening the curve
somewhat. For territorial individuals the
upper portion of the benefit curve will be
shifted slightly to the right while the cost
curve will have a positive slope and
perhaps will be curvilinear (Fig. 5).
Increased intruder pressure is assumed
to decrease the benefit functions for non-
774
LARRY L. WOLF
territorial birds at low resource levels so
the net benefit curve for territorial individuals always exceeds that of nonterritorial (Fig. 5). Territoriality then should
occur at low resource levels until the individuals desert the area. The net benefits of
nonterritoriality exceed those of territoriality at low resource levels if constant
intruder pressure is assumed along the
resource gradient.
The lack of territoriality in some nonnectarivore bird species at low resource
levels (Lederer, in preparation) may relate
to the benefits of non-renewing resources.
A renewing resource allows the position
along the benefit curve to increase as a
result of limited use by intruders. For a
non-renewing resource the position on the
benefit curve remains the same. At least
for the short term the added cost of territorial defense of non-renewing resources
cannot be recouped by the increased
benefits and the net benefit curves will
cross at low resource levels. However,
longer term net benefits can be increased
by the reduced rate of exploitation of the
non-renewing resource over a season.
The net benefit curves can also be made
to cross if we consider that territoriality is
site-fixed while non-territorial behavior is
not. So far we have been considering
benefits within a site; nonterritoriai behavior increases the number of sites that
can be exploited, potentially producing a
higher net benefit for organisms that are
exploiting a non-renewing resource.
GENERAL PREDICTIONS
There are two relatively obvious general
predictions of net benefit models of aggressive behavior. These cannot be tested
now since data are too limited to define
quantitatively the net benefit curves for
territorial and nonterritoriai birds.
The first prediction is that if organisms
can respond to short term changes in
realized net benefits we might expect to see
rapid shifts in type of aggressive interaction when the inequality sign between alternatives is reversed. In the Pied Wagtail
{Motacilla alba), an insectivorous passerine
bird, Davies (1976) showed that the shift
from territoriality to flocking was correlated with spatial location of the individual
and occurred over intervals as small as one
NECTAR VOLUME PER FLOWER
minute. The length of time on the territory
closely correlated with the rate of intake of
food. Gill and Wolf (1975) reported that
Golden-winged Sunbirds (Nectarinia
reichenoun) shifted from dominance to territoriality as nectar volumes per flower
declined during the day in a large field of
flowering mint in Kast Africa. Longer term
variations have been reported by numerous authors, including Garpenter and
MacMillen (19766) for a species of
Hawaiian honeycreeper.
The second prediction is that a behavioral state may be maintained beyond a
predicted threshold by the organism selectively changing benefit or cost terms. The
general response will be to vary costs selecFIG. 5. Similar to Figure 4, but costs of territoriality tively which may have a correlated effect
are assumed to be a monotonically increasing function of the quality of the territory. In this case there is on benefits. Reducing chase costs normally
no lower threshold of territoriality. Symbols as in will increase losses to competitors. Selective
Figure 4.
reduction will be advantageous onh when
AGGRESSIVE SOCIAL ORGANIZATION
I ID
100
chasing a smaller proportion of the intruders (Fig. 6). The territorial birds used
less expensive displays and decreased
80
chase duration as the availability:required
energy ratio fell. They also spent less time
on the territory as relative availability de60
clined. The birds did not shift behavior
drastically as the availability of energy at
the feeder increased above just meeting
40
the energy requirements of the resident.
This may represent a situation where
maintaining a territory provided a predict20
able long term benefit or perhaps the birds
were minimizing total foraging time.
The birds also showed what could be
interpreted as a very short term assessment
0
0.5
1.0
li
2.0
changing benefits and costs. The probaAVAILABLE ENERGY /REQUIRED ENERGY of
bility of chasing an intruder was a positive
Fig. 6. Relationship between percentage of intruders
chased and territory quality, as measured by the function of the time since feeding. This
amount of food available from a feeder in relation to suggests that they viewed the benefit and
what is required by the territorial bird for a 24-hour cost function of aggressive behavior as
period. Modified from Ewald and Carpenter (1978) changing over short time periods.
from data on territorial male Anna Hummingbirds.
costs decline more rapidly then benefits.
Wolf (1975) noted that a male Malachite
Sunbird (N. famosa) in East Africa maintained a large breeding territory if the
number of intruders was low or the nectar
volumes per flower were high. However, at
low nectar volumes with foraging time
budgets of 30% or more and high intruder
pressure, the male collapsed its effective
territory size temporarily. Before a chase
he often fed adjacent to intruders feeding
in portions of its previously defended territory. In this way the bird allowed nectar
to accumulate in a defended core which it
rarely visited while continuing its energy
intake in the undefended periphery in the
face of heavy intruder pressure.
Ewald and Carpenter (1978) experimentally manipulated the availability of
energy from feeders to territorial Anna
Hummingbirds (Calypte anna) in an area
where there were few or no natural nectar
sources. They could regulate the amount
of "nectar" available from feeders. Defense
by the territorial resident changed with the
proportion of daily energy requirements
available at the feeder. As available energy
declined relative to requirements, the territorial birds reduced aggressive costs by
Observations of Lampornis clemenciac also
suggest the possibility of very subtle assessments of net benefits (Lyon et ai,
1977). Ten feeders were arrayed in a territory, and the territory was gradually expanded in size by increasing the distance
from the feeders in the center to eight
peripheral feeders. As the area was increased the probability of the resident
male chasing an intruder varied with
species and sex of the intruder (Fig. 7). In
natural situations the loss of nectar at long
corolla flowers regularly visited by a male
Blue-throat should depend on the bill
length of the intruder. A short-billed intruder should leave more residual nectar
than a longer-billed bird. Benefits of
chasing a short-billed bird should be less
than a longer-billed bird at the same
flower. If each individual is approximately
equally expensive to chase then net
benefits should always be less for small
intruders than for large. We would predict
that the resident bird would be willing to
spend more effort to chase larger-billed
individuals than smaller-billed ones, the
greater expense coming from longer distances at which chases are initiated. In this
example the lack of chasing of intruder
female Blue-throats may be due to data
collection during the breeding season
776
LARRY L. WOLF
not predict the type of social organization
for situations where net benefits of both
alternatives either exceed zero or are less
than zero. In the present model of alter80
natives it is possible that territoriality will
occur when its benefits are less than zero if
the net benefits of alternatives are even
§ 60
more negative. The present model will be
in agreement with the CarpenterMacMillen model if, when the net benefits
of territoriality are > zero, the net benefits
of nonterritoriality are constrained to be
less than zero, and vice versa. The
Carpenter-MacMillen
model is easier to
20
test in the field since it requires knowing
only if the bird is doing well enough to
break even energetically. To test the present model requires that the net benefits of
20
40
60
80
the alternatives be compared.
In conclusion, it is important to begin
TERRITORY SIZE (m«)
Fig. 7. The relationship between the probability of a viewing the form of aggressive social syschase occurring when a bird visits a feeder and the tems by comparing the net benefits of
distance from the feeder for several species and sexes alternative forms. To do this we must
of intruders. The resident, aggressive individual in understand what general function defines
this situation was a male Blue-throated Hummingbird net benefits. It might be, for example, a
(Lampornis clemencine). See text for futher details of
minimization of costs or a maximization ot
experiment. Drawn from data in Lyon el at., 1977.
energy accumulation per time. It also is
essential that we understand the time span
when territories may serve as locations for over which these net benefits are integratmeeting females. In this case, the benefits ed. Finally, I hope that this discussion
for the male may have shifted from has focused attention on the considerations essential to empirical tests of net
energetics to a more direct measure of benefits models of aggressive behavior,
mating success.
especially when to be territorial.
100
I*
S
CONCLUSION
This model for predicting whether an
organism should be territorial or not takes
a somewhat different approach from a
recent model proposed by Carpenter and
MacMillen (1976c/). The premise of their
model is that territoriality will occur at low
environmental productivity whenever the
net benefits of territoriality are positive
and that at high productivity territoriality
will occur when the net benefits of not
being territorial are negative. The present
model requires no fixed level of net benefits for either type of social behavior to
determine the point of shift of the social
system. Rather it requires only that one
behavioral form have a higher net benefit
than the other. 'I heir n:oiie! <>enerailv dors
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