FORAGING SELECTIVITY IN ADULT BUTTERFLIES:

MORPHOLOGICAL, ECOLOGICAL, AND PHYSIOLOGICAL

FACTORS AFFECTING FLOWER CHOICE

By

PETER GREGORY MAY

A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL

OF THE UNIVERSITY OF FLORIDA IN

PARTIAL FULFILLMENT OF THE REQUIREMENTS

FOR THE DEGREE OF DOCTOR OF PHILOSOPHY

UNIVERSITY OF FLORIDA

1985

ACKNOWLEDGEMENTS

I have been helped by a great many people during the course
of this study, and to everyone who has contributed, in whatever
way, I am grateful. I would first like to thank my parents,
Rolland and Sally May, for their support and encouragement
throughout my extended scholastic career.

The direction and final form of this dissertation were
greatly enhanced by my chairman and co-chairman, Carmine
Lanciani and Lincoln Brower. Along with the rest of my
supervisory committee, Jane Brockmann, Tom Emmel, Katherine
Ewel, and John W. Hardy, their advice and comments on various
manuscripts have been invaluable.

Discussions with many people have been incorporated in some
sense into my work. I would especially like to thank Jim Cohen,
Peter Feinsinger, Gene Spears, Craig Hieber, Joel Kingsolver,
Jeff Lucas, Frank Slansky Jr., and Harry Tiebout III.
Invaluable field assistance was provided by Jana Holland and
Eden La Graves.

Equipment of various sorts was loaned or given to me by
Lincoln Brower, Peter Feinsinger, Carmine Lanciani, and Jeff
Lucas. This study was supported by grants from Sigma Xi and the
National Academy of Sciences, as well as various stipends
provided by the Department of Zoology. Thanks to all.

Finally, I would like to thank the Florida Department of
Natural Resources and the staff of Payne's Prairie State
Preserve for permission to conduct this study and assistance
with location of study sites. Especially worthy of mention are
Howard Adams, Jack Gillen, Ed Higgins, Craig Parenteau, and
James Stevenson. All provided valuable service at some time or
another (as well as mowing my study sites once or twice!).

To all of the above, and to anybody I have neglected to
mention, I give heartfelt thanks.

TABLE OF CONTENTS

Page

ACKNOWLEDGEMENTS ii

ABSTRACT vi

CHAPTERS

I GENERAL INTRODUCTION AND PLAN OF THIS STUDY 1

Optimal Foraging Theory — A Selective Review 3

Foraging Behavior of Nectarivores 9

Adult Foraging in Lepidopterans 16

Effects of Adult Foraging on Fitness 23

General Approach of This Study 29

Biology of the Study Species 31

II NECTAR UPTAKE RATES OF AGRAULIS
VANILLAE AND PHOEBIS SENNAE:

EFFECT ON OPTIMAL NECTAR CONCENTRATION 33

Introduction 33

Methods and Materials 37

Results 39

Discussion 50

Summary 5I+

III FLOWER SELECTION AND THE ENERGETICS OF
FORAGING IN AGRAULIS VANILLAE AND PHOEBIS

SENNAE 56

Introduction 56

Methods and Materials 59

Results 65

Discussion 89

Summary 97

IV LIPID STORAGE AND DEPLETION IN AGRAULIS
VANILLAE AND PHOEBIS SENNAE: EFFECTS

OF ADULT FORAGING 100

Introduction 100

Methods and Materials 103

Results 101*

Discussion 113

Summary 119

V THE EFFECTS OF ADULT ENERGY INTAKE ON
SURVIVAL AND FECUNDITY OF

AGRAULIS VANILLAE 121

Introduction 121

Methods and Materials • 12h

Results 126

Discussion 137

, Summary 1^2

VI ADULT FORAGING IN AGRAULIS VANILLAE
AND PHOEBIS SENNAE: SUMMARY, SYNTHESIS,

AND CONCLUSIONS 1^3

Adult Foraging in Lepidopterans -

A General Hypothesis 15^

Obligate Adult Foragers 15*+

Facultative Adult Foragers 156

APPENDIX 158

LITERATURE CITED l6l

BIOGRAPHICAL SKETCH 173

Abstract of Dissertation Presented to the Graduate School

of the University of Florida in Partial Fulfillment of the

Requirements for the Degree of Doctor of Philosophy

FORAGING SELECTIVITY IN ADULT BUTTERFLIES:

MORPHOLOGICAL, ECOLOGICAL, AND PHYSIOLOGICAL

FACTORS AFFECTING FLOWER CHOICE

By

Peter Gregory May

May, 1985

Chairman: Dr. Carmine A. Lanciani
Co-chairman: Dr. Lincoln P. Brower
Major Department: Zoology

I studied flower selection by adult butterflies of two
species, Agraulis vanillae (Nymphalidae) and Phoebis sennae
(Pieridae), from several perspectives. First, I critically
evaluated recent theoretical models of the feeding mechanics of
butterflies. These models predicted that butterflies should
select flowers with nectars of 20-25% sugar concentration, which
provide the greatest rate of energy intake. I measured nectar
uptake rates of these butterflies and empirically determined
that the greatest rate of energy intake is at nectars from
35-^0% sugar. Second, I quantified the energy rewards of the
flowers visited by these butterflies and showed that energy
intake rate while foraging is associated with corolla length and
nectar volume, but not with nectar concentration. The two

butterflies differ significantly in flower selection. Phoebis
sennae selects flowers that are more energetically rewarding,
because a) it has a longer proboscis and can exploit
long-corolla flowers from which Agraulis is excluded, and b) it
discriminates more often between low- and high-reward flowers.
Differences in discrimination (specialization) may be due to
differences in vagility and time-allocation patterns between the
two species. As predicted by recent theory, Phoebis sennae,
which acquires more energy than Agraulis as an adult , emerges
from the pupa with small fat stores and rapidly builds fat
reserves by profitable adult foraging. Agraulis vanillae
individuals emerge from the pupae with larger fat stores and do
not add to them during life, but instead gradually depletes
these lipids acquired through larval foraging. ' Increased energy
intake of adult Agraulis vanillae is associated with increased
fecundity, lower mortality, and a lower rate of fat depletion,
but the benefits associated with increasing energy intake may
diminish at higher energy intake levels.

CHAPTER I
GENERAL INTRODUCTION AND PLAN OF THIS STUDY

All animals are to some extent selective in their choice of food
items. Thus, no animal feeds on all potentially nutritive items
that it encounters while foraging. In large part this selectivity is
due to morphological and biochemical constraints that are the result
of evolutionary adaptation towards feeding on some particular type of
food. Thus, herbivorous insects do not pursue and consume other
insects, peregrine falcons do not browse foliage, and so on. But even
within the range of food items that are potentially consumable by a
given species, some food items are usually preferred over others. In
the last twenty years a large body of literature has developed dealing
with the subject of food choice by animals, and has attempted to
derive generalizations that will explain and predict observed patterns
of prey choice in a variety of animals. This literature is
collectively referred to under the general term optimal foraging
theory and will be discussed in some detail below.

Whereas some authors have pursued a theoretical approach to the
topic of prey choice, other researchers have attempted to apply this
theory to observed feeding behavior of real organisms in both
laboratory and field contexts. Feeding habits and food selection of a
variety of organisms have been studied. There has been relatively
little work on the feeding behavior of holometabolous insects, which
are somewhat distinct in their feeding strategy. Whereas vertebrates

1

and a great many invertebrates do not radically change their food
habits over the lifespan of an individual, holometabolous insects may
have two completely distinct feeding strategies during the life of an
individual. Feeding occurs during the larval stage and may be the
predominant activity engaged in by this stage. In addition, feeding
may or may not occur during the adult stage, and the nature of the
food that is taken is usually quite dissimilar from that of the larva.

Insects of the order Lepidoptera are holometabolous. The primary
function of the larval stage is acquisition of nutrients to be used in
forming the adult insect and provisioning it with reproductive
reserves. These nutrients are obtained through feeding on vegetation
in the majority of species. The main function of the adult
stage is reproduction, and feeding during the adult stage is
highly variable both in extent and in the nature of the food
taken. Generally, feeding by the adult is primarily to obtain energy,
since the insect is fully grown upon emergence and tissue repair does
not occur (Opler and Krizek 198U). Tne importance of adult feeding in
butterflies has been largely ignored (Gilbert and Singer 1975), but is
certainly interrelated in a complex fashion with larval feeding
behavior. The interrelationships between larval and adult feeding
have only recently begun to be addressed in the ecological literature
(Boggs 1981).

Because of the complexity of feeding behaviors during the life of
a holometabolous insect, feeding behavior of either the larval or
adult stage of these insects may be subject to different constraints
or selective pressures than in animals with more homogeneous
feeding habits. In this study I examine flower choice by adults of

two species of "butterflies. Specifically, I have l) revised the
predictions of mechanical models of butterfly feeding that predict
selectivity of flowers based on nectar concentration, 2) examined
energetics of foraging and selection of nectar sources actually chosen
by foraging butterflies, and 3) considered the bases for the observed
foraging choices, k) I have examined differences in the lipid storage
patterns of two butterfly species and the relationship between lipid
dynamics and foraging energetics. Finally, 5) I show effects of
energy intake of adults on fitness components such as longevity and
fecundity. In this introductory chapter, I selectively review the
literature on several topics pertinent to the studies outlined above.
First, I consider some of the literature on optimal foraging.
My work asks the general question: what factors affect flower
choice in foraging butterflies? Therefore, I will concentrate
on that segment of the literature dealing with the selection of
food items by foragers (as opposed to patch choice, time
allocation, etc.). Next, I review some pertinent studies concerning
foraging behavior of other nectarivores , concentrating on factors that
are thought to influence food choice in these animals. I then discuss
the applicability of this information to foraging butterflies.
Finally I review several studies dealing with the effects of adult
diet on fitness, the ultimate criterion by which any animal's foraging
decisions are evaluated.

Optimal Foraging Theory — A Selective Review
The first formal treatments of prey choice (which stimulated the
development of what has come to be known as optimal foraging theory)
were those of Emlen (I966) and MacArthur and Pianka (1966). These
papers were followed by numerous others summarized in Schoener (1971)

and Pyke et al. (1977). All of this work is based on the following
argument. Given that most behavior, including foraging, shows some
heritable variation, there is then a range of possible foraging
strategies within a population or species. If these strategies differ
in their efficiency, then natural selection should favor those
genotypes and individuals whose foraging behavior is most efficient.
This assumes that differences in foraging efficiency (however it is
defined) will result in differences in fitness, and that the rate of
behavioral change is greater than the rate at which the position or
strategy conferring the maximum fitness changes. Thus evolution of
the behavior is capable of tracking environmental changes which might
shift the optimal foraging strategy. In support of the first of these
assumptions, Schoener (1971) points out that it is well known that
increased food intake increases the growth rate in many organisms. He
proposes several mechanisms whereby increased growth rate may increase
reproductive fitness. Still, there are few data linking differences
in feeding behavior to differences in fitness.

The feeding models considered in Schoener (1971) and
Pyke et al. (1977) center on four types of foraging choices that may
affect food intake and thus fitness: a) the types of food to eat
(optimal diet), b) the area in which to feed (optimal patch
choice), c) how much time to spend in an individual patch, and d)
speed and direction of movement while foraging. Pyke (1984) has
updated these reviews and has considered several new classes of
foraging models. I will limit my review to selection of food items.

As pointed out by Schoener (1971), modeling any aspect of
foraging involves first choosing an appropriate currency (energy,
nutrients, nitrogen) to maximize, constructing cost-
benefit functions for that currency, and then solving for the optimum.
In the original foraging models of Schoener (1971), Charnov (1976),
and in most subsequent work, the chosen currency has been energy.
Each potential food item has an associated caloric reward, and this
energy reward is discounted by the energy costs associated with
finding, capturing, and consuming the item. An optimal forager ranks
items for inclusion in the diet on the basis of the energy/time ratio,
and selects the diet by successively adding lower ranking items until
such addition causes the net rate of energy intake /time to drop. The
set of all available food items that do not cause this net energy/time
rate to drop constitutes the optimal diet. This model yields several
predictions regarding the inclusion of food types in the diet, such as
a) the inclusion or exclusion of a food item is independent of the
abundance of that type of food, but dependent on the abundance of
higher ranking items; b) as the abundance of preferred food items
increases, selectivity should increase, i.e., the number of types of
food taken decreases; c) a given food item should always be either
eaten or rejected. In fact, some bee species have been shown to
violate prediction c and exhibit partial preferences (Waddington and
Holden 1979, for example). These insects do not always accept or
reject a given type of food item (flower type in this case). Such
partial preferences have led several authors to speculate on the
causes of partial preferences and other types of diet selection that
are more varied than those predicted by these original formulations.

Pulliam (1975) and Westoby (1978) have both considered factors
leading to diverse diets. Pulliam (1975) showed that nutrient
constraints may cause an optimal predator to show partial preferences,
and Westoby (1978) listed several factors that may cause an animal to
choose a diverse diet. These include situations in which taking
several types of food reduces search time, cases where the optimal
diet cannot be deduced from past experience (i.e., sampling is
required), and cases where different foods are the best sources of
different required nutrients. Heinrich (1976a) and Waddington and
Holden (1979) have also emphasized the importance of sampling to
organisms that must monitor resources that vary over time. The
inclusion of nutritive qualities other than energy content may be
critical to building realistic foraging models for some organisms.
For example, Belovsky (1981) has modeled food selection by a
generalist herbivore, the moose, and has shown that food selection can
be explained reasonably well by consideration of protein and ash
content of browse plant species (which are highly correlated with
digestibility), size of the food items, and relative abundance.

Another factor that may lead to broader diets than those
predicted by early models is the amount of time available to the
animal for foraging. Lucas (1983) points out that these early models
generally assume that infinitiely long periods of time are available
for foraging. In fact in many animals, foraging periods may be
terminated by biotic factors, such as presence of a predator or
conspecif ics , as well as abiotic factors such as tidal cycles. Lucas
has integrated the effects of limited foraging time into
energy-maximization models of foraging. His models make two

interesting predictions: l) as the length of the foraging bout
decreases, the optimal forager should become less selective and
include lower-quality prey items in the diet; 2) variability in prey
distributions can produce situations where partial prey preference
(i.e., not always either rejecting or taking an encountered prey item)
will result in a greater rate of energy intake that either a pure
specialist (always take only one prey type) or a generalist (always
take more than one prey type) strategy. Thus, the nature of the time
constraints under which a given animal operates may be important to
prey selectivity decisions.

Another source of variability in diet selection may be
differences in the variability of nutritive rewards offered by
different food types. Caraco (1980), Real (l980a,1980b,198l) and Real
et al. (1982) have emphasized the importance of variability in the
current energy balance of the individual forager as well as variation
in food quality within a food type in producing diversified diet
selection. Their premise is that some animals may be selected not
to maximize energy intake as suggested by the family of models
reviewed by Schoener (l9Tl) and Pyke et al. (1977) , but to reduce the
uncertainty associated with obtaining some critical level of energy-
intake. Thus, they might choose food types with low variability in
reward over those that on average are more rewarding but also
more variable. Caraco (1980) reasoned that an organism that can
incur an energy deficit and survive may prefer high-variability items
if they offer a higher mean reward. Such animals are "gambling" that
they will encounter some high-reward items and reap the consequent
energy benefit. Such animals are termed risk-prone foragers.

Other animals that cannot afford to incur a negative energy balance
may opt for a more conservative risk-averse strategy and choose
low- variability items even though they may be associated with a lower
mean reward. Experimental tests of these hypotheses have lent some
support. Caraco et al. (1980) showed that white-eyed juncos (Junco
phaeonotus ) exhibit risk-averse foraging when on a positive energy-
budget whereas starved birds switched to risk-prone foraging. They
interpreted these results as indicating that the birds are willing to
gamble on higher net rewards when those rewards are required to
balance the energy budget. Birds that are experiencing no difficulty
in balancing their energy budget are less likely to risk foraging on
high-variability items. Real (1981) conducted feeding experiments
with bumblebees and wasps and found risk-averse foraging in both types
of insects; i.e., both showed preference for low- variability rewards.
Real et al. (1982) found that, in foraging bumblebees, a food type
with high reward variability required a greater mean energy reward
than an invariant food type before the bees would visit it with equal
frequency. The magnitude of the bees' risk-aversion was directly
related to the degree of variability in the variable reward food item.
At high reward levels, however, the degree of risk aversion declined,
suggesting that finely-tuned foraging responses are more likely when
energy may be limiting.

In addition to these factors that may modify the predictions of
simple models of foraging, Mitchell (1981) has offered several
cautions concerning simple energy maximization models of foraging.
Whether the rate of energy intake or foraging efficiency actually
affects fitness is not always clear. Some species select foods that

are most efficiently assimilated, whereas others select foods that are
not. In some blowflies the threshold levels of sugar receptors to
sugar solutions are highly variable, which is unexpected if energy-
content of the diet is directly related to fitness. Some sugar
receptors are also stimulated by various amino acids, suggesting that
there may be selection for dietary diversification in order to provide
nutrients for reasons other than their caloric content. Real (1980a)
has argued that even in species where energy content of the diet is
related to fitness, there may be diminishing fitness returns at higher
energy intake levels.

The foraging models discussed above thus make two basic
assumptions that are rarely tested. First, they usually assume that
animals will forage so as to maximize the rate of energy intake. As
will be pointed out below, this assumption is more reasonable for some
types of animals than others. Second, they assume that maximizing
energy intake will maximize the achieved fitness. As pointed out by
Real (1980a, 1980b, 198l), Caraco (1980), and others, factors other
than energy content, such as variability in energy content, may be
important to maximizing the probability of survival and therefore may
form the basis of foraging choices. In the following sections, I will
review some of the evidence for energy-maximizing behavior and food
choice in nectarivorous animals and the effects of foraging choices on
fitness.

Foraging Behavior of Nectarivores

Despite the untested assumptions of energy-maximization foraging
models discussed above, Pyke (l98la) has emphasized that
nectar-feeding animals are ideal test subjects for energy-based

10

foraging models. First, factors other than energy content affecting
foraging decisions, such as non-energy nutrient content and risk of
predation while foraging, can often be ignored with these animals.
Nectar often contains little other than sugar and water, and is
virtually the only source of energy for some nectarivores such as
bumblebees. The survival, growth, and reproduction of these organisms
are thus directly related to energy intake. Additionally,
nectarivores are often quite visible while foraging, allowing easy
quantification of food choice. Energy content of individual flowers
can be measured. It is possible for researchers to construct
time-energy budgets for foraging animals and reasonably estimate
energetic costs and benefits encountered while foraging. It is
therefore not surprising that much research has focused on
foraging behavior and energetics of nectarivorous animals of diverse
taxa.

Two nectarivore groups that have been thoroughly studied are
nectar-feeding birds (Nectariniidae, Meliphagidae, Trochilidae) and
various species of bees (Apoidea). The birds and their floral
resources have been studied from the viewpoint of community
organization and resource partitioning (Feinsinger 1976, 1978;
Kodric-Brown et al. 198U; Wolf et al. 1976), morphology and flight
energetics (Feinsinger et al. 1979), and energetics and behavioral
ecology of the foraging process itself (Gill and Wolf 1977;
Hainsworth 1978,1981; Hainsworth and Wolf 1972a, 1972b, 1976;
Kingsolver and Daniel 1983; Montgomerie I98U ; Montgomerie et al.
I98U; Pyke 1978, 198la, 1981b; Fyke and Waser 1981; Wolf and
Hainsworth 1971; Wolf et al. 1976). While it has generally not been

11

possible to test rigorous optimal foraging models under the complex
and variable conditions encountered in the field, these studies have
all emphasized the importance of energetic considerations in foraging
selectivity. Numerous studies (Gill and Wolf 1977; Pyke 1978, 198la,
198lb) have shown that hummingbird and sunbird movement patterns while
foraging are non-random and serve to minimize the probability of the
birds revisiting flowers and to maximize the probability of their
visiting the most rewarding flowers. Metabolic rates of perching and
hovering hummingbirds have been measured in the laboratory, and the
energetic costs of the components of foraging have been estimated. By
combining these data with time budgets recorded in the field,
fairly accurate energy budgets have been constructed for several
hummingbird-flower systems. This work has generally supported the
contention that the birds are behaving so as to maximize the rate of
energy gain (Hainsworth 1978). Because of their rapid rate of flower
visitation, energy requirements of these birds may be obtained by
their foraging during as little as 10 to 357" of each active hour
(Hainsworth and Wolf 1972b; Wolf et al. 1976). The effect of the
current energy status of the individual bird on its foraging behavior
has been emphasized by Hainsworth (1981). He has demonstrated that
the rate of energy gain by foraging hummingbirds increases with
decreasing energy reserves, and that sensitivity of the birds to
differences in nectar concentration (which in part determines energy
content) is most pronounced in low-concentration, energy limited
nectars.

One of the primary factors affecting energy content of nectar is
sugar concentration. The relationship between nectar characteristics

12

and their effect on the rate of energy intake has also been studied in
some detail (Hainsworth and Wolf 1976; Heyneman 1983; Kingsolver and
Daniel 1983 ; Montgomerie 1984 ; Montgomerie et al. 1984 ; Pyke and
Waser 1981). Theoretical models of hummingbird feeding mechanics of
hummingbirds indicate that the net rate of energy intake will be
maximized at nectar concentrations between 25 and 40% sucrose
(Heyneman 1983; Kingsolver and Daniel 1983), due to constraints on
nectar uptake rates produced by the high viscosity of concentrated
nectars. Other studies discount the effects of viscosity on uptake
rate and suggest that increasing sugar concentrations will increase
the net rate of energy intake (Hainsworth and Wolf 1976; Pyke and
Waser I98I; Montgomerie et al. 1984; Montgomerie 1984). The studies
of Montgomerie (1984) and Montgomerie et al. (1984) demonstrate the
sensitivity of hummingbirds to nectar characteristics while foraging
under artificial conditions. These authors show that the birds'
foraging decisions are consistent with maximization of the rate of
energy intake or a closely related quantity, net energy per volume
consumed. But nectarivorous birds differ in several important
respects from nectarivorous insects. Foraging hummingbirds
are homeothermic , which increases energy demands by increasing the
rate of energy expenditure. Nectarivorous insects are able to vary
body temperature and thus reduce metabolic rates at certain times to
reduce overall energetic demands (Heinrich 1979b). The smaller body
size of insects further reduces energy demands, allowing them to
exploit nectar resources that would not support larger homeothermic
nectarivores. Nectar quantities produced by insect-visited flowers
are sometimes minute (Heinrich 1975; Watt et al. 1974).

13

The best studied nectarivorous insects are the hymenopterans ,
particularly within the family Apidae. Various studies have
emphasized the effect of dispersion of floral resources on movement
patterns of bees (Waddington I98O; Waddington and Heinrich I98I;
Zimmerman 1979), competition for and differential strategies of
exploitation of floral resources used by more than one species
(Heinrich 1976b; Hubbell and Johnson 1978; Morse 198l; Inouye
1978,1980; Johnson and Hubbell 1975; Schaf f er et al^ 1979), and
selectivity of nectar resources in relation to nectar reward
characteristics (Ginsberg 1983; Heinrich 1979a; Heithaus 1979;
Pleasants 198l; Real et al^ 1982; Real I98I; Roubik and Buchmann
1981+; Waddington et aL 198I; Waddington and Holden 1979; Wells et
al. 198l). The importance of some of these factors to flower
selection in nectarivorous insects is considered next.

Among the more important factors affecting the choice of flowers
by bees are dispersion of the resource, nectar volume, and
concentration and variation thereof, evolved foraging strategy of the
species (social vs. solitary, aggressive vs. passive), and length of
the mouthparts in relation to flower structure. For stingless
bees, the ability to find, recruit to, and defend floral resources
varies among species, and different species select their floral
resources accordingly. For example, two species of Trigona foraging
at Cassia biflora separate on the basis of plant clump size, with the
larger aggressive species foraging at large clumps and displacing the
smaller species to isolated plants (Johnson and Hubbell 1975)* In a
study of several Trigona species, Hubbell and Johnson (1978) found
that solitary foragers were the first to find new

lU

resources, but were later displaced by larger, more aggressive group
foragers. Schaffer et al. (1979) studied foraging of three genera of
temperate bees (Apis , Bombus and Xylocopa ) on Agave schlottii, which
varied in nectar productivity along a density gradient. The solitary
species (Xylocopa) exploited the lowest density sites, and the two
social species required denser floral arrays before foraging was
initiated. These authors suggest that the cost of provisioning the
colony prevents the social species from foraging at the low
productivity sites.

The importance of nectar productivity and availability to floral
choice has also been studied in the field by Heinrich (1975, 1976a,
1979a, 1979b and references therein), Roubik and Buchmann (198*0, and
Pleasants (1981) and in laboratory situations by Real (1981), Real et
al. (1982), Waddington (1980), Waddington and Holden (1979) and
Waddington et al. (1981). Heinrich 's extensive work with Bombus spp.
has shown that individual bees learn to forage efficiently by
specializing on a single flower species that provides them with the
greatest energy reward. However, some sampling of less rewarding
flowers is maintained by the bees in order for them to monitor
changing floral resources. Pleasants (1981) also found that Bombus
chooses nectar sources on the basis of nectar productivity and
relative reward values. However, Corbet (1978) and Corbet et
al. (1979) found that the frequency of bee visits to several species of
flowers did not correspond to periods of maximum nectar availability.
Roubik and Buchmann (198M emphasize the importance of nectar
concentration to flower selectivity by Apis mellifera and suggest that
nectar of k^-60% sugar concentration maximizes the rate of energy

15

intake. They caution, however, that the net rate of energy intake is
seldom due to concentration alone.

Another important factor influencing floral selectivity in wild
bees is mouthpart length. Bees and flowers vary in the length
of their tongues and corollas, respectively. Several studies
have shown that long-tongued bees prefer long-corolla flowers and
short-tongued bees prefer open flowers (Heinrich 1976b; Inouye
1978,1980; Ranta and Lundberg I98O). Because they are inaccessible
to short-tongued visitors, flowers with long tubular corollas or
structures requiring strength to manipulate often accumulate greater
nectar rewards than open flowers, and are preferred by the
long-tongued bees, which can exploit them. Although Inouye (198O)
found that longer-tongued bees were generally more rapid in their
manipulation of the same flowers than short-tongued bees, Ranta and
Lundberg (1980) suggested that intermediate tongue lengths were most
effective. Short tongues may be more efficient at exploiting densely
packed flowers with short corollas, such as composites (inouye I98O).

Foraging selectivity of bees and wasps at artificial flower
arrays is generally consistent with predictions of energy maximization
models. Bees consistently learn to discriminate among flowers varying
in reward value (waddington I98O; Waddington and Heinrich 198l;
Waddington et al. I98I; Waddington and Holden 1979). To this
component of selectivity, Real (1981) has added the effect of
variability in nectar rewards as a factor influencing choice, and has
shown selectivity by bees and wasps for nectar sources with lower
variability in volume and thus lower variability in energy content
(Real et al. 1982).

16

The foraging behavior and energetics of insect nectarivores other
than bees has been largely ignored. In particular, the feeding
behavior of adult lepidopterans is described in the literature only
anecdotally, although Schmitt (1980) has demonstrated that bees and
butterflies foraging at the same resource differ in behavior.
Butterflies foraging at Senecio (Asteraceae) tend to visit
fewer flowers per plant and fly longer distances between plants than
do bees. She suggested that the butterflies might be foraging
suboptimally, but pointed out several differences between bee and
butterfly biology that could cause the observed differences. These
included the non-social nature of butterflies , the fact that foraging
butterflies may be simultaneously searching for mates or oviposition
sites while foraging, and the non-aggressive characteristics of
lepidopterans. Thus we might expect floral selectivity of butterflies
to be subject to different constraints than those of bees. In the
next section I will review the available information regarding the
choice of foods by adult lepidopterans.

Adult Foraging in Lepidopterans

Gilbert and Singer (1975) pointed out that the importance of
resources to adult butterflies is highly diverse but poorly
understood. Moth species of several families (Oestriidae, Gastro-
philidae, Saturniidae) emerge from the pupae as adults with
degenerate mouthparts and subsist completely on lipid

resources stored as larvae (Domroese and Gilbert I96H; Heinrich 1975;
House 197*0. At the other extreme are groups such as sphingids, which
due to their high wing-loading and hovering flight have metabolic

IT

expenditures while foraging comparable to those of hummingbirds , and
are consequently highly dependent on adult resources (Heinrich 1975).
Some butterflies, such as some tropical Heliconius species, may live
for up to six months and are highly dependent on pollen sources for
maximal egg production (Gilbert 1972). Several authors anecdotally
mention that adult resources may be a limiting factor to several
butterfly species (Heliconius charitonius, Cook et al. 1976; H.
ethilla, Ehrlich and Gilbert 1973; Chlosyne lacinia, Neck 1977) but
no evidence is presented. Clench (1967) showed that population sizes
of eleven hesperiine species were highly correlated with abundance of
major nectar sources, and that the phenologies of ecologically similar
skipper species were staggered. This suggests competition for
limiting nectar resources. He concluded that most "typical" butterfly
species may be limited by nectar resources. Murphy (1983)
demonstrated that oviposit ion by Euphydrias editha is highly dependent
on the proximity of suitable nectar sources to the larval host plants.
Scott (1973) documented extensive flights by males of four species of
lycaenids in search of nectar. Gilbert (1976) described an African
lycaenid, Megalopalpus zymna, that feeds on larval lycaenid secretions
(honeydew) and is morphologically adapted to mimic an ant in order to
elicit honeydew production and avoid aggression by ants tending the
larvae. Emmel (1971) reported an apparently mutualistic symbiosis
between an Ecuadorian skipper (Perichares philietes) and a Maxillaria
orchid. The orchid has a long, convoluted corolla that prevents
access to the nectar by most insects. The skipper has apparently
morphologically adapted to this orchid and was not observed visiting

18

other flower species. These studies suggest that in some butterflies
there is strong selection for profitable or efficient adult foraging.

Butterflies as a group feed on a wide variety of substances.
Various species have been reported feeding on floral nectar, pollen,
honeydew, froghopper secretions, rotting fruit, urine, perspiration,
dung and carrion (Gilbert and Singer 1975). Within a species,
however, food habits are more restricted. Opler and Krizek (198U)
point out that many forest-dwelling butterflies do not visit flowers.
Certain groups of butterflies tend to be associated with particular
food types. Danaine butterflies tend to be flower feeders, ithomiines
feed on nectar and bird droppings, charaxines feed on dung and rotting
plants, and among the nymphalines, the Heliconiini and Argynnini tend
to be nectar feeders whereas the Apaturini and Nymphalini are
generally not flower visitors, but may feed on sap or rotting fruits
(Gilbert and Singer 1975).

The nutrients obtained from these diverse food sources are also
varied. Arms et al. (197*0 identified sodium as the stimulus
eliciting "puddling" behavior in Papilio glaucus . This is a common
behavior in several butterfly families in which congregations of
butterflies gather to suck on wet sand or soil. Curiously, these
gatherings are usually composed entirely of young males (Adler 1982;
Adler and Pearson 1982). The behavior seems to be due to the high
sodium requirements of males for spermatophore production (Adler and
Pearson 1982). Watt et al. (197*0 studied nectar sources of several
montane Colias species and concluded that water balance may be a major
function of nectaring. Amino acids may be obtained by butterflies
feeding at dung, carrion, etc., and are certainly one of the main

19

sources of nutrition of pollen-feeding Heliconius butterflies.
Gilbert (1972) has shown that amino acids released from pollen after
soaking in nectar are rapidly incorporated into eggs and significantly
increase fecundity.

Although as a group butterflies feed on a variety of food types,
the main source of nutrition for many species is floral nectar.
Nectar composition in relation to pollinator type has been extensively
studied by Baker and Baker (1983 and references therein). Although a
variety of compounds has been detected in nectar, such as amino acids,
proteins, lipids, ascorbic acid, and alkaloids (Baker and Baker
1975), the main component of most nectars is a variety of mono- and
disaccharide sugars (Heinrich 1975; Baker and Baker I983). Most
nectars, regardless of pollinator type, contain some fructose, glucose
and sucrose, although their relative proportions vary (Baker and Baker
1983). Butterfly visited flowers tend to contain about 25% sugar
(weight /weight) (Heinrich 1975; Watt et al. 197*+; Pyke and Waser
198l), and can be divided into two groups. Butterflies visit
short-corolla, open flowers that are also exploited by other insects
(termed bee-butterfly flowers by the Bakers), and these flowers tend
to be hexose-rich (glucose, fructose). Most composites (Asteraceae)
fall into this category. Shields (1972) found that the plant family
most commonly used by butterflies for nectar is the Asteraceae. The
second type of butterfly-visited flower, comprising long-corolla
tubular flowers, is characteristic of the "butterfly pollination
syndrome" (Faegri and van der Pijl 1979) and tends to be sucrose-rich
(Baker and Baker 1983). Watt et al. (197^) suggest that hexoses may
be cheaper for the plant to manufacture, but point out that Colias

20

butterflies have the enzymatic capability of converting hexoses to
sucrose and vice-versa. Butterflies are therefore presumed to be able
to use the sugars found in most floral nectars.

The amount of nectar produced by a flower is closely related to
the metabolic needs of the pollinator (Heinrich and Raven 1972;
Heinrich 1975)* Because of the low energy demands of butterflies,
nectar availability of butterfly flowers tends to be low relative to
other pollinator types (Watt et al. 19lh; Opler 1980). In fact, no
published data exist concerning standing crops of butterfly nectar,
the amount actually available to the forager. Both Watt et al.
(1971+ ) and Opler (1980) bagged flowers to prevent insect visitation
and measured accumulated nectar after 2k hours. Opler found a maximum
availability of 0.93ul/ flower (of eight butterfly visited plant
species), and Watt et al. found between 0.1+ and 5«6ul/ flower among
16 species of flowers visited by Colias species. Opler found a
maximum nectar avilability of 9»7 ul in large-bee pollinated flowers.
Butterflies can forage at low-reward flowers because their energetic
costs while foraging are relatively low. They do not thermoregulate
by endothermy as bees do, but rather use solar energy to maintain high
body temperatures (Clench 1966; Heinrich 197^; Rawlins I98O).
Energetic cost of flight in butterflies is probably relatively low due
to their low wing-loading and ability to use wind currents for gliding
(Heinrich 1975; Casey 198l).

The selectivity and use of nectar resources by butterflies have
not been quantitatively studied. Numerous studies suggest that
butterflies feed on a limited subset of available floral resources
(Boggs et al. 198l; Neck 1977; Wiklund and Ahrberg 1978; Opler and

21

Krizek I98U; Watt et al. 197*+; Levin and Berube 1972; Ohsaki 1979;
Richman and Edwards 1976 ; Wiklund 1977 ) , although these are mainly
qualitative observations and do not attempt to determine the factors
influencing selectivity. Foraging studies of Heliconius charitonius
at artificial flowers have shown that these butterflies learn to
discriminate by color among flowers differing in nectar reward
(Swihart and Swihart 1970; Swihart 1971), and Vaidya (1969) showed
that Papilio demoleus prefers larger artificial flowers" to smaller
ones and that a fused corolla is preferable to separate petals. Root
and Kareiva (198U) compared the behavior of ovipositing versus
nectaring Pieris rapae and showed that distinctly different behaviors
were used, with nectar foraging involving more turning in order to
keep the butterfly within a restricted area. They did not quantify
selectivity between available nectar sources. Wasserman and Mitter
(1978) suggested that lepidopterans that are generalist feeders as
larvae tend to be larger than specialists, but they do not extend
their discussion to adult feeding habits. Butterflies as a group are
apparently more generalized and opportunistic in their feeding habits
than most other nectarivores (Gilbert and Singer 1975; Opler and
Krizek 1984; Clench 1966).

One factor that has been related to adult resource use in
butterflies is the relationship between proboscis length and flower
morphology. Opler and Krizek (1984 ) report on visitation patterns of
a northern Virginia butterfly community and show a positive
correlation between proboscis length and mean corolla tube length of
flower species visited. They also point out that the ratio of
proboscis length to forewing length (an indicator of body size) is

22

indicative of feeding habits of individual species. Non-flower
visitors have ratios of 0.3:1.0 or less, flower visiting butterflies
generally fall between 0.3 and 0.5:1.0, and skippers have ratios
greater than 0.45:1.0. The benefits of having such a long proboscis
have not been quantified. Other factors they feel are important in
determining flower choice are flower abundance (the most abundant
species is usually preferred) and flower color (white, blue, pink or
purple are preferred).

Nectar characteristics may also be imporant to floral
selectivity. From a theoretical standpoint, Kingsolver and Daniel
(1979) and Heyneman (1983) have constructed theoretical models that
predict that butterflies should prefer flowers with nectar
concentrations of 20-25% sucrose, as these nectars should provide the
maximal rate of energy intake during feeding. Both papers are based
on simulation models and lack empirical support, but reach the same
conclusions independently. The models are based on the physics of
fluid flow through a tube-like conduit, such as a butterfly proboscis.
In such a system, the rate of energy intake is determined by the
volumetric rate of consumption as well as the energy content per
volume, which depends on sugar concentration. Since the viscosity of
sugar solutions (which limits volume uptake rate) increases
exponentially with increasing concentration while energy content
increases linearly, the result is a decline in uptake rates at higher
sugar concentrations that outweighs the effects of increased energy
content. The maximal rate of energy intake thus occurs at moderate
concentrations. Neither model addresses factors other than nectar

23

concentration, but, if realistic, these models may have important
implications regarding floral selectivity in butterflies.

From the above discussion, it seems clear that adult butterflies
are quite variable in their dietary needs. The volumes and
concentrations of nectar sources used by butterflies suggest that
energy intake of these insects may be quite small relative to that of
other nectarivores. Yet there are suggestions, based on both
qualitative observations and theory, that some butterflies may be
selective in their choice of flowers. Is there any evidence that
adult resources or selectivity of such significantly influences
fitness? This question is considered below.

Effects of Adult Foraging on Fitness

The voluminous literature on animal foraging in the past decade
has dealt almost entirely with the immediate behavior and proximate
consequences associated with foraging decisions. Yet an underlying
assumption of all optimal foraging models is that an increase in
foraging efficiency (or rate of energy gain, or whatever quantity is
being studied) will result in increased fitness (Schoener 1971;
Mitchell 1981 ; Pyke et al. 1977). This assumption is rarely tested,
and for some organisms there is virtually no information regarding the
relationship between foraging efficiency and survival, fecundity,
longevity, or any other factor affecting fitness. Some authors of bee
studies have asserted that nectar is by far the most important source
of energy to the colony, so that increasing the energy supply will
increase the growth and reproductive success of the colony (Heinrich
1979; Pyke 198la). No data or corroborating studies are cited.

2k

For a number of organisms there are data on the relationship
between adult dietary intake and factors affecting fitness. In many
holometabolous insects, the feeding habits of adults are completely
different from those of the larvae. Even though the larva is usually
considered the main feeding stage of the insect's life cycle, dietary
intake during the adult stage can also be crucial to fully realizing
potential longevity and fecundity. Smith (1965) compared the effects
of a water diet and a diet of dried, powdered aphids to adult
coccinellid beetles of 13 species. The water diet increased longevity
over starved insects, but protein in the diet further increased
longevity and was required for egg production in some species. Finch
and Coaker (1969) studied the effects of various carbohydrates on the
survival and fecundity of the cabbage root fly, Eroischia brassicae.
In contrast to most dipterans, which must feed on both carbohydrates
and protein before egg laying, E^_ brassicae needs only carbohydrates
before laying the first egg batch. Protein is required for later
clutches. These authors showed that water alone doubled the longevity
of female flies but stimulated virtually no egg production. The
effects of different sugars were quite variable. Pentoses and hexoses
(except for glucose and fructose) resulted in poor fecundity, while
glucose and fructose increased fecundity by a factor of more than 25.
Sucrose produced the greatest fecundity increases. Interestingly,
0.1M sucrose solutions promoted greater longevity than 0.5M solutions.
They also tested the effects of a variety of wild nectars normally fed
on by the flies and found fecundity was increased in most cases.

For lepidopterans , the picture is more complex. As mentioned
earlier, some species do not feed as adults, and their resources for

25

adult activities and reproduction come solely from reserves stored by
the larvae. Thus, in Hyalophora cecropia, females contain about 9%
lipid (of fresh weight) on the second day after eclosion, while males
contain about 33%. These lipid stores fall throughout the lives of
the adults. The greater lipid content of males is attributed to the
greater metabolic expenditures of these insects incurred as a result
of searching for the sedentary females. Interestingly, these insects
use only lipids as flight fuel and cannot use glucose added directly
to the muscle (Domroese and Gilbert 1964). Similarly, in Galleria
melonella (Pyralidae), adults do not feed, and energy for adult
activities is derived from stored lipids (as indicated by respiratory
quotients between O.T5-0.77). Females use about 51% of their eclosion
energy for metabolic costs and 17% for reproduction (Carefoot 1973).

Even in species that do feed as adults, the foods ingested by the
larvae and the amount of stored reserves carried over to the adult
stage can markedly affect fitness (Beckwith 1970; Fenemore 1977;
Slansky 1982 and references therein) as well as adult morphometries
and behavior (Angelo and Slansky 1984). The effects of adult feeding
on fitness seem to be quite variable though. Fecundity and longevity
differences caused by variation in adult diet have been best studied
in several pest moth species, which show a variety of patterns. For
example, the European corn borer (Ostrinia nubialis: Fyralidae) does
not need even water in the diet to realize some egg production (Raina
and Bell 1978). In soybean loopers (Pseudoplusia includens :
Noctuidae) the inclusion of sugar in the diet increases fecundity over
starved and water-fed moths. Similarly, in cabbage loopers
(Trichoplusia ni: Noctuidae) the number of eggs laid is directly

2b

related to the sugar concentration on which the adults are fed (Raina
and Bell 1978 ) . In the pink bollworm (Pectinophora gossypiella:
Gelechiidae) the number of eggs laid is increased by sucrose or honey
in the diet, but viability of these eggs is no greater than those
produced by starved or water-fed moths. The same effects were seen in
the cotton leaf perforator (Bucculatrix thurberiella: Lyonetiidae)
(Benschoter and Leal 1976), where fecundity increases to a maximum
with k0% sucrose solutions. In the potato tuber moth (Pthorimaea
operculella: Gelechiidae), however, fecundity is higher on a 5%
sucrose diet than on more concentrated diets (El-Sherif et al. 1979).
In studies of the same species, Fenemore (1977, 1979) found that water
feeding alone doubled the fecundity over that of starved moths , but
that sucrose did not further increase egg production. Labeyrie (1957)
found however that honey caused a tripling of fecundity over that of
starved moths, leading Fenemore (1979) to conclude that honey contains
important nutrients other than sucrose.

Among the butterflies, effects of adult feeding on fitness are
not as well known as in moths. Stern and Smith (i960) studied the
factors affecting egg production in Colias philodice eurytheme
(Pieridae) and found that egg production is supported in part by fat
stored during the larval stage. However, the presence of sugar in the
diet decreases the rate at which the fat body is depleted and
increases the number of eggs laid. Water alone tripled the fecundity
of females as compared to starved individuals. Starved individuals
usually lived no more than 6 days compared to a normal lifespan of
2^-30 days. The presence of sucrose in the diet causes another
tripling of egg production over that of water-fed females. Gilbert

27

(1972) showed that Heliconius butterflies rapidly incorporate amino
acids from pollen-feeding into eggs, and that pollen-feeding
significantly increases egg production over nectar-feeding alone.
Brower (in press) has shown that migrating monarchs
build up lipid stores while in the southern U.S. Tuskes and Brower
(1978) suggest that the amount of stored lipid possessed by an
individual monarch arriving on the overwintering grounds is an
important factor determining the probability of surviving the winter
as well as the distance to which that butterfly can remigrate the
following spring.

The most detailed study of the importance of adult resources to
fitness is that of Murphy et al. (1983) on the nymphalid Euphydryas
editha. They fed female butterflies on six different diets and
measured weight change, survival and fecundity. The diets included
starvation, water only, 20% sucrose, water and O.OO^M amino acids, and
20% sucrose plus O.OOHM or 0.02M amino acids. The most significant
increases in fecundity and longevity were due to sugar in the diet.
Weight declined most rapidly in the water-fed group, less quickly in
the water/amino acid diet, and least quickly in the sucrose and
sucrose/amino acid treatments. Fed females lived longer than unfed
ones, and the maximum longevity was seen in the sucrose diets. The
sucrose diets increased fecundity, but only in later egg masses.
Amino acids did not increase fecundity, but did increase the weight of
later eggs, which directly affects hatchability. They found no effect
of increasing amino acid concentration above that normally found in
floral nectar. They concluded that since early egg masses contribute
more to fitness than later ones (because larval foodplant quality

28

declines in the latter part of the season and many caterpillars die),
adult feeding increases fitness only in wet years when later egg
masses have a chance of surviving. Murphy and his colleagues also
speculated that populations without nectar sources may be at a higher
risk of extinction in dry years.

It thus seems clear that adult diet can have significant effects
on fitness. Furthermore, adult dietary requirements may depend to a
large degree on the amount of stored resources provided by the larval
stage. Boggs (1981) has discussed this interdependence between larval
and adult feeding requirements in holometabolous insects. She
reasoned that the potential reproductive effort of an insect depends
on the proportion of larval resources allocated to reproductive
reserves plus the overall proportion of adult-acquired nutrients to be
allocated to reproduction. This leads to the prediction that resource
allocation during metamorphosis should be adjusted relative to the
expected adult nutrient intake. Boggs tested this prediction using
three species of heliconiine butterflies (H^_ cydno, H. charitonius
and Dryas julia). She examined nitrogen budgets of these animals and
estimated the proportion of nitrogen earmarked for reproduction as the
ratio of abdominal N to total body N. This proportion is independent
of body size as predicted. The three species differ in the extent of
pollen-feeding exhibited as adults (D^ julia does not feed on
pollen). As predicted, the greater the amount of pollen-feeding as an
adult, the lower was the proportion of reproductive nitrogen to total
nitrogen in the newly emerged adult. IK_ julia stores the largest
amount of reproductive nitrogen from larval feeding and this stored
nitrogen declines most rapidly in this non-pollen feeding species.

29

Boggs concluded that an adjustment in overall adult nutrient intake is
accompanied by a concomitant change in allocation of larval reserves
at metamorphosis. This hypothesis has not been tested with nutrients
other than nitrogen. Most butterflies do not feed on pollen (Gilbert
1972) , however, and the major adult dietary component is sugar from
floral nectar. We should thus see a similar relationship between
expected adult energy intake and larval energy reserves stored (as
lipid) for adult activities.

General Approach of This Study

Clearly, foraging behavior of adult insects is affected by a
large number of factors that determine the extent of adult feeding and
the choice of food items. I have reviewed models and data regarding
energetic considerations in food choice, including mechanical
constraints as well as parameters of the reward itself (such as nectar
concentration and volume) that affect the rate of energy intake. The
dispersion of food items may also affect the rate of energy intake
while foraging. Also, the selection of nectar resources by the adult
insect can be based upon morphological properties (proboscis length
and corolla tube length), and on the patterns of nutrient storage by
larval stages. Finally, to understand fully the foraging decisions
made by a species requires some knowledge of the effects of the chosen
food items or nutrients contained therein on fitness parameters.
Below I review the purpose and plan of each of the following sections
with regard to the above considerations.

Chapter II addresses the theoretical modes of Kingsolver and
Daniel (1979,1983) and Heyneman (1983). These models are based on the
mechanics of fluid flow through nectarivore mouthparts and predict

30

that certain nectar concentrations (20-25% for butterflies) will
maximize the net rate of energy intake of the feeding animal and
should therefore be preferred by the foraging insect. I present data,
heretofore lacking, that address the applicability of these models to
butterflies. These data were collected from two common butterfly
species (described in detail below). The same species, Agraulis
vanillae and Phoebis sennae, are considered in subsequent chapters as
well.

Chapter III pertains to the nectar sources used by these two
species and the characteristics thereof. Combining data on energetic
rewards offered by these nectar sources with time budget data on
foraging behavior, I construct energy budgets to estimate foraging
profits offered by the various flower species. I use these estimates
to determine which floral characteristics (nectar volume,
concentration, corolla length, floral density) most significantly
affect the energetic profits obtained by the butterflies. Data are
also considered that deal with the effect of differing morphologies
(proboscis length) on flower visitation. Using observations on the
two species foraging in the same floral arrays , I demonstrate that
these species do differ in foraging selectivity. Finally, data from a
mark-recapture study of Agraulis are considered with respect to the
effects of mobility on flower selectivity.

In Chapter IV, I compare the stored larval resources (lipids) of
the two species in light of the observed differences in flower
selectivity and foraging energetics described in Chapter II, in order
to test Boggs' (I98l) hypothesis of larval reserve-adult feeding
interdependence. I also examine the change in lipid stores over the

31

adult lifespans of the two species, and relate differences in fat
storage and depletion to foraging behavior.

Chapter V considers the effects of sugar components of nectar on
various components of fitness such as fat storage, longevity and egg
production. I describe in this section feeding experiments designed
to determine the effect of varying the level of energy intake of adult
Agraulis vanillae on these factors. Data are also presented which
address the effect of larval feeding success on adult fecundity.

Finally, I present a general discussion in Capter VI of the
entire set of studies and summarize the major conclusions.
Biology of the Study Species

The gulf fritillary, Agraulis vanillae nigrior (Nymphalidae:
Heliconiinae) ranges from the southern U.S. through central
America to Argentina. In the Alachua Co., Florida, area it is a
common inhabitant of open areas, such as old fields, roadsides and
pastures (Opler and Krizek 1984). Breeding populations are restricted
to the vicinity of the larval food plant, Passiflora incarnata
(Arbogast 1965 ) , which is commonly found in a variety of disturbed
habitats. Eggs are laid singly on older leaves, and the period
between oviposition and eclosion as an adult lasts 22-28 days.
Breeding in the Alachua Co. area is continuous from April-May to
November. Adults live lH-21 days, and only adults overwinter
(Opler and Krizek 1984). This species apparently does not overwinter
in Alachua Co. (Arbogast 1965), and is presumed to recolonize
northern Florida each spring from overwintering populations in
southern Florida. Extensive southward migrations occur from September

32

to November, and a less distinct remigration occurs in April-May
(Walker 1979)* Details of the migration are unknown.

The cloudless sulphur, Phoebis sennae eubule (Pieridae), is also
a common inhabitant of open habitats in Florida. It ranges from the
southern U.S. (with occasional incursions farther north) through
central America to Argentina (Opler and Krizek 1984). The adults are
most commonly found in the vicinity of the larval host plants (Cassia
obtusifolia and Cj_ fasciculata) , but are apparently not as restricted
to local concentrations of the food plant as in Agraulis. Although
there is a large southward migration from September-November (Walker
1979), some individuals overwinter in the Alachua Co. area and can be
seen flying in small numbers on warm days throughout the winter. Only
adults of this species overwinter also (Opler and Krizek 1984).
Though adults can be seen throughout the year, sizable numbers are not
usually seen until August-September when the Cassia foodplants mature.
Population sizes near the food plants tend to be smaller than those of
Agraulis populations around Passiflora. Howe (1975) noted that wide
fluctuations in populations are characteristic of Phoebis species.
Although the longevity of adults is unknown, it is apparently greater
than that of Agraulis , because overwintering Phoebis adults are in
reproductive diapause and presumably survive to remigrate inthe spring
(Opler and Krizek 1984).

Both species are often abundant in the north Florida area. Both
frequent open habitats, making observation practical. Finally, both
are avid flower visitors and floral nectar is apparently the major
component of the adult diet. They are thus ideally suited for
comparative studies of many aspects of adult foraging.

CHAPTER II

NECTAR UPTAKE RATES OF AGRAULIS VANILLAE

AND PHOEBIS SENNAE: EFFECT ON OPTIMAL

NECTAR CONCENTRATIONS

Introduction

Ecologists in recent years have devoted much attention to the

foraging behavior of animals, particularly addressing the problem of

dietary optimization (Schoener 1971; Pyke et al. 1977).

Many theoretical studies have yielded predictions about foraging time

allocation, prey selectivity, habitat utilization, and other

behavioral decisions regarding foraging behavior, whereas other recent

models have considered mechanical aspects of the feeding structure in

an attempt to identify physical optima regarding food choice. In

particular, the models of Kingsolver and Daniel (1979,1983) and

Heyneman (1983) have addressed the feeding mechanics of nectarivores

and have derived predictions regarding optimal nectar concentrations.

The Heyneman (1983) model, applicable to nectarivores in general,

predicts that nectar of 20-25% sucrose concentration yields a maximal

rate of energy intake. Kingsolver and Daniel have applied two

different approaches to nectar feeders that result in different

predictions depending on the feeding mechanism. One model (Kingsolver

and Daniel 1979), designed for suction feeders such as butterflies

that feed continuously in a steady-state fashion, also predicts that

20-25% sucrose concentrations maximize the rate of energy intake.

33

31*

Interestingly, field studies of nectar composition from
butterfly-visited flowers have found sugar concentrations to average
about 25% (Pyke and Waser 198l; Watt et al. 197h). The second model
(Kingsolver and Daniel 1983), which applies to non-steady-state
feeders that rely on cyclic filling and emptying of the feeding
apparatus (such as the tongue of a hummingbird), predicts that 35-^0%
sucrose solutions maximize the rate of energy intake. While these
models stress the importance of mechanical constraints (especially the
effects of viscosity) in determining the optimal nectar concentration,
other workers (Pyke and Waser 198l) minimize the effects of these
mechanical factors and have argued that energy intake rate should
increase with increasing sugar concentration. According to Pyke and
Waser (1981), the optimal nectar concentration (for hummingbirds) is
around 70% sucrose.

The rate of energy intake is crucial to most optimal foraging
models, as it is this quantity that is generally assumed to be
optimized while foraging (Pyke, Pulliam and Charnov 1977 )• The
Kingsolver-Daniel (1979) model predicts that a 20-25% sugar
concentration provides the maximal rate of energy intake while the
butterfly is actually feeding. This optimum occurs because the energy
content of nectar increases linearly with increasing sugar
concentration, while the viscosity increases exponentially. The
exponential increase in viscosity limits the rate of nectar uptake at
higher concentrations and causes the rate of energy intake to decline
above 20-25% sucrose. The mathematical form of this model
is summarized in Table 2-1. In their model simulations, Kingsolver
and Daniel (1979) and Heyneman (1983) estimated uptake rates

35

TABLE 2-1 - A SUMMARY OF THE KINGSOLVER-DANIEL (1979)
FEEDING ENERGETICS MODEL

1 diff in ~ met ~ mech

where Ej-ff = net rate of energy intake

E. = gross rate of energy intake

E = metabolic rate of feeding insect

Eme , = mechanical energy required to pump nectar
mech

2) E. = QRAS/100

in

where Q = nectar uptake rate
R = nectar density
A = energy content of sugar
S = nectar concentration

3) Emech " (P1 " V Q/E

where E = muscle efficiency

other terms as above or as in equation k

k) P - P2 = 32V1uL(l+C+C2)/3D12C3 - rY^H-l/^) /2

where P - P = pressure drop generated by sucking insect
VT = nectar velocity at distal end of proboscis
L = proboscis length
u = nectar viscosity
r = nectar density

D = proboscis diameter at distal end
C = constant obtained by dividing proximal diameter
of proboscis channel by distal diameter

36

by assuming that the nectarivores exert a constant pressure drop at
all nectar concentrations. The pressure drop is the change in
pressure between the proximal and distal ends of the proboscis (due to
frictional losses and change in diameter of the feeding channel), and
this quantity along with nectar viscosity and the morphology of the
proboscis determine the nectar uptake rate. The assumption of
constant pressure drop predicts that uptake rates decline
curvilinearly with increasing sugar concentration. They
estimated the net energy intake rate from predicted uptake
rates of the feeding animal. The uptake rates are critical to the
rate of energy intake, since uptake rate (volume/time) multiplied by
energy content of the nectar (energy /volume) determines the energy
intake rate. As mentioned by Kingsolver and Daniel (1979), the
mechanical cost of pumping the nectar (E , ) should be
negligible. Since metabolic rate of feeding insects is assumed to be
independent of nectar concentration and thus does not affect the
optimal concentration, it will be ignored here. % purpose is to
examine the relationship between nectar concentration and nectar
uptake rates. This relationship, which is crucial to estimating
energy intake rates, requires empirical support. Specifically, I
present data that test the pressure drop assumption and uptake rate
predictions of both the Kingsolver-Daniel (1979) and Heyneman (1983)
models. The actual nature of the concentration-uptake relationship
necessitates modifications of the predictions of these models
concerning both the sucrose concentration of the "optimal" nectar as
well as the evolutionary importance of such an optimum with regard to
natural selection for food choice in these nectar feeders.

37

Methods and Materials

I captured adult Agraulis van i 11a e (Nymphalidae) and Phoebis
sennae (Pieridae) while they were feeding at nectar sources at field
sites on Paynes 's Prairie State Preserve, Alachua Co., Fla. I
maintained them in the laboratory by keeping each individual in a
glassine envelope in a plastic box at room temperature. The boxes
were kept at high humidity to prevent dessication. Each butterfly was
kept for five days , during which time it was allowed to feed once a
day and its nectar uptake rates measured. Each butterfly was fed with
solutions of 10,20,30,^0 and 50% sucrose concentration
(weight /weight ) . The five concentrations were presented to each
individual butterfly on consecutive days in a random order, so that
during captivity each butterfly was fed once at each concentration. I
released all butterflies at the end of the five-day test period.

I measured the insects' nectar uptake rates of by inducing the
butterflies to feed from lOOul microcapillary tubes (Drummond
microcaps) that had been filled with sucrose solution of known
concentration. The microcap was mounted on a small balsa platform
alongside a millimeter scale (see Appendix). I placed the
butterfly on a perch in front of the platform and induced it to feed
by uncoiling its proboscis manually and touching the tip to the nectar
inside the microcap. The rate at which the rear meniscus of the
nectar column moved along the millimeter scale was timed with a
stopwatch. I made three to five measurements for each butterfly
during a feeding bout and averaged these figures to obtain one
uptake rate per butterfly at each concentration. As both species
maintain body temperatures in the field that are 6-8 C above ambient

38

temperature (see Chapter III)', and since nectar uptake rate of
these poikilothermic insects is most likely related to body
temperature, the entire procedure was performed inside a styrofoam
chamber that was heated to 28 C. Before each butterfly was tested
it was allowed to warm up to flight temperature in the chamber. The
procedure is described in the Appendix and in May (in press).

Because the amount of nectar imbibed by butterflies was not
controlled, the actual caloric value of each butterfly's daily meal
varied. (This depended on the uptake rate of that individual, the
nectar concentration that was tested on that particular day, and
feeding duration, which varied depending on how quickly the
required measurements could be made. ) To determine whether or not this
variation in energy intake affected the uptake rates, I measured
uptake rates of two groups of butterflies receiving diets of the same
sucrose concentration but different caloric content over a five-day
period. One group received 12.9 ul of 30% sucrose nectar per day, or
0.21 Joules/day (this corresponded to 15 mm on the scale) and the
other received 3^. 5 ul per day, or 0.57 Joules /day (Uo mm on the
scale). The low-energy group consisted of k male and 2 female
Agraulis vanillae, and the high-energy group consisted of 2 male and 3
female Agraulis vanillae. The daily energy contents of the diets for
the two groups encompassed the range of energy contents of the diets
received by the butterflies used in the main uptake rate measurements.
This design also allowed me to test for effects of age (over a
five-day time span) on uptake rate.

39

I measured proboscis lengths by excising the proboscides at the
bases, mounting them on clear glass slides with transparent tape, and
measuring them with a millimeter scale. Proximal and distal diameters
of the internal feeding channel of each proboscis were measured by
scanning electron microscopy.

Results

Proboscis measurements are presented in Table 2-2. The length of
the proboscis and the proximal and distal diameters of the
feeding channel are parameters of the Kingsolver-Daniel (1979) model.
These measurements were taken without regard to sex. Internal
diameters of the feeding channels do not differ greatly between the
two species, but Phoebis sennae has a proboscis that is a full
centimeter longer than that of Agraulis vanillae. According to
Kingsolver and Daniel (1979) this should result in lower nectar uptake
rates and therefore lower energy intake rates for Phoebis. The ratio
of proximal diameter to distal diameter of the feeding channel, C,
is slightly larger in Phoebis, indicating that the feeding channel of
Phoebis is more sharply tapered than that of Agraulis. The uptake
rates of both species differ considerably from those predicted by the
models, particularly at low sucrose concentrations (Figures 2-1
and 2-2). The predicted curves were obtained using the equations of
Kingsolver and Daniel (1979) and the proboscis dimensions of
Agraulis and Phoebis by assuming a constant pressure drop of
one bar. Two-way ANOVAs indicate that there are
significant effects of both sex and concentration on volume
uptake rates for both species (Table 3-2). All regressions of uptake

ho

TABLE 2-2 - PROBOSCIS DIMENSIONS OF AGRAULIS VANILLAE AND PHOEBIS
SENNAE. [mean + 1 standard deviation (n)j

Agraulis

SPECIES

Phoebis

Length (cm) 1.92 + 0.18 (l8)

Proximal

diameter (um) 79. 5 + 3.31 (U)

Distal

diameter (um) 59. 7 + 2.20 (k)

Ca 1.33 + 0.09 (U)

2.95 + 0.22 (9)

86.5 + 3.hk (2)

55.^ ± 27.1 (2)
1.56 + 0.01 (2)

C = proximal diameter/ distal diameter

Ul

TABLE 2-3 - RESULTS OF TWO-WAY ANOVAS OF NECTAR UPTAKE RATES VS.
CONCENTRATION AND SEX. Uptake rates as a function of concentration
are presented in Figures 2-1 and 2-2. Analyses of variance indicate
that both sex and nectar concentration significantly affect uptake
rate.

Agraulis vanillae

Two-way analysis

of

variance

F

Source

DF

MS

p

Sex

Nectar cone

Interaction

1
1+

0.152
0.752
0.009

25.27

12^.78

1.U5

< 0.0001

< 0.0001
> 0.21

Phoebis sennae

Two-way Analysis

of

Variance

F

Source DF

MS

P

Sex 1
Nectar cone. k
Interaction k

0.076
0.927
0.007

6.67

81.71

0.61

< 0.011

< 0.0001

> 0.65

U2

Agraull* vanilla*

• MALES
O FEMALES

% SUCROSE

Figure 2-1 - Predicted and observed nectar uptake rates (mean +. one
standard error on either side of the mean, in ul/s) as a function of
nectar sucrose concentration (weight /weight ) in Agraulis vanillae.
Given are means + one standard error. Predicted curve based on
Kingsolver and Daniel (1979) assuming a pressure drop of one bar at
all concentrations.

1+3

%SUCROSE

Figure 2-2 - Predicted and observed nectar uptake rates (mean + one
standard error on either side of the mean, in ul/s) as a function of
nectar sucrose concentration in Phoebis sennae. Given. are means + one
standard error. Predicted curve based on Kingsolver and Daniel (1979)
assuming a pressure drop of one bar at all concentrations.

kk

rate on nectar concentration are highly significant (Agraulis males:
n = ll6, F = Ul8.1, p < 0.0001; Agraulis females: n = 101, F =
158. 7, p < 0.0001; Phoebis males: n = 108, F = 183.0, p < 0.0001;
Phoebis females: n = 66, F = 150.2, p < 0.0001.). There were no
significant differences in uptake rates between the two groups
receiving different amounts of energy in the diet (Table 2-k); i.e.,
uptake rates are independent of energy intake within the range of
diets used in this study. In addition, the two-way AN0VA indicates
that there is no effect of day number on uptake rate over the five-day
course of the experiment. I therefore conclude that failure to
control rigidly daily energy intake did not affect the uptake rate
measurements presented in Figures 2-1 and 2-2.

Using the measured uptake rates and proboscis dimensions
for each species, I calculated the rates of energy intake,
E. (uptake rate multiplied by energy content of the nectar);
E , the mechanical energy required to pump the nectar;
E,.„ , the net rate of energy intake; and P - P?, the pressure
drop produced at each concentration (Table 2-5). (Viscosity
data are from Weast [197^1 •) These data show that a) the butterflies
do not produce a constant pressure drop at all nectar concentrations,
but instead increase pressure drop with increasing sucrose concen-
tration of the nectar; b) that this pressure drop exceeds 1 bar (as
calculated by equation 1 in Table 2-1) at higher concentrations; and
c) that the optimal sucrose concentration, i.e., that concentration
providing the maximum rate of energy intake, is from

k5

TABLE 2-1+ - UPTAKE PATE VS.
one standard deviation (n)]

DAILY ENERGY CONTENT OF DIET. [mean +

Day #

Daily Energy Intake
0.57 Joules /day 0.21 Joules /day

Uptake Rates (in ul/s)

0.1+09 + 0.050 (6)

0.1+U3 + 0.01+0 (6)

0.1+06 + 0.061+ (6)

0.1+36 ± 0.06U (6)

0.1+05 + 0.139 (6)

0.1+18 + 0.095 (5)
0.1+1+T + 0.111+ (5)
0.1+31* ± 0.097 (5)
0.1+36 + 0.091 (5)
0.1+15 + 0.116 (5!

Two-way analysis of variance

Source

DF

MS

Energy content
Day number
Interaction

0.0015
0.0018
0.0010

0.18
0.22
0.11

> 0.67

> 0.92

> 0.97

1+6

TABLE 2-5 -

- FEEDING ENERGE
calculations.

TICS OF AGRAU

LIS AND PHOEBIS

5. See text for

details of

E.
in

Emech Ediff

P - P
1 2

%sucrose

Gross rate of

Mechanical

Net rate of

Pressure

energy intake
(Watts )

energy
(Watts)

energy intake
(Watts)

drop
(Bars)

Phoebis sennae

- males

10

20

30
1+0
50

1.1081+
1.8712
2.6398
2.6525
1.1+299

Phoebis sennae

0.000151
0.000171
0.000228
0.000230
0.000177

- females

1.0182
1.8710
2.6396
2.6523
1.1+297

0.1+7!+
0.609
0.901
1.257
1.71+6

10
20
30
1+0
50

0.9956

1.8012
2.21+1+1
2.1699
1.8556

0.00011+1+
0.000159
O.OOOI65
0.000153
O.OOOI65

0.9955
1.8011

2.21+39
2.1668

1.8551+

0.1+63
0.586
0.766
1.027
1.686

Agraulis vanillae - males

10
20
30
1+0
50

O.9I+8O
1.61+81
1.9109
2.1017
1.7791

0.000125
0.000127
0.000111+
0.000138
0.00011+5

0.9V79
1.61+80
1.9108
2.1016
1.7790

0.1+22
0.513
0.623
0.952
I.5I+6

Agraulis vanillae - females

10
20
30
1+0
50

0.8112
1.31+18
1.7599
1.7575
1.1+106

0.000092
0.000081+
0.000097
0.000097
0.000091

0.8111
1. 31+17
1.7598
1.7571+
1.1+105

0.361
0.1+17
0.57h
0.796
1.225

hi

35-^0% rather than 20-257». The calculations of pressure drop are
based on an assumption of steady state flow (for other assumptions see
Kingsolver and Daniel [ 19791 )• Observations of feeding butterflies
indicate that the flow is not steady state. The butterflies seem
to vary pressure drop while feeding because the nectar being removed
from the microcapillary tubes moves in pulses. The pressure drop
calculations should therefore be taken as rough approximations.

The observed rates of energy intake differ from those
predicted by Kingsolver and Daniel (1979) (Figs. 2-3 and 2-4).
These predicted curves were derived from the actual proboscis
dimensions given in Table 2-2 and the model of Kingsolver and Daniel
(1979), assuming a constant pressure drop of 1 bar. This assumption
predicts a higher rate of energy intake at all sucrose concentrations
for Agraulis than for Phoebis. Since Phoebis has a longer and
slightly narrower proboscis, the Kingsolver and Daniel (1979) model
predicts lower uptake rates and consequently lower rates of energy
intake for this species. In fact, Phoebis has a higher rate of energy-
intake at any nectar concentration (Table 2-5) because of the greater
pressure drops generated and the greater uptake rates produced
(Figures 2-1 and 2-2). Table 2-5 illustrates two additional points:

a) pressure drops increase with increasing nectar concentration, and

b) males have greater rates of energy intake due to the higher uptake
rates. Higher uptake rates in males are presumed to be the result of
greater pressure drops produced by males. Alternatively, sexual
dimorphism in proboscis dimensions might cause this difference.
Regardless of the basis for the difference between males and females,
the assumption of constant pressure drop that is central to the

48

CO

<

Ui

<

Z
>

o

£t
Ui

Z
UJ

u_
O

UJ

<
QC

5-|

4-

3-

2-

I-

% SUCROSE

Figure 2-3 - Predicted and observed rates of energy intake (watts) of
feeding butterflies as a function of sucrose concentration in Agraulis
vanillae. Predicted curve based on Kingsolver and Daniel (19791
assuming a pressure drop of one bar at all concentrations. See text
for details.

U9

% SUCROSE

Figure 2-4 - Predicted and observed rates of energy intake (watts) of
feeding butterflies as a function of sucrose concentration in Phoebis
sennae. Predicted curve based on Kingsolver and Daniel (1979)
assuming a pressure drop of one bar at all concentrations. See text
for details.

50

theoretical models is not upheld, and consequently the optimal sucrose
concentration is shifted upward. In addition, the ecological
significance of this optimum is likely to be less important than
suggested by the model simulations, as the relative increase in energy-
intake rate around the optimum sucrose concentration is not as great
as the models predicted. That is, the empirically determined graph of
energy intake vs. sucrose concentration is not as sharply peaked as
the original simulations suggested.

Examination of the data in Table 2-5 shows that E is

mech

negligible with respect to the energy content of the nectar, and the
major factor influencing the net rate of energy intake is simply the
volume uptake rate.

Discussion
The data presented here suggest that modification of the original
theoretical models is in order, and they raise new questions about the
energetics of feeding butterflies. Contrary to the assumption of the
Kingsolver and Daniel (1979) and Heyneman (1983) models, neither
species exerts a constant pressure drop at all nectar concentrations.
Instead, both butterflies increase suction pressure with increasing
nectar concentration. This is enigmatic, as they could greatly
increase the rate of energy intake at lower nectar concentrations by
exerting the pressure drops that they produce at higher nectar
concentrations. The fact that they do not produce greater suction at
lower nectar concentrations suggests that there may be some physical
limit on the rate at which the feeding apparatus can accept nectar.
Producing a high pressure drop with a low concentration nectar might
exceed this limit. Alternatively, if the insects are under little or

51

no selection pressure to maximize energetic efficiency of foraging or
minimize feeding time, there may be no advantage to producing higher
uptake rates.

If these species are under selection to maximize the rate of
energy intake, then the data here suggest that they should selectively
forage at flowers with 35-^0% sucrose nectars, as these nectars
provide the greatest energetic return per unit time. The intensity of
selection to forage at the "optimal" nectar concentration, however, is
probably weaker than suggested by the Kingsolver-Daniel (1979) and
Heyneman (1983) models since the increase in energy intake realized by
feeding at the "optimal" concentration is not as great as predicted by
their simulations. Surprisingly, the nature of this empirically
determined optimum and the shape of the energy intake vs.
concentration curve are similar to those predicted by Kingsolver
and Daniel (1983) for discontinuous feeders such as hummingbirds.
While measuring the uptake rates of both species I observed pulsing of
the nectar in the microcapillary tube as the butterflies were feeding,
suggesting that butterfly feeding may be a discontinuous
process. If so, then the Kingsolver and Daniel (1983) model
may more accurately describe the energetics of feeding in these
insects than does the earlier model for suction feeders. This latter
model is based on a feeding structure that relies on capillary flow of
nectar to fill the apparatus rather than suction, however, so it is
not directly applicable to butterflies without modification.

Particularly curious is the male-female dichotomy in uptake
rates. Males have higher nectar uptake rates, resulting in greater
rates of energy intake at any given nectar concentration. Females of

52

Agraulis vanillae are significantly larger than males , so one might
expect the females to be able to generate greater suction pressure and
thus greater uptake rates. (Males and females of Phoebis sennae do
not differ in size. ) As a proximate mechanism, sexual dimorphism in
proboscis morphology could also cause differences in uptake rates and
energy intake rates. However, since females of Agraulis vanillae are
larger in body size, they would be expected to have larger
proboscides, and thus produce greater uptake rates than males exerting
a similar pressure drop. Females must bear the energetic expense of
egg production, suggesting at an ultimate level that selection for
maximizing the energy intake rate might be greater than in males.
However, neither of these alternatives is suggested by the data.
Males may be under greater selective pressure to maximize foraging
efficiency and/or minimize foraging time because of the energetic and
time expense associated with finding females and courting them.
Stanton (1982) and Kingsolver (1983) showed that males of some
Colias species spend a greater amount of time in flight and make
longer flights than females. Males of the two species described here
seemed to spend a greater amount of time in vigorous flight around
nectar sources, chasing both females and other males. A
female may be as easily found by a male when she is feeding as when
she is in flight, and therefore there may be weak selection for
females to minimize feeding time. Searching for mates by males may
require active searching while in flight, which imposes obvious time
and energy constraints on foraging.

One important caution concerning these models should be
mentioned. The models discussed here make the implicit assumption

53

that nectar concentration is the major factor affecting the rate of
energy intake by a foraging butterfly. Several other unrelated
factors may also affect the rate of energy intake while these
butterflies are foraging. If they were offered unlimited quantities
of nectar varying only in concentration, with foraging involving no
more than imbibing nectar, then 35-^0% sucrose nectars would provide
the greatest rate of energy intake. Butterflies foraging at real
flowers, however, spend only a small fraction of foraging time
actually extracting nectar. Most foraging time is spent in transit
between flowers or in handling time (Chapter III). Heyneman
(1983) incorporates the effect of transit costs into her model and
suggests that increasing travel costs will raise the optimal nectar
concentration. In addition, since the butterfly's rate of energy-
intake while foraging is dependent in part on the number of flowers
visited per unit time, a nectar source that occurs in dense
concentrations but is of a nonoptimal concentration could be more
profitable than a nectar source that is of the optimal concentration
but occurs at low density. Further, once a butterfly has reached a
flower, it must find the nectaries. A long-corolla flower with
relatively inaccessible nectar and high handling time can lower the
rate of energy intake by decreasing the proportion of foraging time
devoted to actually imbibing nectar (Heinrich I983). Finally, nectar
does not occur in unlimited quantities but in small discrete packets,
often in minuscule amounts (Watt et al. 197*+; Chapter III). If there
is great variation in volume among nectar sources, this could nullify
the energetic benefits of feeding at the "optimal" nectar
concentration. More complex models incorporating the effects of

5h

variation in nectar concentration, nectar volume, flower density and
handling time on foraging profitability may be necessary for a full
understanding of foraging behavior in these nectarivorous animals. An
important question to be addressed in the next chapter, then, is what
are the relative values of single-factor approaches (such as the
concentration models here) and multi-factor approaches in describing
the energetics of foraging in nectar ivores?

Summary
Mechanical models of butterfly feeding energetics have predicted
that the maximum rates of energy intake of butterflies imbibing nectar
occur when sugar concentration of the nectars are between 20 and 25%
sucrose. This prediction is based on the assumption that the
butterflies exert a constant pressure drop at all nectar
concentrations (assumed in the original simulations to be one bar). I
measured uptake rates of Agraulis vanillae and Phoebis sennae and
found these rates to deviate significantly from those predicted by the
models. These butterflies vary the pressure drop produced as a
function of nectar concentration; pressure drop is increased with
increasing sugar concentration (and therefore viscosity) of the
nectar. Calculated pressure drops range from 0.36 to 1.8 bars. One
effect of varying pressure drop in this mannner is to produce lower
uptake rates at low nectar concentrations than those predicted by the
original models. In addition, males of both species produce greater
pressure drops and uptake rates than do females. Since energy intake
rate is determined by the volume uptake rate (volume imbibed/time)
multiplied by the energy content (energy /volume) of the nectar, these
butterflies exhibit lower rates of energy intake at low nectar

55

concentrations (since pressure drop is less than one bar) than
predicted by the models. Higher rates of energy intake are exhibited
at higher nectar concentrations than predicted, since pressure drop is
greater than one bar. The empirically determined energy intake rates
show that the optimal nectar concentration (that concentration
maximizing the energy intake rate) is between 35 and hQ% sucrose
rather than 20 and 25%.

CHAPTER III
FLOWER SELECTION AND THE ENERGETICS OF FORAGING IN AGRAULIS VANILLAE

AND PHOEBIS SENNAE

Introduction

The importance of nectar sources to adult butterflies is not well
known. Clench (1967) argued that nectar sources were a limiting
factor to several species of hesperiines, based on the synchrony of
flowering phenologies of several nectar sources and the numbers of
adult skippers. Shreeve and Mason (198O), however, found that the
number of butterfly species in a woodland habitat was not related to
the abundance of nectar sources, and Sharp, Parks and Ehrlich (197^)
found little correlation between abundance of nectar sources and
numbers of several butterfly species. Sugar in the diet of adults has
been shown to increase both fecundity and longevity for Colias (Stern
and Smith i960) and Euphydryas (Murphy et al. 1983) butterflies and
for several moth species including Bucculatrix thurberiella
(Lyonettiidae) (Benschoter and Leal I98O), Pectinophora gossypiella
(Noctuidae) (Raina and Bell 1978), and Phthorimaea operculella
(Gelechiidae) (El-Sherif, Gomez, and Hemeida 1979, Fenemore 1979).

If the energy derived from nectar sources is critical to adult

butterflies, natural selection should favor foraging behavior that

maximizes the energy intake rate while they forage at these resources.

I have shown in Chapter II that energy intake is maximized at nectar

concentrations of 35-^0% sucrose rather than 20-25% as suggested by

56

57

Kingsolver and Daniel (1979) and Heyneman (1983). Yet Roubik and
Buchmann (198U) caution that foraging success is rarely due to the
effects of nectar concentration alone. Other variables affecting
foraging success include nectar volume, flower handling times, and
flower density (and hence travel costs). Thus it is important to
evaluate the relevance of single factor models, such as Kingsolver and
Daniel (1979), to modeling phenomena that are known to be affected
by a variety of factors, such as the energetics of foraging butter-
flies. The relationship between variables such as volume, floral
density, and handling times and foraging energetics has not been
investigated for any butterfly species, and surprisingly little is
known about the quantitative characteristics of butterfly nectar
sources in general. Watt et al. (197M investigated nectar resource
use by two montane Colias species and found that the butterflies
chose nectar sources that tended to be rather dilute in sugar
concentration (about 25% sugars) and rich in monosaccharides. Nectar
availability was measured, but only after preventing visitation for 2k
hours, which provides little information about standing crop actually
available to foraging butterflies. Wiklund and Ahrberg (1978)
qualitatively described nectar use by Anthocaris butterflies, but did
not quantify nectar characteristics. Richman and Edwards (1976)
briefly described visitation patterns of four species of migrating
butterflies in Florida and showed differential flower selection by
these species, but again did not quantify nectar characteristics.

Flower selection and foraging energetics of bees have been
thoroughly studied. Heinrich ( 1979b) has done much work on the
foraging energetics of bumblebees and has attempted to estimate

58

foraging success in terms of energetic profit, but this probably has
little relevance to butterflies because of the major differences in
the biology of these two groups. Schmitt (1980) compared bee and
butterfly foraging at several species of Senecio and demonstrated
significant differences in foraging behavior. Butterflies (all
foraging species were lumped under the general category of
butterflies) tended to visit fewer flowering heads per plant than
bumblebees and to fly. greater distances between flowers than did bees.
She suggested that the butterflies were not foraging optimally in
terms of energy intake.

In this section I consider the behavior and energetics of
foraging by Agraulis vanillae and Phoebis sennae at the nectar sources
most frequently used by these two species at my study sites in order
to determine which floral characteristics are most closely related to
the energetic gain realized by butterflies foraging at these flowers.
By quantifying the nectar available (standing crop volume and sugar
concentration), and butterfly foraging behavior (flower visitation
rate and amount of time spent perching and in flight), I estimate
energy budgets of each species at the major nectar sources. These
estimates can then be used to search for ecologically relevant cues to
foraging success, including the nectar characteristics themselves
(concentration and volume) and floral characteristics. Corolla length
has been shown in bees to affect the floral resources available to a
given bee species (Inouye I98O; Ranta and Lundberg 1980 ) . By
preventing access of short-tongued nectarivores to the nectar,
long-corolla flowers may accumulate more nectar; corolla length may
therefore be a useful predictor of foraging profitability. Flower

59

density may also be a predictor of foraging success as flower species
that occur in higher densities result in a greater visitation rate
(increased energy intake) and reduced traveling distances (reduced
energy expenditure).

One goal of this chapter is to address the utility of
single-factor (concentration) models of foraging energetics as
compared to a multi-factor approach. In addition to seeking
correlations between floral and nectar characteristics and foraging
success, I compare foraging selectivity in these two butterfly
species. Both are commonly found in the same habitats, so foraging
decisions made in response to the same resource arrays can be
compared. Several questions can be addressed with this sort of
comparison. Do these species differ in their foraging behavior -at the
same resources? Do these differences result in different energetic
consequences to the species? What factors might lead to divergent
foraging tactics and energetics when the two species are feeding at a
common resource?

Methods and Materials
Nectar characteristics

I monitored nectar resource use by both Agraulis van i 11a e and
Phoebis sennae at several sites on Payne's Prairie State Preserve,
Alachua County, Florida, between April and October 1982. I defined
major nectar sources as all flower species at which feeding was
frequent enough and of sufficient duration to permit collection of
behavioral data (described below). I did observe visitation at other
nectar sources, but only sporadically. For major nectar sources,
available nectar volume and sucrose concentration were measured at

60

three to seven different times for each species. Corolla length and
flower density ( flowers /m ) were also measured once for each nectar
source at a typical patch of flowers. I measured nectar volume with
Drummond microcapillary tubes (l - 5 ul). Most previous studies of
nectar characteristics of butterfly visited flowers have not
quantified available nectar, but have allowed nectar to accumulate for
up to 2k hours (Watt et al. 1971*; Opler 1980), as available nectar
is often minuscule. Most workers measure nectar by insertion of the
capillary tube into the flower corolla; this is impossible in many
butterfly flowers because of the small corollas. I measured nectar
volumes by removing the flowers from the calyx, and squeezing the
corolla tube from the top to expel the nectar as a small droplet from
the bottom of the corolla. This droplet can then be picked up with a
microcap; this allows measurement of nectar volumes that are
undetectable by insertion of the microcap into the corolla. Nectar
concentrations were measured by use of an American Optical 10^31
temperature-compensated hand refractometer, which measures nectar
concentrations in per cent sucrose equivalents. Since both glucose
and fructose have refractive indices approximately half that of
sucrose, the concentration of nectars that are mixtures of these
sugars can be expressed as the equivalent amount of sucrose to give
similar refractive properties. A single concentration measurement
requires about 0.5 to 1 ul of nectar; since many of the flowers
measured contained volumes of a few thousandths of a microliter per
flower, this often required the pooling of nectar from as many as
25-100 flowers to obtain a single nectar concentration. Given sucrose
concentration and nectar volume, milligrams of sugar per flower can be

6l

calculated (Bolt en et al. 1979), and this quantity can be converted
to energy per flower, assuming l6.kQ joules per mg of sucrose
(Heinrich 1975). Inouye et al. (1980) have shown that various
non-sugar nectar constituents (such as lipids, amino acids, etc.) can
add to the refractive index of nectars, causing overestimation of
energy content. However, even at very high concentrations of several
of these constituents, Inouye and his colleagues found a maximum error
of 3.6% sucrose equivalents. Each of these constituents alone (at
high concentrations) caused errors ranging from 0.06 to 0.9*+% sucrose
equivalents. This magnitude of error is acceptable for the
approximate energetic estimates derived here.

Foraging behavior and energetics

Foraging behavior of the butterflies at each nectar source was
quantified by measuring the visitation rate (flowers visited/s), and
the proportion of foraging time spent in flight. This was done using
two stopwatches. On one stopwatch, the length of the foraging bout
under observation was timed, and on the other, the duration of flight
during the bout was recorded. From these data, I calculated the
proportion of foraging time spent in flight for each butterfly species
at each of the nectar sources. A tally was kept of the number of
flowers visited during the observation period to calculate foraging
rate. As the butterflies often moved out of sight fairly rapidly, the
length of most bouts I measured was about one minute. These data were
then used to estimate energy intake and expenditures of the foraging
butterflies. Energy intake was calculated as the mean visitation rate
multiplied by the mean energy available per flower or

E. = flowers/s x joules /flower. (3-1)

62

Energy expenditure was estimated as the proportion of time in flight

(Tfl) multiplied by the metabolic expense of flight (E ) plus the

proportion of time perched (T ) multiplied by the resting

metabolic rate (T ) or
per

Ecost = Tfl <V + V (3W- (3-2)
Heinrich (1975) suggests that in nectarivorous insects the metabolic
costs of walking and feeding are probably close to resting metabolic
rates. Metabolic rates were obtained from the literature. Zebe
(195*0 measured the metabolic rate of Vanessa io (Nymphalidae) at rest
and in flight. The resting metabolic rate was measured at 0.32
cc02/g/hr at 21.5 C. I have used this figure for both Agraulis and
Phoebis, whose average weights are 0.195 g and 0.231 g, respectively.
Thoracic and abdominal temperatures of foraging butterflies were
measured using a Bailey BAT-12 electronic telethermometer and needle
probe. Butterfly temperatures were measured within 10 seconds after
the insect was netted. As both species attain thoracic temperatures
averaging about 38°C in the field, metabolic costs must be scaled '
accordingly. Chaplin and Wells (1982) found a Q of 3.0 for
monarch metabolic rates. Using this figure, I calculated resting
metabolic rates at 38° C for Agraulis and Phoebis to be 1.53
cc02/g/hr. Since butterflies burn mainly fat as fuel (as indicated
by an RQ of 0.7) (Zebe 195*0, one cc of oxygen oxidizes 0.000**97g
of fat, which produces 19-75 joules of energy. Thus, the resting
energy expenditure of Agraulis is estimated at 0.00l6j/sec at 38°C,
and that of Phoebis is estimated at 0.0019 J/sec. Using a similar
procedure, and starting with Zebe's (195*0 measurements of the
metabolic cost of flight in Vanessa io, I estimated flight costs in

63

Agraulis as 0.0573 J/sec and in Phoebis as O.O679 J/sec. Because Zebe

measured flight metabolism of butterflies forced to

flap continuously in a metabolic chamber, he probably overestimated

the cost of flight compared to foraging butterflies which may glide or

use wind currents to reduce energetic expenditure. Thus, foraging

costs are probably overestimated, resulting in conservative estimates

of foraging profit. Foraging profitability for each nectar source was

calculated as energy intake (Equation 3-1 ) minus metabolic cost of

foraging (Equation 3-2) or

E +. = E. - E (3-3).
net in cost v J;

Measuring the energy content of each nectar source species
several times throughout the day gives several estimates of
foraging profitability for each nectar source species. Foraging rates
and percent flight time are assumed to be constant for each nectar
source species. Since only nectar volume changed between times of
day, and since the time required to extract the nectar is only a small
fraction of foraging time, changes in nectar volume should not affect
the butterflies' foraging rates or their amount of time spent in
flight.

Flower selectivity

I observed both species while they foraged at two patches of
flowers of different composition. The first floral array, observed
from 7 September to 12 September 1984, occupied approximately 100 m2,
and included two major nectar species (Hyptis mutabilis and Verbena
brasiliensis). The second floral array was observed between ik
September and 26 September 1984, was of approximately 150 m2 and
included four major nectar species (Hyptis, Verbena, Bidens pilosa,

6k

and Ipomoea trichocarpa) . Foraging bouts of individual butterflies
were quantified by recording the sequence of flowers (or flower heads
for Bidens) visited while in the patch.
Temporal changes in behavior

To determine if diurnal partitioning of foraging and other
behaviors occurred, I conducted censuses of all Agraulis vanillae seen
along a 220 m transect (described below) at half -hour intervals
throughout the morning and early afternoon on eleven days between 10
August and 31 August 1984. The length of the transect was traversed
in approximately five minutes, and each butterfly sighted was recorded
as exhibiting one of the following behaviors: l) nectaring, 2)
■basking or perched, 3) in reproductive flight, or k) in rapid
searching flight. Reproductive flight included several distinct
behaviors. Females spend a large proportion of their activity time in
a slow, turning flight through the vegetation in search of oviposition
sites. Males engage in a similar flight, apparently in search of
females. Occasional courtship flights (following, wing fluttering)
were also observed and included in this category. The last category
included flight behavior quite different from reproductive flight.
This flight is more rapid, direct, and usually about lm above the
vegetation. I observed mostly males exhibiting this type of flight.

Movement patterns

The vagility of a species can determine what resources it is
exposed to, which could influence flower selectivity. Because the two
species studied here were markedly different in this regard, I
quantified the extent of movement by individuals within a population.
This was possible only for Agraulis vanillae, due to low population

65

densities and difficulty of capturing sufficient numbers of Phoebis
sennae. A mark-recapture study of Agraulis vanillae was carried out
between 9 August and lk September 198k at a population about 500 m
south of the Alachua sink on the north edge of Payne's Prairie. This
butterfly population was centered on a population of Passiflora
incarnata growing along a network of dikes through the marsh. A 220 m
transect was set up along the main dike road, and numbered flags were
placed at 10 m intervals along this transect. The entire length of
the transect contained both larval host plants (Passiflora) and nectar
plants. At one- to three-day intervals, all butterflies captured
along this transect were marked using the 1-2-1+-7 wing marking method
(Ehrlich and Davidson i960). Before release, the location of capture,
behavior prior to capture, sex and wing wear condition of each
butterfly were recorded. Wing wear was subjectively assigned to one
of the following categories: l) fresh - no visible wear, 2) young —
< 25% scale loss (visually estimated), little or no fraying of wing
margins, 3) 25-50% scale loss, light to moderate fraying of wing
margins, and k) >50% scale loss, heavy fraying of margins. Behaviors
were categorized as l) nectaring, 2) basking or perching, 3)
oviposition, mate search or courtship flight, and k) rapid searching
flight. The location, date, time and behavior of any marked butterfly
observed or recaptured were recorded.

Results
Phoebis , with a proboscis of nearly 3 cm, can feed at a greater
range of floral resources than does Agraulis , resulting in a greater
range of flowers to select from and consequently greater energetic
rewards during foraging. Table 3-1 presents the proboscis lengths of

66

TABLE 3-1 — MEM PROBOSCIS LENGTH OF AGRAULIS AND PHOEBIS AND FLORAL
CHARACTERISTICS OF NECTAR SOURCES. [mi^TT-Standi^Tli7iation (n)].
Comparisons between species were by Mann-Whitney U test.

Agraulis vanillae Phoebis sennae U d

Proboscis '

length(cm) 19. 2 ± 1.8l (16) 29-5 + 2.20 (9) 0 <.0001

Corolla

length (cm) 6.27 + 4.13 (7) lit. 09 + 9-93 (7) 11. 5 0.10

Nectar

volume (ul) 0.107 ± 0.192 (36) 0.486 ± 0.889(31) 314 <.005

Nectar

concentration

(% sucrose) 24.01 + 9.81 (21) 25-90 + 9-21 (25) 199.5 0.46

Energy/flower

(joules) 0.400 + 0.701 (36) 2.884 + 5-062(31) 316.5 <.002

67

the butterflies and floral characteristics of the major nectar sources
of the two butterfly species. The differences in foraging selectivity-
are considered in more detail below. On a gross level, however,
resource use by Phoebis results in an average energy reward per
visited flower over seven times as great as that of Agraulis . This is
due primarily to differences in the mean nectar volume of the flowers
visited by the two species. Nectar concentrations of the flowers
visited do not differ between the two species. Although the corolla
lengths of the two butterflies ' nectar sources do not differ
statistically (Table 3-1), the difference is biologically significant.
Four of the nectar sources visited by Phoebis have corolla lengths
over 2 cm long. The nectar in these flowers is inaccessible to
Agraulis. As shown below, there is a highly significant correlation
between corolla length and energy per flower.

I observed both species foraging at seven or eight major nectar
sources. Table 3-2 presents the phenologies of the nectar sources
studied. These observations are qualitative only; no attempt was
made to collect phenological data. Not all of these species were
available at the same site. Cnidoscolus stimulosus was available for
only 2-3 weeks at a upland site south of the prairie and was the only
nectar source for this Agraulis population for the period during which
Cnidoscolus bloomed. Vernonia gigantea bloomed at a site in the NW
section of Payne's Prairie and was essentially the only nectar source
used by Agraulis and Phoebis foraging in this area. Richardia scabra
is a common plant of roadsides and waste areas and I studied it at a
fallow agricultural field west of Lake Alice on the University of
Florida campus. Interestingly, this low-reward flower was only

68

TABLE 3-2 — NECTAE SOURCES AND FLOWERING PHENOLOGY

Species Blooming period Peak visitation Foragers

Cnidoscolus
stimulosus

Verbena
brasiliensis

Sida
rhombifolia

Bidens
pilosa

Hyptis
mutabilis

Vernonia
gigantea

Richardia
scabra

Agalinis
purpurea

Ipomoea
trichocarpa

1^
coccinea

quamoclit

May - September
April - September
May - September
June -October

mid-June - October

August - September

June-October

October

August - October

August - October

August - October

late May -June

May - September

July-August

August - October

August

October

Agraulis

Agraulis

Both

September-October Agraulis

Both

Both

September-October Agraulis

Phoebis

September-October Phoebis

September-October Phoebis

September-October Phoebis

69

visited by Agraulis where it occurred in large stands away from other
nectar sources. Small patches blooming simultaneously with preferred
nectar sources at the Alachua sink population were generally ignored.
The three Ipomoea species are also common roadside species and I
observed them both on Payne's Prairie and in the Gainesville area.
Agalinis purpurea was studied in an open field south of Payne ' s
Prairie near Lake Wauberg. I observed all of the other nectar source
species on the north side of Payne's Prairie near the Alachua sink,
where all are available simultaneously for a period of several weeks
from late summer to early fall. Notice that the peak numbers of
nectar sources are available in late summer and fall; this
corresponds to the peak of butterfly abundance for both species.
Flower density seems to peak at this time as well.

The available nectar volumes of the flowers visited by these
species span a wide range of variation, and consequently the energetic
reward per flower varies widely as well. The flowers selected by
Phoebis, however, tend to have greater nectar volumes and therefore
energy contents. Table 3-3 presents the nectar availability data
broken down by flower species. The nectar availability of each
species was measured several times throughout the morning and mid-day
when foraging behavior was at a maximum. These measurements were
analyzed to give a mean reward averaged throughout the foraging
period. The sample sizes referred to in Table 3-3 thus refer to the
number of discrete samples taken (i.e., times of day) and the total
number of flowers measured (or number of concentration readings
taken). As nectar concentration measurements required more nectar
than was sometimes available, not all nectar volume measurements

70

TABLE 3-3 — NECTAR AVAILABILITY AND ENERGY CONTENT OF MAJOR NECTAR
SOURCES OF AGRAULIS AND PHOEBIS. [mean ± 1 standard deviation, (n;n).
First number indicates number of times sampled, second number
indicates total number of flowers sampled].

Species X volume X concentration X energy /flower
(ul) (% sucrose) (joules)

Richardia

scabra 0. 0076+. 0125(5 ;98) 18.7 + 9.8(3;9) 0.015 + .018 (5)

Verbena

brasiliensis 0.0079+-00l+l(7;l88) 38.1+ + 5.8(l;6) O.O58 + .030 (7)

Bidens

pilosa 0.01l8+.00l+8(3;68) i+0.4 + l.9(l;8) 0.093 ± .038 (3)

Agalinis

purpurea 0. 0U15+. 021+3 (U; 67) 17.1 + l.l(3;23) 0.123 + .071 (1+)

Vernonia

gigantea 0.0387+.0337(6;110) 29.5 + lU.5(3;l8) O.17I+ + .185 (6)

Hyptis

mutabilis 0.0832+.0l+99(6;96) 18. 7 + 8.5(5;l8) 0.21+8 + .079 (6)

Sida

rhombifolia 0.132+.039 (U;55) 25.6 + 6.6(3;13) 0.568 + .238 (1+)

Ipomoea

trichocarpa 0. 220+0. 159(3;l+5 ) 3k. 9 + 1.1+(3;10) 1.1+88 ± l.lUU (3)

Cnidoscolus

stimulosus 0.1+9l++.293(5;8l) 19. 8 + 1.6(U;37) 1-770 ± 1.126 (5)

Ipomoea

coccinea 1.562+0.235(3;^) 31.1 + 1.7(3;2l) 9.102 + 1.751 (3)

Ipomoea

quamoclit 1. 853+1. l+90(5;70 ) 28.1+ + 0.5(3;25) 9-270 + 7-85 (5)

71

were accompanied by a concentration reading at the same time of day.
In these cases, energy/flower was calculated using the concentration
that was taken closest in time to the volume measurement. For two of
the extremely low volume flowers, Verbena brasiliensis and Bidens
pilosa, accumulation of enough nectar for a concentration measurement
required bagging the flowers and preventing visitation for several
hours; thus nectar concentration could not be measured before
mid-day, and the concentration obtained at that time was used in
conjunction with all volume measurements taken earlier. The result is
probably an overestimation of the energy content of these flowers, as
the nectar on which I took the concentration measurement was probably
more concentrated due to evaporation than the actual available nectar
on which the volume measurements were taken (Corbet 1978; Corbet et
al« 1979). A common trend in most nectar sources begins with
maximum availability in the morning, usually soon after the flowers
open or begin secreting nectar. Nectar availability then declines
throughout the morning. By noon, the visitation rate by butterflies
and a host of other nectarivorous insects is so great that nectar
availability at most flowers is kept at a minuscule amount. After
about 1300 hours nectar volumes approached zero for most species.
Most nectar sources showed very high variances in volume of available
nectar. Variation in nectar concentration was most pronounced in open
flowers with short corollas (see Table 3-4) and apparently is due to
evaporation and concentration of the nectar as the morning progressed.
There seems to be less of a tendency for evaporation in flowers with
long corollas, such as the Ipomoea spp. and Agalinis purpurea. It
became apparent early in the study that Phoebis did not visit

72

TABLE 3-h — DENSITY AND
standard deviation (n)].

COROLLA LENGTHS OF NECTAR SOURCES [mean + 1

Species

Richardia

Verbena

Bidens

Agalinis

Vernonia

Hyptis

Sida

Ipomoea trichocarpa

Cnidoscolus

Ipomoea quamoclit

Corolla length (mm)

7.03 ± 0.62 (15)

3.59 ± 0.28 (21)

*+.56 + 0.72 (12)

21.91 + 2.16 (16)

10.30 + O.76 (15)

6.09 + 0.33 (16)

0(no corolla)

20.80 + 1.87 (10)

12.30 + 1.27 (28)

2U.93 ± 0.76 (15)

Density (flrs/m )

199.2

+

117.7 (15)

1272.0

+

936.0 (10)

1312.3

+

U59.O (20)

66.8

+

31.8 (20)

511+.1

+

1+01.7 (10)

527.9

+

226.2 (12)

124.0

+

58.3 (10)

UT-T

±

17.0 (2U)

72.1

+

33-9 (18)

60.1+

+

28.6 (15)

73

low-reward species such as Richardia, Verbena and Bidens. Occasional
visits by Phoebis to these flowers were seen, but they were apparently
for sampling aS no prolonged foraging was seen at these
species. Conversely, Agraulis does not feed at the Ipomoea species or
at Agalinis , due to morphological exclusion. These flowers are
energetically quite rewarding but have corolla tubes so long as to
prevent Agraulis from reaching the nectar (see Tables 3-1 and 3-M«
When all nectar sources are considered, the range in energy contents
of flowers is quite remarkable, and spans several orders of magnitude.
The largest part of this variation is due to differences in nectar
volume, which ranges between 0.0076 and 1.85 ul/flower. Nectar
concentration shows much less variation, ranging between 17.1 and
k0.k% sucrose.

Both species visit flowers that occur at a wide range of
densities. In addition, the morphology of visited flowers is variable
and includes dish-shaped flowers with no corolla tube (Sida) ,
composites (Bidens, Vernonia) , and flowers with long tubular corollas
(ipomoea spp. , Agalinis). Table 3-*+ presents the floral densities and
corolla lengths for each of the nectar sources. The effect of corolla
length on nectar rewards has already been mentioned. Low reward
flowers such as Bidens and Verbena generally occur in higher densities
than the other species, somewhat offsetting the energetic consequences
of their low nectar volumes.

The two butterfly species differ significantly in their patterns
of exploitation of these floral resources. These differences are most
apparent at nectar sources used by both species. Table 3-5 gives
percent of time in flight while foraging and foraging rates for both

74

TABLE 3-5 — FLIGHT TIME AND FORAGING RATE OF AGRAULIS AND PHOEBIS.
[mean + 1 standard deviation (n)].

Nectar species

Vernonia

Verbena

Sida

Cnidoscolus

Hyptis

Bidens

Richardia

Agalinis

I_. trichocarpa

I.quamoclit

% of time in flight Foraging rate (flrs/s)
Agraulis Phoebis Agraulis Phoebis

26.8±18.0(21) 19.5+11.0(17) 0. 541+0. 137(l8) 0.475±0. 176(10)

20.8+8.4 (65)

35.8+8.8 (25) 23.^+10.6(19)

21.0+7.1 (18)

30.9+10.5(20) 18.1+7.6(22)

15.3+7.1 (20)

22.7+7.5 (17)

26.3±9.2 (23)

34.9110.4(24)

27.6+6.7 (20)

0.493+0.134(65)

0.191+0.057(29) 0.155+0.049(22)

0.339±0.076(24)

0.318+0.109(20) 0.321+0.061(22)

0.680+0.137(20)

0.618+0.109(17)

0.184±0.036(23)

O.156+O. 029 (24)

0.162+0.052(26)

75

species at each of the nectar sources. These data were not collected
for Ipomoea coccinea. Because its floral morphology and density are
quite similar to those of I.quamoclit, density, percent flight, and
foraging rate used in calculating the foraging profit for I. coccinea
were those measured for I.quamoclit. Phoebis generally spends less
time in flight than does Agraulis. The differences in percent flight
are significant for two of the three shared nectar sources (Sida: U =
378; p<.0002; Hyptis: U = 369-5; p <.0002; Vernonia: U = 217, p
= .26). Phoebis also forages at a slower rate than does Agraulis , but
these differences are only significant at one of the three shared
nectar sources (Sida: U = 1+1+9, p < .05). This is not due to the time
required to extract the nectar since Phoebis has a higher uptake rate
than Agraulis (Chapter II). It may reflect a cost of having a longer
proboscis, which may not be as efficient at probing short corolla
flowers as a short proboscis. This may increase handling time, as has
been shown for some bumblebees by Inouye (1980). For both species,
less time is spent in flight at the nectar sources with higher
densities. Foraging rate is also greatest at these densely packed
flowers.

Because of the selection of high-reward flowers by Phoebis and
because of this species' more efficient foraging behavior, it
generally realizes greater foraging profits does Agraulis. Table 3-6
shows the estimated foraging profits at each of the nectar sources.
Some caution need be applied in interpreting these estimates. First,
the metabolic costs on which they were based are rough estimates at
best. Metabolic costs of flight as measured in butterfies in a
metabolic chamber may differ significantly from the the costs of

76

TABLE 3-6 — FORAGING PROFITABILITY OF AGRAULIS AND PHOEBIS AT
DIFFERENT NECTAR SOURCES. [mean + 1 standard deviation (n)l.

Nectar source Agraulis Profit Phoebis Profit
(joules /s) (joules/s)

-0.005 + 0.011(5)

0.016 + 0.015(7)

Bidens 0.053 ± 0.026(3)

Agalinis 0.006 + 0.011+ (1+)

Vernonia 0.069 + 0.086(6) 0.053 + 0.069(6)

0.060 + 0.025(6) 0.066 + 0.025(6)

0.087 ± 0.01+5(1+) 0.071 ± 0.037(1O

0.207 ± 0.178(3)

0.587 ± 0.382(5)

I.coccinea 1.1+55+0.287(3)

I.q.uamoclit 1.675 ± 1.183(5)

77

flight in unhampered butterflies in the wild. Second, the energy-
benefits are based on mean nectar rewards available and not on rewards
of individual flowers. Thus meaningful patterns of variation among
individual flowers will be obscured. Nonetheless, these estimates
should be useful for comparative purposes, because the magnitude of
error in estimation should be similar among nectar sources. According
to these estimates, Agraulis may occasionally forage at or near an
energy deficit (Richardia) , but Phoebis never does. There is a wide
range of foraging profitability at different nectar sources.
Particularly note the difference between Sida and Verbena; Agraulis
is commonly observed going from one species to the other during a
foraging bout , even though there is nearly a ten-fold difference in
energy reward. Two of the Ipomoea species (coccinea and quamocl it )
are by far the most rewarding of the flowers visited by either
species, and are available to Phoebis for about six weeks during the
fall migratory period (Walker 1978).

Using the nectar availability data, the behavioral data, floral
characteristics, and energetic profit estimates, I asked the question:
Which cues available to the butterflies are most likely to be related
to energetic profitability of foraging? Table 3-7 is a correlation
matrix of several of the variables presented above. Notice first that
energetic reward per flower is most strongly correlated with nectar
volume, and both variables are highly significantly correlated with
foraging profits of both species. Concentration, on the other hand,
shows no meaningful correlation with any of the other variables.
Flower density is correlated strongly only with foraging rate, and
then much more so in Phoebis than in Agraulis. Combined with the fact

78

TABLE 3-7 — CORRELATION MATRIX OF FORAGING ENERGETICS DATA

* indicates correlation significant at .05 level
** indicates correlation significant at .01 level

Volume Cone Density Corolla Energy/flower

Energy/flower 0.9949** 0.1052 -O.3698* 0.6216**

Phoebis rate -0.4343* O.O989 0.9504** -0.5279** -0.1+407*

Agraulis rate -0.4305* 0.3156 0.5214** 0.1945 -0.4271*

Phoebis flight 0.3743 -0.0726 -0.9155** 0.6948** 0.3879

Agraulis flight -0.0376 -0.4107* -0.4955* -O.3065 -0.0340

Phoebis profit 0.9972** 0.2057 -0.3768 0.5756** -0.9942**

Agraulis profit 0.9745** -0.1771 -O.3836 0.5080* 0.9844**

79

that Agraulis generally flies more while foraging, this may indicate
that Agraulis is less efficient in its between flower movements than
Phoebis. This interpretation is supported by the negative
correlations between density and the amount of time spent in flight,
which again are more strongly correlated in Phoebis than in Agraulis.
Corolla length is correlated well with energy reward and foraging
profitability, again more strongly in Phoebis. A longer corolla
flower is generally a more rewarding flower, presumably due to its
inaccessibility to most foragers, which allows accumulation of greater
nectar rewards. Corolla length is negatively correlated with foraging
rate in Phoebis but not in Agraulis. This is due to the long-corolla
Ipomoea spp. , which have high nectar volumes and occur in low
densities. This causes the butterflies to spend more time at
individual flowers and more time flying between flowers, and thus
produces low foraging rates. The lack of a similar correlation in
Agraulis is probably because Agraulis visits no long corolla flowers
with nectar volumes comparable to those of Ipomoea. The correlation
between percent flight time and corolla length in Phoebis is also due
mainly to the influence of the Ipomoea spp., which are borne singly
and in low density, thus requiring more between extensive flower
flights.

As mentioned above, nectar concentration is not clearly
correlated with any aspect of foraging success. The Kingsolver and
Daniel (1979) model, however, (as modified in Chapter II) predicts a
maximum energy intake rate at nectars of 35-1+0% sucrose concentration.
As the maximum nectar concentration in the flowers visited by these
two butterflies is just over k0%, we should see a correlation

80

between nectar concentration and foraging profit or energy intake if
nectar concentration is of overriding importance in determining energy
intake rate. As seen in Table 3-7 however, none of the correlations
between concentration and energy/flower or foraging profit of either
species is significant. The variation in other determinants of
foraging profit, particularly nectar volume, are more closely related
to differences in foraging profit.

The foraging selectivity of the two butterflies at mixed floral
arrays differs significantly. In a mixed floral array containing
mainly Hyptis and Verbena, Phoebis restricts its visits to the more
rewarding species (Hyptis ) to a greater degree than does Agraulis
(Table 3-8). The two flower species are quite similar in color, size
and general appearance, yet Phoebis is still able to discriminate
between them. The small number of visits by Phoebis to Verbena
flowers may be attributed to either sampling or misidentification by
the butterflies, as generally only 1 or 2 flowers of Verbena were
visited before the insects returned to Hyptis. Within a foraging
bout, Agraulis frequently switches flowers, whereas Phoebis does so
much less often. The average foraging bout of Agraulis is about twice
as long as that of Phoebis in this floral array. Table 3-9 presents
similar data for a mixed patch of Bidens, Ipomoea trichocarpa, Hyptis
and Verbena. This patch was observed about one week after the
Hyptis-Verbena patch was observed. During this time span, Ipomoea
trichocarpa had begun to bloom, and Phoebis completely ceased visiting
any other flowers. Notice that Agraulis concentrated its visits on
Bidens , the most common flower in the patch. The number of Bidens

81

TABLE 3-8 — FORAGING SELECTIVITY AT MIXED FLORAL ARRAY 1 (SEE TEXT),
[mean + 1 standard deviation (number of bouts observed)]. Comparisons
between species were with Mann-Whitney U test.

Agraulis (38) Phoebis (15) U p

# Hyptis visited 8.9 ±_8.3 8.5 + 8.1 293.5 0.87

# Verbena visited 13.6 +11.5 1.7 + 2.2 I+78 <.0005
Switches/bout 2.5 ± 2.6 0.7 + 1.2 1+12 <.010
% Hyptis visited kk.S + 3^.2 77.2 + 35.3 135.5 <.005
Total flowers/bout 22.7 ± 13-9 10.3 + 8.0 41+7.5 <.005

82

TABLE 3-9 — FORAGING SELECTIVITY AT FLORAL ARRAY 2 (SEE TEXT). [mean
+ 1 standard deviation (number of bouts observed) ] .Comparisons between
species were with Mann-Whitney U test.

# Bidens visited

# Ipomoea visited

# Hyptis visited

# Verbena visited
Switches /bout

% visits to Bidens
% visits to Ipomoea
Total flowers visited

Agraulis (37)

7.6 + 6.9

0.0

k.l + 8.7

0.6 + 1.9

O.k ± 0.9

70.8 + kk.3

0.0
12. k ± 8.1

Phoebis (36)

0.0
15.2 ± 10.7

0.0

0.0

0.0

0.0
100.0 + 0.0
15.2 ± 10.7

u

1170 <0.0001

0 <0.0001

864 <0.0005

756 0.023

792 0.006

1170 <0.0001

0.0 <0.0001

581.5 0.351

83

visited per bout refers to the number of flower heads visited; as
each head may contain 10-1+0 individual flowers, the actual number of
flowers visited per bout is much greater. Thus, even though there was
no significant difference in the total number of flowers visited per
bout, this is probably misleading as it does not take individual
Bidens florets into account. As before, Agraulis switches between
flower species within a foraging bout more often than Phoebis, which
was completely constant in its flower preference.

Agraulis maintains a body temperature that is 5-7°C above
ambient temperature (Figure 3-1 ). This is accomplished primarily by
dorsal basking (Clench 1966), both while foraging and when perched.
Because the body temperature rises, metabolic expenditure increases
through the morning as ambient temperature increases. In addition,
nectar availability and energy content per flower generally decrease
throughout the day, particularly in the afternoon. If Agraulis is
selected to maximize energy intake while foraging, we might expect
foraging activity to be restricted to the morning when energetic costs
are lowest and nectar rewards are high. Figure 3-2 shows that this is
not the case. Although the proportion of individual butterflies
observed that are nectaring does decrease from a maximum after 1100 to
1200 hr, a significant amount of nectaring occurs throughout the
mid-afternoon. As shown in Table 3-10, the individuals foraging in
the afternoon are generally older individuals. (These data were
compiled from first capture records of the mark-recapture study.
Young individuals were defined as those belonging to age classes 1 and
2, and age classes 3 and k were considered older.) Figure 3-2 also
shows that there is no distinct partitioning of behaviors to different

81*

43 -i

• THORACIC TEMPERATURE
o ABDOMINAL TEMPERATURE

AMBIENT TEMPERATURE °C

Figure 3-1 — Thoracic and abdominal temperatures of Agraulis vanillae
as a function of ambient temperature (T ). See p. 62 for details
of measurements. Regression equation for abdominal temperature
(T b): T = 0.857 T& + 8.1+58 (r = 0.907). Regression
equation for thoracic temperature (T. ): T,, = 1.018 T +
5.988 (r = 0.890). t th

85

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DE3QI

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86

TABLE 3-10 — AGE OF NECTARING INDIVIDUALS VS. TIME OF DAY. Data
analyzed using 2x2 contingency X .

Time of day

0900 -1100 1100 - li+00

Young 61 37

Old 22 27

x2 = 3.999
p = O.Oi+55

87

times of day. Courtship, mate search and oviposition search occur
throughout the morning concurrently with nectaring. None of these
activities occurs until the thoracic temperatures of the butterflies
reaches approximately 30 C however. Thus, basking is the only
behavior observed until about 0900, and the amount of basking behavior
then declines throughout the morning. Agraulis divides its time
during the morning between nectaring and reproductive behaviors, and
it is not unusual to see a female momentarily cease oviposition search
to nectar or a male quit nectaring to chase a female. Butterfly
activity reaches a peak between about 1100 and 1200 hr, after which
time the number of butterflies seen per unit time decreases throughout
the afternoon. The frequency of rapid searching flight increases in
the afternoon, although the function of this behavior is unknown. It
is seen mainly in males. Females apparently retire to the vegetation
in the afternoon as relatively few are seen after 1300.

Agraulis vanillae is a fairly sedentary butterfly, and
individuals appear to have quite restricted home ranges. Table 3-11
presents average movement distances between capture and recapture of
Agraulis , separated by age and sex. There are no significant
differences among these categories. These data represent 62
individuals that were recaptured or resighted out of a total of 2U7
marked (25.1%). Notice that the average amount of movement between
captures averaged between 18 and 5^+ m. These represent inter-capture
periods of up to 16 days. Thus this species is apparently quite
sedentary, and individuals seem to remain within a restricted area for
extended periods. This has two implications to foraging behavior.
First, the variety of nectar resources to which they are exposed and

TABLE 3-11 — AVERAGE DISTANCE MOVED (m) BETWEEN CAPTURES FOR AGRAULIS
[mean + 1 standard deviation (n)].

Distance moved (m)
Age Males Females

1 25.6 +. 2i+.9 (32) 5^.0 + 37. 8 (5)

2 31*-1* ± 55.5 (18) 29.7 + 21.9 (3*0

3 29.3 ± 31.3 (MO 35-8 ± 1+3.6 (12)
k 18. 5 ± 16.9 (39) 25.0 ± 17.3 (U)

89

can select among may be quite small relative to a more mobile species.
In addition, travel costs must be quite low as very little prolonged
flight is required. Total energetic costs may therefore be low
relative to a more mobile species.

Discussion
ASraulis vanillae and Phoebis sennae differ significantly in
their selection of nectar source plants, both on a seasonal basis and
when foraging at the same resource arrays. The effect of these
differences is to provide Phoebis with a greater rate of energy intake
when considering foraging within a single array of flowers and a
greater mean energy reward per flower visited overall. This
difference is due primarily to differences in the nectar volumes of
flowers visited by the two species and not to sugar concentration
differences between the nectars. Nectar volumes, and thus energy
contents, of flowers visited by Phoebis are greater than those
encountered by Agraulis for two reasons. First, Phoebis avoids low
nectar volume flowers such as Bidens pilosa, Richardia scabra and
Verbena brasiliensis, which are avidly visited by Agraulis. Second,
Phoebis visits several flower species (ipomoea spp. ) with extremely
large nectar volumes (relative to other butterfly-visited flowers)
that are inaccessible to most other butterflies due to their long
corolla tubes. These flowers accumulate greater nectar rewards
because insect visitation is restricted to those insects with
sufficiently long mouthparts to reach the nectar (Faegri and van der
Pijl 1979). There may also be differences in nectar secretion rates,
but these were not measured here.

90

Phoebis sennae selects flowers with greater mean energy rewards,
and it is also more energy efficient in its foraging behavior at the
three flower species that are visited by both butterflies. Phoebis
spends less time in flight at these nectar sources, thus reducing
energetic expenditures. Between flower flights are more direct than
those of Agraulis. However, the foraging rate is either the same
(Hyptis, Vernonia) or slower (Sida) at these shared resources. This
may result from increased handling time per flower because of the
longer proboscis. However, Inouye (i960) found that, in bumblebees,
long-tongued species generally had shorter handling times than
short-tongued species at the same flowers. Decreased flight
costs (increases foraging profit) and slower foraging

rates (decreases foraging profit) offset each other such that the rate
of energy intake while foraging at these nectar sources does not
differ greatly between the two species.

The rewards offered by the nectar sources of both these species
vary greatly, both within a species of flower and among flower
species. Nectar volumes range from thousandths of a microliter (many
flowers are in fact empty) to several microliters per flower. Nectar
concentration shows less variation, although it is still significant.
The effect of both of these factors is to produce a remarkable amount
of variability in energy availability per flower. The major component
of variance in energy content, however, is variation in nectar volume.

If either of these species is selected to maximize the rate of
energy intake while foraging, either to maximize the energy available
to the animal or to minimize the amount of time spent foraging, as
suggested by optimal foraging models (Schoener 1971; Pyke et al.

91

1977), what cues might be used by these species as predictors of
foraging profit? Kingsolver and Daniel (1979) and Heyneman (1983)
have predicted that certain nectar concentrations should maximize the
rate of energy intake while the butterfly is imbibing nectar. These
models as modified in Chapter II predict that nectars of 35-^0% sugar
concentration will provide the maximal rate of energy intake and
should be preferred by the insects. However, these models consider
only the rate of energy intake while the insect is actually imbibing
nectar. In fact, a very small proportion of total foraging time of
butterflies is spent actually extracting the nectar; most of their
time is spent flying between flowers and finding the nectar within a
given flower. Even in flowers with only thousandths of a microliter
of nectar, which requires a small fraction of a second to extract,
visit duration at a single flower can be several seconds. The amount
of time spent in flight between flowers depends on the floral density
and the handling time of a flower is dependent on flower morphology.
When these factors are taken into account, the importance of the
nectar concentration in determining energy intake is insignificant, as
indicated by the lack of correlation between nectar concentration and
foraging profit estimates. Therefore I suggest that the single-factor
approach to modeling foraging energetics used by Kingsolver and Daniel
(1979,1983) and Heyneman (1983) is of little value for these insects.
Much meaningful variation in the profitability of foraging caused by a
variety of factors other than nectar concentration is ignored by this
approach. Viewed in this light, I would not expect these insects to
base foraging decisions on nectar concentration.

92

The density of flowers may affect foraging profit in several
ways. High density floral arrays reduce inter-flower flight distances
and thus decrease foraging costs. This effect is more evident in
Phoebis , again apparently due to their more direct flight "between
flowers. High density flowers are thus associated with lower foraging
costs (lower foraging costs) as well as greater visitation rates, both
of which will increase the profitability of foraging. However, high
floral density is also correlated with relatively small nectar
rewards, thus decreasing profitability. Again the different factors
offset each other, so that there is no consistent relationship between
floral density and foraging profit. Therefore I would not expect
foraging decisions to be made on the basis of density either.

Length of the corolla tube is positively correlated with foraging
profit. This is because flowers with long corollas restrict access to
nectarivores and thus tend to accumulate larger amounts of nectar. On
the other hand, for the flowers visited by Phoebis , increasing corolla
length is associated with decreased foraging rates, most likely due to
increased handling times (the long corolla takes longer to probe) as
well as increased extraction times (high nectar volumes increases time
spent actually removing nectar ) . Overall , however , corolla length is
positively correlated with foraging profitability for both butterfly
species.

The best predictor of foraging profitability is simply nectar
volume. This variable explains over 99% of the variance in the energy
available per flower and is highly correlated with foraging profit in
both species. Therefore, if these butterflies forage so as to
maximize energy intake, they should select the nectar sources with the

93

greatest nectar volumes, irrespective of concentration, density or
corolla length. This would maximize their water intake while they
nectar as well, which Watt et al. (197*0 have suggested may be
important to some butterflies. The usefulness of nectar volume as a
cue influencing foraging decisions may be hampered by the large amount
of variance in this quantity, both within and among species. A
critical factor in a forager's decision making process is the size of
its "memory window" (sensu Cowie 1977) used in evaluating the rewards
offered by a given resource. If only a few flowers are sampled and
used as a basis for foraging decisions, the result is a high variance
in the estimates of nectar availability for a given nectar source
among sampling estimates. It is not at all uncommon to encounter
several empty flowers or several rewarding flowers in a row for
several of the nectar sources used by these species. Patchiness in
the dispersion of nectar resources may be common in other types of
flowers as well (Zimmerman 198l). The result of using only a few
flowers for estimating nectar availability might thus result in
frequent switching among nectar sources, as is seen in Agraulis
vanillae. Using a greater number of flowers to estimate nectar
availability would improve the accuracy of the estimate, but would
also entail greater costs of sampling, as it would take the insect
longer to decide not to forage at an unrewarding species. Such a
sampling pattern may be more feasible in butterflies than in other
nectarivores, however, as butterflies possess significant lipid
reserves that would carry them through periods of energy-deficit
foraging while sampling.

9h

Do either of the species considered here select nectar resources
on the hasis of volume? It seems likely that they do. Agraulis does
not visit some available nectar sources, such as Heterotheca
subaxillaris, that have exceedingly minute nectar volumes.
Furthermore, it only visits Richardia scabra when this flower is
growing by itself. This low-reward flower is avoided when in the
presence of flowers with higher nectar volumes such as Verbena
brasiliensis and Hyptis mutabilis. As previously discussed, Phoebis
sennae exhibits even greater selectivity, again seemingly due to
differences in nectar volume. It completely avoids several low-volume
flower species such as Richardia, Bidens pilosa, and Verbena. It is
also more constant than Agraulis when visiting a mixture or flowers
differing in nectar rewards. When foraging at a mixed patch of Hyptis
and Verbena, Phoebis for the most part avoids the less-rewarding
Verbena flowers, even though they are quite similar to Hyptis in
shape, color and size. This discrimination, not seen in Agraulis, may
be based on differences in inflorescence type between the two nectar
species (spike vs. panicle).

Both butterfly species exhibit some evidence of selectivity,
which seems to be based on nectar volumes and thus energy contents.
Why then do they differ in the degree of their selectivity? One major
difference is that foraging by Agraulis occurs mainly in the vicinity
of the larval food plant Passiflora incarnata. Phoebis however is
apparently much more mobile between patches of its Cassia food plants.
Murphy (1983 ) has shown a relationship between Euphydryas oviposition
sites and proximity of nectar sources. In Phoebis and Agraulis , the
differences in vagility may be related to the persistence of their

95

food plants. Passiflora is a long-lived perennial that is available
at any one site throughout the butterflies' flight season. The Cassia
species fed on by Phoebis are annuals that senesce in some areas
before the flight season ends, perhaps favoring greater inter-patch
mobility. Thus Agraulis populations appear to be quite sedentary,
comparable to other nymphalid butterflies such as Euphydryas editha
(Ehrlich et al. 1975; Gilbert and Singer 1973). Phoebis sennae, on
the other hand , seems to be more mobile, like some other pierids such
as various Colias spp. (Tabashnik 198O; Watt et al. 1977) and may
exhibit the "egg-spreading" syndrome described by Root and Kareiva
(1984) for Pieris rapae, where the females are highly mobile and lay
eggs on widely spaced host plants, possibly to minimize risks of
individual plant-related larval mortality. The effects of these
divergent mobility patterns to the foraging strategies of Phoebis and
Agraulis are potentially manifold. First, the less mobile species is
exposed to a lower diversity of resources and therefore has less
opportunity to exercise selectivity. Second, as inter-patch flight is
less common, energetic expenditures may be lower in the more sedentary
species, reducing the selective pressure for energy maximization in
foraging. Third, since the more mobile Phoebis are often not in the
presence of larval host plants, there may be temporal separation of
nectaring and reproductive behaviors. Minimizing the amount of time
spent foraging might thus increase reproductive success by freeing
more time for mate search, courtship, oviposition site search, etc.

In Agraulis , there is no distinct temporal separation of
nectaring and reproductive behaviors. Both types of behavior are
alternated throughout the activity period, as larval food plants and

96

nectar sources are interspersed. Mate search by males may be nearly
as effective during nectaring as when they are searching in a more
active manner. There may thus be little selection pressure to
minimize foraging time. In addition, Agraulis must bask to maintain
high body temperatures required for activity. Thermoregulation in
flight is not known to occur in any butterfly species (Heinrich 198l),
so Agraulis may have to perch frequently to thermoregulate. Nectaring
may thus serve multiple functions, including feeding and basking.
Feeding is not restricted to the morning hours when it is most
profitable (because of lower body temperatures and greater nectar
rewards). However, butterflies foraging in the afternoon are more
likely to be older individuals that may be more energy stressed due to
depleted fat stores.

These species differ in the way they allocate time to foraging
versus reproductive behaviors and this may also explain the observed
differences in selectivity. Lucas (1983) considered the effect on
foraging selectivity of limiting the amount of time available for
foraging by an animal. He argues that the "cost" of being
non-selective in prey choice is the probability that a forager will
miss the opportunity to capture a high-quality food item while the
animal is handling or consuming a low-quality item. As the amount of
time available for foraging decreases, the probability of encountering
a high-quality food item decreases, so the forager should become less
selective. Stated in another way, animals with short foraging bouts
should be more generalized in their food selection than animals with
long foraging bouts. I have presented evidence here suggesting that
Agraulis forages in very short bouts, alternating these foraging bouts

97

with reproductive activities or intraspecific interactions. Phoebis ,
on the other hand, often forages farther from larval food plants and
appears to segregate their foraging and reproductive activities into
longer, mutually exclusive periods. Lucas' (1983) model would
therefore predict that Phoebis should be more selective than Agraulis ,
even when foraging in the same flower patches. This is exactly what I
observed.

To conclude, then, several diverse factors may interact to affect
foraging decisions and selectivity in these two butterfly species.
The overall effect of all of these factors produces different patterns
of selectivity between these two nectarivores. Morphology of the
feeding apparatus influences selectivity by determining which
resources are available to a given species. The life history-
characteristics of a species, such as vagility, food-plant
distributions and temporal properties, and allocation of time to
various activities, may also influence foraging decisions by affecting
the types of resources encountered and the energetic expenditures of
the animal. Another factor that may have important consequences to
foraging behavior, to be considered in the next section, is the amount
of stored energy available to the butterfly and differences in this
quantity among species.

Summary

I estimated energy budgets of foraging Agraulis vanillae and
Phoebis sennae at their major nectar sources using time-budget data
combined with metabolic data from the literature, energetic rewards
offered by the various nectar sources , and the rate at which the
butterflies exploit these flowers. Using estimated foraging profits,

98

I sought proximate cues that might be used by energy-maximizing
butterflies as a basis for flower selection. Recent theoretical
models, as revised in Chapter II, suggested that butterflies should
selectively feed on flowers producing nectars with sugar
concentrations between 35 and k0%. My data suggest no relationship
between nectar concentration and foraging profit. Similarly, floral
density is not correlated with foraging profit either. Corolla length
and nectar volume are positively correlated with energetic reward and
foraging profitability and should be used by the butterflies as a
basis for flower selection. Differences in nectar volume alone
account for more than 95% of the variance in foraging profitability,
and might be used as the sole basis on which flowers are accepted or
rejected for inclusion in the diet.

Agraulis and Phoebis showed significant differences in flower
selectivity. Phoebis is consistently more selective than Agraulis
with regard to energy content of flowers. This results in greater
rates of energy intake while Phoebis is foraging than those
experienced by Agraulis. This is partly due to morphological
differences ; Phoebis has a longer proboscis and can feed at highly
rewarding flowers with long corollas from which Agraulis is excluded.
But Phoebis also avoids several low-reward flower species visited by
Agraulis . Agraulis individuals often fail to discriminate between
low- and high-reward flowers and frequently switch between them within
a foraging bout. These differences in selectivity are probably linked
to differences between the butterflies in population structure and
time-allocation patterns. Agraulis is a more sedentary species and
does not forage far from its larval food plant. Energetic costs of

99

travel are therefore reduced, and foraging bouts tend to be short
since they are frequently interrupted by intraspecific interactions or
reproductive behaviors (courtship, chasing behaviors, oviposition
search, etc.)* Phoebis individuals appear to spend longer periods of
time devoted solely to foraging or reproductive behaviors. Recent
models have predicted that a species that forages in short bouts
should be more generalized in food selection than a species which
forages in long bouts, as observed here.

CHAPTER IV

LIPID STORAGE AND DEPLETION IN AGRAULIS VANILLAE AND

PHOEBIS SENNAE : EFFECTS OF ADULT FORAGING

Introduction

The feeding ecology of holometabolous insects may be quite
complex, since feeding may occur during both larval and adult stages;
the types of food taken during the different stages may be quite
dissimilar. Nevertheless, Boggs (1981) has stressed the
interdependence of larval and adult feeding and the importance of each
to realizing the maximal potential reproductive fitness. She argues
that the total expected reproductive output is determined by energy
and nutrients acquired through both larval and adult feeding as well
as and the proportion of adult energy or nutrient intake allocated to
reproduction. Therefore, other factors being equal, a reduction in
adult nutrient or energy intake should be accompanied by an increase
in the proportion of larval nutrients or energy stores earmarked for
reproduction. Boggs1 argument was focused at the species level; thus
two species that differ in expected adult nutrient intake should show
corresponding differences in the allocation of larval nutrients at
metamorphosis .

Boggs tested and validated this hypothesis using three species of

heliconiine butterflies (Boggs 1981) that differ in the amount of

adult feeding. Boggs' predictions and tests were focused on nitrogen

budgets and the allocation of nitrogen at metamorphosis to

100

101

reproductive reserves. Nitrogen is acquired by feeding adults through
pollen feeding, and the extent of pollen feeding varied among the
three species , with one species (Dry as Julia) not feeding on pollen at
all. In accord with the predictions, she found that the proportion of
total body nitrogen allocated to reproduction varied inversely with
the extent of pollen feeding as an adult. Further, she found that the
rate at which these reproductive nitrogen stores declined depended on
both the rate of adult nutrient intake as well as the rate of
reproductive output of these nutrients.

Boggs remarked that few other data were available concerning the
inter-relationship between larval and adult feeding, but that the
model should be applicable to other nutrients and dietary components
as well. Heliconius butterflies are apparently unique among the
Rhopalocera in their demand for nitrogen in the adult diet, as no
other butterflies are known to feed on pollen (Gilbert 1972).
However, many butterflies feed on floral nectar as adults, and energy
intake acquired through this feeding is known to increase fecundity
and survival in many lepidopteran species (Stern and Smith I96O;
Murphy et al. 1983). In addition, energy reserves are provided for
adults through larval storage of lipids, which serve as a major fuel
source for adult activities (Stokes and Morgan I981). We might
therefore extend Boggs' (1981) hypothesis and predict that the amount
of larval resources allocated at metamorphosis to lipid reserves will
vary inversely with the expected adult energy intake, and further,
that the rate of change in these lipid reserves will depend on the
amount of adult feeding as well as the amount of energy expended on
other activities.

102

Although lepidopterans were thought to use only lipid as an adult
energy source (Zebe 195*+; Brown and Chippendale 197*0, this may only
be true in those species that do not feed as adults (Stokes and Morgan
198l). Most lepidopterans apparently can use carbohydrates as a fuel
source for initial stages of flight activity, but then switch to lipid
oxidation for prolonged flight activity (van Handel and Nayar 1972;
Stokes and Morgan 1981). However, lipids are the primary means of
storing energy (Brown and Chippendale 197^; Cenedella 1971; Domroese
and Gilbert 1964). The amount of stored lipid is known to vary
markedly during different phases of adult life. Chaplin and Wells
(1982) found that overwintering monarch butterflies ( Danaus plexippus )
deplete their fat stores over the course of the winter. Walford
(1980) and Brower (in press) present data suggesting that migrating
monarchs begin building large lipid reserves by extensive nectaring as
they reach the southern U.S. The extent of these lipid reserves may
determine both the probability of surviving the winter as well as the
distance to which they can re-migrate in the spring (Tuskes and Brower
1978).

Adequate lipid reserves of adult butterflies thus appear to be
necessary for achieving maximum survival and therefore fitness and are
mediated by both larval storage and adult feeding. In Chapter III, I
presented data showing that Phoebis sennae forages more profitably in
terms of rate of energy intake than does Agraulis vanillae. Assuming
that these two species spend similar proportions of adult activity
time feeding, Phoebis sennae should have a greater expected adult
energy intake than does Agraulis. In fact, unquantified observations
suggest that Phoebis may spend a greater proportion of activity time

103

feeding, as I have observed them feeding during mid- to
late-afternoon, when most Agraulis are inactive. In this
chapter, I consider data testing the prediction' that expected adult
energy intake is inversely related to the amount of lipid stored
during metamorphosis from resources acquired through larval feeding.
In addition, I examine changes in lipid stores and body composition
over the adult life span to determine whether differences in adult
energy intake correspond to differing patterns of storage or depletion
of lipid reserves. Does Phoebis sennae, which has a greater energy
intake as an adult, store more lipid through adult foraging or deplete
its emergence lipid stores at a slower rate than does Agraulis?
Methods and Materials

I collected late instar larvae, pupae and adults of Agraulis
vanillae and Phoebis sennae at various sites on Payne's Prairie State
Preserve, Micanopy, Fla. I brought larvae back to the laboratory and
reared them to adults. Adults collected in the field were
individually placed in glassine envelopes and frozen within four hours
of capture. Care was taken during capture to handle the adults by the
forewings only, so as not to augment scale loss from the hindwings.
Field-collected adults were assigned relative ages by counting the
number of scales missing along 1 cm transects in each of five cells of
the ventral hindwing (Rs,M ,M ,M_ and Cu). Each transect was made
parallel to the anterior vein bordering the cell. Scale loss has been
shown to be a reasonable estimator of adult age in other butterfly
species (Ehrlich and Gilbert 1973; Watt et aL 1977).

I reared larvae of both species to pupae in the laboratory, where
temperature was approximately 2k C and photoperiod was uncontrolled.

ioi+

Freshly emerged adults were frozen within 12 hours of emergence, after
they expelled their meconial wastes.

I measured forewing lengths of the butterflies prior to lipid
analysis. Each individual was analyzed for lipid content, after
drying to constant weight in a drying oven, using the petroleum ether
extraction technique of Walford (I980) and Brower (in press).
This technique extracts only neutral lipids and is more suitable
for assaying energy reserves than other lipid extractions, as
membrane-bound phospholipids are not available as an energy source. I
calculated percent lipid for each individual by dividing lipid weight
by initial dry weight and multiplying by 100.

I compared body composition characteristics (dry weight, lipid
weight, lean weight, percent lipid) of freshly-emerged and
field-collected butterflies using analyses of variance programs in the
BMDP statistical software package (Dixon et al. 198l)- In addition,
dry weight, lipid weight, lean weight, and percent lipid of field
collected individuals were compared after grouping them into age
classes based on the relative amount of scale loss. All analyses of
variance were two-way ANOVAs permitting determination of age-related
as well as sexual differences in body composition.

Results

Agraulis vanillae shows significant sexual differences in all
body composition characteristics, with females being larger and
containing more lipids than males (Table 1+-1). Females emerge from
the pupae weighing approximately O.llTg (dry weight), whereas males
emerge at only 0.08g. Of this dry weight, females contain 0.019g of
lipids while males contain only O.Ollg, or 15.9 and 12.8% of dry

105

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106

weight, respectively. Dry weight, lean weight, lipid weight and
percent lipid of field-collected individuals are all signif i :antly
lower than in freshly-emerged butterflies. This suggests tr it lipids
as well as non-lipid body components are being metabolized c iring
adult life.

As predicted, Phoebis sennae adults emerge from the pup e with
less stored lipid than do adults of Agraulis (Table k-2) . F x>ebis
shows no significant differences between the sexes for body
composition characteristics. Forewing length in Phoebis is greater in
males. The F and p values presented in both tables k-1 and —2 refer
to the two-way ANOVAs using sex and age class as the groupir. ;
variables. Although in some comparisons, Levene's test for squal
variances indicated significant differences in variance amor, samples ,
the significance of all differences was confirmed by Brown-F rsythe
and Welch analyses of variance, which do not assume equal va iances
among groups (Dixon et al. 198l). Phoebis sennae adults emerge from
the pupae with only about h% of their dry weight allocated t lipids,
compared with 13-l6% in Agraulis vanillae. However, the pro ortion of
dry weight contributed by lipids increases in the field-coll cted
samples, indicating that this species accumulates lipid rese ves as an
adult through nectar feeding.

One possible complicating factor in comparisons of
field-collected and lab-reared butterflies is the conditions under
which the larvae were reared. Angelo and Slansky (1982) hav shown
that for several moth species, larvae reared under adverse c nditions
may produce smaller adults with lower lipid stores. If the .aboratory
conditions under which the larvae were reared in this study are less

107

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108

suitable than those experienced by the wild larvae, greater lipid
contents of field-collected butterflies might be due to this factor
rather than lipid storage from adult feeding. Forewing lengths,
which are a general indicator of body size, were not measured in the
lab-reared Agraulis van i 11a e, so it is impossible to test for
differences in overall body size between lab-reared and
field-collected samples. However, for this species, such differences
would cause underestimation of lipid contents at emergence. Since
lab-reared individuals were shown to have greater lipid contents than
the field-collected individuals, such biases would lessen the
difference between lipid contents at emergence and later in the adult
life.

In Phoebis sennae forewings of lab-reared individuals
were significantly smaller than those of the field-collected
individuals (Table k-2) . However, the critical comparison between
these two groups with regard to Boggs ' (1981) hypothesis is the
proportion of the soma allocated to lipids, so the percent lipid
comparison should not be affected unless percent lipid is correlated
with body size. There is no significant correlation between percent
lipid and forewing length among the freshy emerged butterflies (n =
18, r = 0.1156, p > 0.05), even though these individuals varied in
forewing length between 26 and 37 mm. The highest percent lipid seen
in any freshly emerged individual was only 1%. It thus appears that
Phoebis responds to poor larval conditions by producing a smaller
adult; however, the proportion of body tissue invested as lipid
stores apparently is not affected, as predicted by Boggs (1981). The
significant differences in body size between lab-reared and

109

field-collected samples make comparisons of dry weight, lean weight,
and absolute lipid weight impossible to interpret in terms of the
effects of adult energy intake on these characteristics.

In order to examine changes in body composition over the adult
life span, individuals were assigned to one of six age classes based
on scale loss. Freshly emerged butterflies were assigned to age class
A, and the field collected butterflies were assigned to the following
five categories: B - 80-99% of scales remaining; C - 60-79% of
scales remaining; D - h0-59% of scales remaining; E - 20-39% of
scales remaining; F - 0-19% of scales remaining.

Agraulis vanillae males and females generally decrease in dry
weight throughout adult life (Figure k-l). It is not
known if the relationship between age and scale loss is a linear one,
so whether the x-axis can be directly interpreted as age is unclear.
Males are smaller than females in all age classes. Age class C
females show an increase in dry weight, but this is probably an
artifact of small sample size (n = 6). Two of the individuals in this
sample were unusually large, and if these two data were removed the
graph would show a consistent decline in dry weight throughout life as
in the males. As seen in Figure k-2, the decrease in dry weight is
due in part to a decrease in lean weight, which seems to occur mainly
in later age classes. Again the apparent increase in lean weight of
class C females is attributable to the two abnormally large females in
this sample. Figure k-3 demonstrates that the proportion of body
composed of lipids declines rapidly early in life, and then levels off
in older individuals at about 5%.

110

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AGE CLASS

Figure k-l - Dry weight (g) of Agraulis vanillae vs. age class. Age
class determination is based on degree of scale loss (see text for
details). Circles indicate means, bars show one standard error on
either side of the mean, and sample sizes are in parentheses.

Ill

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Figure k-2 - Lean weight (g) of Agraulis vanillae vs. age class. Age
class determination based on degree of scale loss (see text for
details). Circles indicate means, bars show one standard error on
either side of the mean, and sample sizes are in parentheses.

112

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Figure l*-3 - Per cent lipid (of dry weight) of Agraulis vanillae vs.
age class. Age class determination based on degree of scale loss (see
text for details). Circles indicate means, bars show one standard
error on either side of the mean, and sample sizes are in parentheses.

113

In contrast, Phoebis sennae adults increase their dry weight
dramatically, mainly by accumulating lipids acquired through adult
feeding. Figure k-h shows the relationship between dry weight and age
class of Phoebis sennae adults. As mentioned above, analyses of
variance indicated no significant differences in weight
characteristics between sexes, so data from males and females were
pooled. Because of the smaller size of laboratory-reared individuals,
the weight of class A individuals is suspect. However, all other
classes were composed of field-collected butterflies that did not
differ in body size among age classes. These data show that Phoebis
increases dramatically in weight during most of the adult life, and
then apparently declines. Figure k-5 shows that this increase in dry
weight may be due to slight increases in lean weight, but as seen in
Figure k-6 it is mainly due to storage of lipids acquired through
adult foraging. The proportion of dry weight contributed by lipid
increases through most of adult life. Up to 0.07 g of lipid
was found in some field-collected individuals, or kf% of dry weight.
This represents a 10-fold increase in the proportion of dry weight
contributed by lipids over the freshly-eclosed butterflies.

Discussion

Boggs (1981) states that little evidence is available from other
studies to support her model of larval-adult feeding interdependence.
The data presented here suggest that her hypothesis may have broad
applicability to many aspects of insect nutrition. Although the
original model pertained strictly to nutrients allocated to
reproductive reserves at metamorphosis, in this study it was
impossible to determine how much of the lipid reserves set aside at

Ill*

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5 -12

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flC .08
O

.04 -

(2)

(14)

(IS)

(7)

(3)

(10)

AGE CLASS

Figure k-k - Dry weight (g) of Phoebis sennae vs. age class. Age
class determination based on degree of scale loss (see text for
details). Circles indicate means, bars show one standard error on
either side of the mean, and sample sizes are in parentheses.

115

14 -i

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m

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<

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(2)

(13)

(14)

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AGE CLASS

Figure k-5 - Lean weight (g) of Phoebis sennae vs. age class. Age
class determination based on degree of scale loss (see text for
details). Circles indicate means, bars show one standard error on
either side of the mean, and sample sizes are in parentheses.

116

(2)

40 -i

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AGE CLASS

Figure k-6 - Per cent lipid (of dry weight) of Phoebis sennae vs. age
class. Age class determination based on degree of scale loss (see
text for details). Circles indicate means, bars show one standard
error one either side of the mean, and sample sizes are in
parentheses.

117

metamorphosis are used directly for reproduction, i.e., egg or
spermatophore production. These reserves are used to fuel all adult
activities, most or "which are at least indirectly related to
reproduction, such as mate searching, courtship, oviposition site
searching, etc.

The adaptive advantage of using lipids as a fuel reserve,
especially for flying insects, has been known for some time. Lipids
contain more energy/mass than other fuel sources such as carbohydrates
(9 cal/mg compared to Ucal/mg), and can be stored in anhydrous form
rather than in a hydrated state as are carbohydrates (Kleiber I96I;
Bailey 1975). However, lipids are not as rapidly
mobilized as carbohydrates are, and therefore most lepidopterans
apparently use carbohydrates first and then fall back on lipid
reserves once carbohydrates are depleted (Stokes and Morgan 1981).
The main energy-yielding components of stored lipids are
apparently triglyceride fatty acids such as oleic and palmitic
acids (Cenedella 1971; Brown and Chippendale 197*+ )•

In her original model, Boggs (1981) was able to assume that
larval nutrition and survivorship were invariant among species by
comparing three closely related species with similar life histories
and food plants. The data here suggest that her model may apply
in general to all butterflies, since the two species here are from
different families (Nymphalidae and Pieridae) and have completely
unrelated larval food plants (Passiflora spp: Passifloraceae and
Cassia spp.: Fabaceae). If the assumption of similar life histories
and larval nutrition can be relaxed, this model may be a powerful tool
for understanding inter-relations between feeding during larval and

118

adult stages. For example, it may be possible to predict the
importance and extent of adult feeding in a variety of lepidopteran
species simply by examining lipid storage at metamorphosis.

Other factors, however, may confound this simple relationship
between lipid storage at metamorphosis and adult foraging. The
longevity of the adult may significantly affect the requirement for
stored lipids. In the two species considered here, Agraulis may live
up to 21 days as an adult ; the longevity of Phoebis is unknown but is
presumed to be greater, as overwintering adults are in reproductive
diapause and must live several months if they are to survive and
reproduce the next spring. In addition, patterns of reproductive
expenditure vary significantly among lepidopterans. Species that lay
eggs in several large masses, such as Euphydryas editha (Murphy et al.
1983), may require greater lipid stores since forming a batch of eggs
produces more of an immediate energetic drain than laying eggs singly.
Both species studied here lay eggs singly, although the rate of egg
production, total lifetime fecundity, and differences in these
quantities between the two species are unknown. Another factor that
may affect the magnitude of lipid storage is the vagility of the
species. In the two species studied here, there are significant
differences in mobility. Agraulis vanillae is a sedentary species ;
mark-recapture studies indicate that home ranges are restricted to the
vicinity of Passiflora food plants. Phoebis sennae engages in
extensive inter-patch movements between its Cassia food plants, which
may necessitate greater lipid reserves. In this species, these
reserves are acquired mainly through adult foraging. In migratory
monarch butterflies ( Danaus plexippus ) , lipids may constitute up to

119

b5% of dry weight (Brown and Chippendale 197*0 • This species also
acquires these lipid reserves mainly through adult foraging and not by
larval feeding (Walford 19o0; Brower in press). The pattern of fat
storage and depletion by Agraulis vanillae more closely resembles that
seen in Hyalophora cecropia (Saturniidae) (Domroese and Gilbert 1964)
or Magicicada cassini (Homoptera) (Brown and Chippendale 1973). In
these species, fat reserves laid down at metamorphosis are not
augmented by adult feeding, but progressively decline through the
adult life span.

Lipid reserves in butterflies may serve as a buffer against
environmental variability in species that encounter highly variable
conditions as adults. For Agraulis vanillae, the Passiflora food
plants required for reproduction may occur in a variety of plant
communities. These vary greatly in the amount and quality of nectar
sources co-occurring with the larval food plants. Large lipid
reserves in newly emerging adults may allow them to take advantage of
these nectar-poor food plant patches, or allow emigration to more
suitable areas. In Phoebis sennae, adults are able to exploit more
energetically rewarding nectar sources due to their longer proboscis,
and thus adults can store sufficient lipid reserves to allow great
mobility among larval food plant patches that vary in quality. in
addition, this species apparently can tolerate variability in food
plant quality by producing smaller adults when larvae are faced with
suboptimal food plant material or feeding conditions.

Summary

Agraulis vanillae and Phoebis sennae differ significantly in fat
storage patterns, as predicted by theory. Boggs (1981) hypothesized

120

that two species differing in expected adult intake of a nutrient
should show corresponding differences in the allocation of that
nutrient at metamorphosis. Phoebis sennae, which has a higher adult
energy intake, emerges from the pupa with 3—5% of dry weight allocated
to lipid. Agraulis vanillae, which is relatively non-selective in
adult foraging and obtains less energy through adult feeding, emerges
from the pupa with 16-20% of dry weight allocated to lipid. Whereas
the lipid reserves of Agraulis vanillae decrease regularly to about 57°
of dry weight, Phoebis sennae accumulates lipids and builds reserves
up to k0% of dry weight.

CHAPTER V

THE EFFECTS OF ADULT ENERGY INTAKE ON

SURVIVAL AND FECUNDITY OF AGRAULIS VANILLAE

Introduction

Optimal foraging models assume that maximizing the rate of

intake of some dietary component, such as energy, will maximize

the fitness of the individual, and therefore natural selection

will favor those individuals that forage so as to maximize the

rate of intake of that component over a given time period

(Schoener 1971; Pyke et al. 1977; Mitchell 198l). However,

this assumption is rarely supported empirically (Mitchell 1981).

Real (1980a) suggests that in some animals where energy is the

quantity maximized, the fitness benefits derived from increasing

energy intake may not be linear, but concave downwards. In

other words, there may be diminishing fitness returns at

increasing levels of energy intake. With regard to

nectarivores, which obtain mainly energy from nectar (Heinrich

1975)» maximizing energy intake in energy-stressed individuals

may confer large fitness benefits, whereas non-stressed

individuals may realize smaller increments in fitness from

behaviors maximizing energy intake. Thus selection pressures

favoring behaviors maximizing energy intake may be strong for

energy-stressed individuals, but weak for individuals under no

energy stress.

121

122

The effects of the energy-yielding components of nectar
(mono- and disaccharide sugars) on fitness components such as
fecundity and longevity of lepidopterans are quite variable.
Some species require no adult feeding at all (Carefoot 1973);
in others, individuals on water diets realize fecundities equal
to those of sugar-fed individuals (Fenemore 1979; Raina and
Bell 1978). However, in most species that feed as adults,
sugars in the diet result in increased fecundity or survival
(Labeyrie 1957; Raina and Bell 1978; Stern and Smith i960;
El-Sherif et al. 1979; Murphy et al. 1983). Yet maximizing
energy intake apparently does not necessarily maximize
fecundity. El-Sherif et aL (1979) found that the moth
Pthorimaea operculella (Gelechiidae) achieved maximum longevity
and fecundity when fed 5% sucrose solutions; increasing the
sucrose concentration, which presumably increased energy intake,
reduced survival and fecundity below that of the 5% diet. These
studies all dealt with laboratory strains of pest moth species;
their relevance to wild populations is uncertain. In addition,
in many lepidopterans the reproductive output achieved by adults
may be significantly affected by the feeding success and food
plant quality experienced by the larvae (Slansky 1982; Beckwith
1970).

Observations of foraging Agraulis vanillae have suggested
that selection for energy maximization during adult feeding may
be weak. I have presented evidence that this species is
relatively non-selective when foraging at mixed floral arrays
and fails to discriminate among flower species varying widely in

123

energy return. Furthermore, this species emerges from the pupa
with relatively large lipid reserves that are depleted
throughout adult life. Freshly-emerged individuals apparently
spend less time foraging than do older adults, as older
individuals tend to forage later in the day when nectar
resources are less rewarding. Thus there may be age-related
differences in foraging strategies of individuals related to the
current energy balance and the benefits to be realized from
further energy intake.

In this section, I describe experiments designed to measure
the effects of adult feeding and larval reserves on fitness in
Agraulis vanillae. Specifically, I wish to test the assumption
that increasing energy intake increases fitness. Further, I
would like to determine the form of the energy-fitness function,
i.e., linear or concave. Fitness will be quantified in several
ways, including survivorship, fecundity, and lipid storage.
Fitness is a complex function determined by fecundity and
survivorship as well as interactions between these variables.
No attempt is made here to integrate the various traits into a
single model of fitness. Rather, my intent is merely to show
that certain life-history traits that affect fitness are
sensitive to energy intake by the adult insect. Fecundity is
quantified here as the number of fully-formed (chorionated) eggs
found in the ovarioles of females and is assumed to be a
relative measure of reproductive output. The effects of energy
content of the adult diet on lipid storage and survival in males
are also considered.

124

Methods and Materials
Effect of energy intake on fecundity and lipid storage
I collected late-instar larvae of Agraulis vanillae in the
field and reared them to pupation in the laboratory.
Freshly-emerged adults were individually numbered, marked and
released in flight cages. These cages measured 2.5 x 2.5 x 3.1
m and were located in the shade of a large live oak so that they
received no more than one hour of direct sunlight per day. I
randomly assigned each butterfly to one of the following four
diet treatments: a) fed once a day to satiation with a 0.25%
sucrose solution (the butterflies would not imbibe pure water),
hereafter referred to as the water treatment; b) 10% sucrose
solution (weight /weight) , restricted to a maximum feeding bout
of three minutes per day; c) 10% sucrose solution, fed once a
day to satiation; d) 50% sucrose solution, fed once a day to
satiation. Butterflies in the satiation treatments were assumed
to be satiated when they had removed their proboscides from the
feeding vessel three times. For a randomly selected sample of
individuals in each treatment, I timed the feeding duration of
each day's feeding bout with a stopwatch. The cumulative
feeding time was used to estimate energy intake during adult
life by multiplying cumulative feeding time by energy intake
rate (joules/s) for the sucrose concentration on which the
individual was fed (see Chapter II for explanation of energy
intake rate determinations). Cages were checked daily for
mortality, and at ages of 1 to 9 days randomly chosen
individuals were sacrificed for fecundity or lipid measurements.

125

Females were preserved in 70% ethanol and later dissected to
determine the number of chorionated eggs formed in the
ovarioles. Males were frozen and later subjected to a petroleum
ether lipid extraction to determine the magnitude of lipid
reserves (see Chapter IV for details of the extraction
procedure).

Effect of body weight on survival

Body weight is highly correlated with lipid content in both
Phoebis sennae and Agraulis vanillae (Phoebis: n = 59 ; wet
weight-lipid weight r = 0.8462, dry weight-lipid weight r =
0.9442; Agraulis : n = 91; wet weight-lipid weight r = O.696,
dry weight-lipid weight r = 0.706; all p < 0.01). To determine
if body weight (and therefore lipid weight) was significantly
related to survivability, freshly-emerged and field-collected
adults of Agraulis vanillae and Phoebis sennae were individually
numbered, weighed and placed in the flight cages described
above. They were not fed, but were provided with water via an
enamel pan of moist sand, in which pinned butterflies of both
species were placed to stimulate puddling (Arms et al. 1974).
Both species were observed to visit the pan to puddle. The
cages were checked daily for butterfly mortality.

Effect of eclosion weight on fecundity

To determine if larval feeding success (as measured by
weight of the adult butterfly at eclosion) influenced adult
fecundity, I collected late-instar larvae of Agraulis vanillae
in the field and reared them to pupation in the laboratory. I
weighed freshly-emerged females were weighed within 3 hours of

126

eclosion. Eclosion weight is assumed to reflect in some sense
the feeding success during the larval stage (as well as genetic
influences ) . Females were maintained for three days in the
laboratory at room temperature by keeping each female in a
glassine envelope within a 10 x 1^ x 20 cm plastic box
maintained at high humidity. Each female was fed for a maximum
of three minutes daily with a 30% sucrose solution after warming
to flight temperature with a heat lamp. At the end of the
three-day period, each female was weighed and preserved in 70%
ethanol. At a later date I dissected each female and counted
the number of chorionated eggs formed in the ovarioles.

Results
Feeding bout duration varied widely among individual
Agraulis vanillae used in the diet experiments. Individuals
offered 10% sucrose solutions would feed for durations as short
as 55 seconds per day or as great as 1200 seconds per day. With
50% sucrose solutions similar variation was seen, with bouts
ranging between 5 seconds and 900 seconds per day.
Consequently, there was a wide range of energy contents of diets
received by different individuals, even within treatment groups.
Individuals in the water treatment (0.25% sucrose) showed a
fairly consistent pattern of feeding behavior. Bout duration
for the first 1 to 3 days of adult life was quite short (l to 5
seconds), but later in life lengthened to as long as 325
seconds. As mean uptake rate at this concentration is about
0.7ul/s, this corresponds to a daily water intake ranging

127

between 1 and 225ul. Energy content of diets within this range
was negligible (average of 9«*+ joules over entire adult life).

There is a significant effect of adult energy intake on
chorionated egg production (Table 5-1 )• Because sacrificed
females differed in age (although not significantly among
treatments), and because this might affect the number of eggs
formed, data from this experiment were analyzed using a one-way
analysis of covariance (Dixon et al. 198l) with age as an
independent covariate of the dependent variable egg number.
Even after statistically removing any possible effects of age on
egg production, there was still a highly significant effect of
diet on egg production. However, inspection of the group means
in Table 5-1 suggests that the relationship between energy
intake and fecundity (as measured by chorionated egg production)
is not linear. Females in the 10% satiation treatment received
on the average about twice as much energy as females in the 10%
restricted group, and egg production was almost exactly doubled.
The 50% satiation group received more than twice as much energy
as the 10% satiation group, yet fecundity was increased only
slightly.

Figure 5-1 shows the relationship between total adult
energy intake and egg production for all females for which
feeding durations were measured. Two features of this plot
deserve comment. Although there is a significant correlation
between energy intake and egg count (r = 0.3952, n = 30 ), egg

128

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ADULT ENERGY INTAKE (joules)

Figure 5-1 - Total energy intake (Joules) during adult life
versus chorionated egg production. Line is fit by least squares
regression. (n = 30, r = 0.395, p < 0.05, y = 0.105x + 30.68.)

130

production appears to level off at energy intakes above 1200
joules. Second, there is wide variation in egg production of
females receiving very little or no energy in the adult diet (<
150 joules). In fact, some females receiving virtually no
energy in the adult diet produced as many eggs as females
receiving the highest amounts of energy. This suggests that
much of the realized fecundity of some females may be due to
stored resources carried over from the larval period and that
variation in fecundity among these low-energy females may
reflect variation in larval feeding success. To test this, I
sought correlations between eclosion weight of females and the
number of chorionated eggs produced after 3 days on a
standardized diet. As seen in Figure 5-2, eclosion weight is
strongly related to the number of eggs produced (r = 0.557, n =
26, p < 0.01). Egg production was also significantly correlated
with forewing length (r = O.506, n = 26, p < 0.01), final weight
after 3 days (r = 0.72^, n = 26, p < 0.01), and weight gain over
the three day period (r = 0.596, n = 26, p < 0.01). Some of
these butterflies gained weight over the course of the
experiment, in contrast to field-collected individuals and
individuals in the flight-cage experiments previously described.
In this experiment however, females were maintained in a
relatively cool laboratory (about 2k C) within glassine
envelopes , so that metabolic expenditures were minimal and
weight gain was possible.

Energy intake of adult males also significantly affects
body composition and lipid storage. Table 5-2 presents the data

131

I05n

.150

.200

.250

.300

.350 .400

INITIAL WEIGHT (g)

Figure 5-2 - The relationship between emergence weight Agraulis
vanillae females and the number of chorionated eggs produced
after 3 days on a nectar diet (see text for details). Line fit
by least squares regression. (n = 26, r = 0.557, p , 0.01, y =
287. 2x - 22.0.)

132

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133

from lipid analyses of male Agraulis vanillae on different adult
diets. Feeding durations of males in the 10% satiation
treatment were not measured; I was therefore unable to
determine adult energy intake and they were consequently omitted
from the analyses. Statistical comparisons of wet weight, dry
weight, lipid weight, lean weight and percent lipid (of dry
weight) were performed using one-way analysis of covariance with
age and forewing length as covariates (Dixon et al 1981).
Increasing adult energy intake decreased the rate at which body
weight was lost. However, the lipid contents of the 10%
restricted males did not. differ from those of water-fed males.
At low energy intake levels, stored lipid is apparently depleted
at the same rate; increasing the energy intake to levels within
the range received by individuals within the 50% group decreases
the rate at which stored lipid is depleted. There is no
evidence that any individuals stored lipids above the level seen
at eclosion from the pupa (about 15% of dry weight). One factor
not controlled in this experiment was activity level; all
butterflies were maintained in the same flight cages , so amounts
of flight activity may have varied among treatment groups
depending on energy content of the diets. This might obscure
any real differences in rate of lipid depletion between the 10%
restricted and water treatments.

Some mortality occurred among all treatment groups during
the course of the diet experiments. To determine if mortality
was influenced by treatment, I analyzed the mortality data using
a clinical life-table approach, which allows comparisons among

131*

treatments when survivorship of all individuals is not known
(those individuals withdrawn for egg counts or lipid
extractions). Data from males and females were pooled for this
analysis. Table 5-3 presents the observed and expected numbers

of deaths in each treatment group. Expected number of deaths

2
were calculated using the log-rank method. A X test showed

2
mortality to be significantly affected by treatment group (X =

9.U; df = 3; p < 0.025). Number of deaths observed was close

to expected in the 10% restricted and 10% satiation groups, but

was much greater than expected in the water treatment and less

than expected in the 50% sucrose treatment. I therefore

conclude that energy content of the adult diet significantly

affected the probability of mortality.

Body weight and survival

The data presented above show that increasing the adult
energy intake of males decreases the rate at which they deplete
body weight and stored lipids. A better fed butterfly is thus a
fatter butterfly. To determine whether differences in body
weight were related to mortality, I compared survival of
freshly-eclosed and field-collected individuals of both Phoebis
sennae and Agraulis vanillae that were maintained in a flight
cage with water but no access to food. Table 5-k presents the
data from that experiment. Freshly-eclosed Agraulis were about
0.05 g heavier than field-collected individuals and survived an
average of 2.5 days longer. Although field-collected Phoebis
were heavier than freshly-eclosed individuals, survival time of
both groups was equal. Variance in survival time of

135

TABLE 5-3 - NUMBER OF OBSERVED AND EXPECTED DEATHS OF AGRAULIS
VANILLAE VS. DIET TREATMENT. Expected deaths calculated using
log-rank method.

TREATMENT DEATHS

OBSERVED

WATER

13

10% RESTRICTED

5

10% SATIATION

k

50% SATIATION

2

EXPECTED

6.8
6.0
k.l
7.1

X2 = 9.U, DF = 3, p < 0.01

136

TABLE 5-1+ - SURVIVAL IN DAYS OF AGRAULIS VANILLAE AND PHOEBIS
SENNAE WITHOUT NECTAR VS. INITIAL WEIGHT"! [mean + 1 standard
deviation (n)]. Butterflies had access to water.

WET WEIGHT (G)

SURVIVAL (DAYS)

Freshly-eclosed
Agraulis

0.21+6 ± 0.028
(10)

5.9 ± 1-1

(10)

Field collected
Agraulis

0.202 + 0.01+2
(65)

3.3 + 1.7
(61)

Freshly-eclosed
Phoebis

0.199 + 0.026
(8)

5.3 ± 0.8
(7)

Field collected
Phoebis

0.225 + 0.056
(39)

5.3 ± 2.8
(33)

F

1+.26

IO.98

P

< 0.01

< 0.0001

137

field-collected individuals was higher than in freshly-eclosed
individuals. In both species, there were highly significant
correlations between initial wet weight and survival time
(Agraulis: r = 0.1+955, n = 71, P < 0.01; Phoebis: r = 0.661+3,
n = 1+0, p , < 0.01). These data are plotted in Figures 5-3
(Phoebis) and 5-1+ (Agraulis ).

Discussion

Adult feeding and energy content of the adult diet have
significant effects on several life-history traits affecting
adult fitness in Agraulis vanillae, including egg production,
fat storage and mortality rate. In addition, data from Phoebis
sennae indicate that survival is strongly correlated with body
weight, which is increased through adult feeding (Chapter IV).
Thus there should be selection on these butterflies to achieve
some level of energy intake through adult feeding.

However, data from Agraulis vanillae suggest that the
relationship between energy intake and fitness is not linear as
assumed by most optimal foraging models. Increasing energy-
intake of females above a given amount does not necessarily
result in corresponding increases in egg production.
Additionally, some females are able to produce a large number of
eggs with very little adult energy intake. Both of these
findings suggest that selection for energy maximization may be
quite variable among different individuals of this species. Egg
production in this species may be constrained by factors other
than energy intake. Abdominal storage space of females may
limit the number of eggs that can be produced at any one time.

138

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II -

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(0

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_l 7

<
>

>

CO 5

3-

1 1 1—

12 .16

-l 1 1 1 1 1 J

.20 .24 .28 .32

NET WEIGHT (g)

Figure 5-3 - The relationship between initial wet weight and
survival in days of Phoebis sennae in a flight cage without
nectar resources. Line is fit by least squares regression. (n
= 1+0, r = 0.66k, p < 0.01, y = 31. Ux - 1.55.)

139

12.0-

10.0-

(0 8.0

>-
<
Q

<
>

>

a.

05

6.0-

4.0-

2.0-

— • • — m •

0.0-

150 .200 .250 .300

NET WEIGHT (g)

.350

Figure 5-4 - The relationship between initial wet weight and
survival in days of Agraulis vanillae in a flight cage without
nectar resources. Line is fit by least squares regression. (i
= 71, r = O.U96, p < 0.01, y = 20. 9x - 0.72.)

Nitrogen or other nutrients may begin to limit egg production
once energy limitations are overcome. Thus increasing energy
intake may increase until other constraining factors make egg
production insensitive to further increases in energy intake.
Selection for energy-maximization may be relaxed once some
threshold energy level has been achieved.

For the nymphalid Euphydryas editha, Murphy et al. (1983)
showed a somewhat similar relationship between adult diet and
fitness. Sucrose in the diet did not significantly affect egg
production during early clutches, but increased the size of
later egg masses. However, the authors suggested that the
potential for later egg masses to survive to maturity was
minimal except during wet years and therefore concluded that
adult feeding increased fitness only during favorable years.
Thus selection pressures for energy-maximization or efficient
adult foraging may be variable in this species as well.

Variable or weak selection for foraging efficiency or
energy maximization in Agraulis vanillae is consistent with
observed foraging behavior in this species. Individuals are
relatively non-selective in flower visitation and will
frequently switch flower species during a foraging bout even
when the flower species differ significantly in energetic
rewards offered. These apparently non-selective individuals may
be choosing flowers for qualities other than energy, such as
amino acid content. There is also significant variation in
length of the foraging period among individuals depending on
age. Older individuals, which have depleted much of their lipid

lUi

reserves, forage later in the day, when energetic rewards are
reduced, than do younger, more lipid-rich individuals. It is
possible that that some individuals may forage very little'
(except perhaps to meet water demands, which are apparently
minimal) if they have emerged from the pupa with large lipid
reserves procured through larval foraging.

Phoebis sennae, on the other hand, is much more selective
during adult foraging and apparently requires extensive adult
feeding to obtain sufficient lipid reserves. Thus, selection
for energy maximization and efficient adult foraging should be
stronger in this species than in Agraulis vanillae. The effects
of adult energy intake on fitness components of Phoebis were not
studied due to difficulty in obtaining sufficient numbers of
larvae during the past two field seasons of this study.
However, from observing foraging behavior and lipid storage
patterns, I would suggest that the effects of energy intake on
survival and fecundity would be more pronounced and more nearly
linear than in Agraulis. Furthermore, since all individuals of
Phoebis apparently emerge from pupae with similar, small lipid
reserves, I would expect less variance in fecundity in this
species due to differences in larval feeding success. In fact,
extensive and efficient adult foraging may be part of an evolved
strategy allowing these butterflies to exploit low-quality
larval food plants and still realize high reproductive success
as adults.

As mentioned earlier, fitness or reproductive success is a
complex function influenced by mortality, fecundity, and other

ll+2

variables. There may be trade-offs involved in adjusting one of
these variables. For example, lowering the age of first
reproduction may also result in decreased probability of
survival later in life. To fully understand the effects of
adult energy intake on fitness, it will be important to study
the interactions between the fitness components studied here and
to integrate these components into a single measure of fitness.

SuTnma,ry
I fed freshly-emerged adults of Agraulis vanillae on
different diets differing in sugar (and therefore energy)
content to determine the effects of adult energy intake on
survivorship, egg production, and fat storage. Increasing the
energy intake of females increased chorionated egg production,
but there appeared to be diminishing returns at higher energy
intake levels. Males that received more energy in the adult
diet depleted their lipid reserves at a slower rate than did
males with low energy intakes. For both sexes, mortality was
significantly reduced by increasing energy intake. Both
Agraulis vanillae and Phoebis sennae showed significant
correlations between body weight and survival time when deprived
of nectar. Although the various components of fitness are
sensitive to energy intake in the adult diet, egg production in
female Agraulis vanillae is influenced by larval feeding as
well, as suggested by a positive correlation between female body
weight at emergence from the pupae and chorionated egg
production.

CHAPTER VI

ADULT FOPAGING IN AGRAULIS VANILLAE AND PHOEBIS SENNAE:

SUMMARY, SYNTHESIS AND CONCLUSIONS

Foraging optimization models assume that animals should
select food items so as to maximize the rate of intake of one or
more dietary components. Most models assume that energy intake
is of primary importance and therefore predict that foraging
animals should structure their diets and foraging activities to
maximize the rate of energy intake while foraging. Because
floral nectar contains predominantly sugars and water,
nectarivores have been suggested to be ideal test subjects for
these energy-maximization models of foraging behavior (Pyke
198la).

A large volume of work conducted on foraging in various bee
species has suggested that these insects generally seem to
select flowers and behave while foraging so as to maximize
energy intake (for references and an excellent review of bee
foraging and energetics, see Heinrich [ 1979b].) This is not
surprising; bees partition their behaviors so that no other
activities occur concurrently with foraging. Thus no
conflicting adaptive goals compromise foraging efficiency.
Furthermore, in many bee species foraging is performed by
sterile workers whose main function is to provision the hive

143

Ikk

with nectar and pollen. This provisioning must not only supply
the nutritional demands of the adults but of the larvae as well.

In contrast, foraging behavior in adult lepidopterans is
subject to a number of conflicting selection pressures. In
these holometabolous insects, feeding may occur during both the
larval and adult stages, and feeding success during both stages
can significantly affect fitness. Whereas all lepidopteran
species feed as larvae, not all species require food as adults
to carry out their reproductive activities, and in some species
the mouthparts are degenerate, making adult feeding impossible.
Even among those species that do feed as adults , there is great
variation in the nature, extent and importance of adult feeding.
The types of food taken by adults are immensely variable,
Including blood, pollen, sap, rotting fruit, dung and nectar.
The amount of food taken during the adult stage is highly
variable as well, as some groups such as satyrids and some
nymphalines are rarely observed feeding, while others such as
long-lived tropical Heliconius species are highly dependent on
adult food resources for fully realizing potential fecundity
(Gilbert 1972; Gilbert and Singer 1975).

Important questions to be addressed regarding adult feeding
in lepidopterans include: What are the relative importances
of larval and adult feeding to maximizing fitness, and
consequently how rigorous are the selection pressures exerted on
adult foraging behavior? It is clear that the importance of
adult feeding spans a continuum among species ranging from
species not feeding at all to those for which adult nutrition is

1U5

essential. The two species studied here, Agraulis vanillae and
Phoebis sennae, appear to occupy different points on that
continuum. Their foraging behavior and energetic profitability
differ significantly. These differences can be explained in
terms of a variety of morphological, ecological and
physiological factors that differ between them and affect adult
foraging behavior as well as the selective pressures to which
such behavior is subjected.

Both species are to some degree selective of nectar
sources. Although this selectivity does increase the rate of
energy intake, Phoebis sennae is apparently under greater
selective pressure to achieve a maximum energy intake during
adult feeding. Nectar uptake rates are higher in Phoebis than
in Agraulis , even though Phoebis has a longer, slightly narrower
proboscis. This requires production of greater pressure drops
by Phoebis but results in a greater net rate of energy intake
while nectar of any concentration is being extracted. It also
reduces the amount of time spent extracting nectar from flowers.
This difference between the species is probably due in part to
the differences in nectar volumes encountered by the
butterflies. Some flowers visited by Phoebis contain up to
several microliters of nectar; minimizing time spent at these
flowers may be important in minimizing total foraging time.
Agraulis , on the other hand, visits mainly low- volume nectar
sources with tenths to thousandths of a microliter of nectar per
flower. The majority of the time spent at these flowers is

1U6

spent finding the nectar (handling time), so increasing the
extraction rate would result in negligible time savings.

The male-female dichotomy in extraction rates of both
species is curious and suggests that sexual differences in
energetic needs, foraging behaviors and selectivity may occur as
well. Males of both species have significantly higher
extraction rates than do females, even though females are of
equal (Phoebis) or greater (Agraulis) body size. Males may be
under greater selection pressure to minimize foraging time or
maximize energy intake due to the time and energy constraints
associated with finding and successfully courting receptive
females. In Agraulis , even when densities are high, courtship
is relatively infrequently seen, and copulating pairs are rare.
Nearly all females collected in the field have at least one
spermatophore in the bursa copulatrix, so finding unmated
females is probably a very time and energy consuming activity.

In terms of the foraging choices and behaviors exhibited by
these two species, differences in foraging success are even more
pronounced. Each species chooses a set of nectar sources that
is distinctly different from that of the other. Some overlap in
nectar sources does occur, but on the average, Agraulis forages
at flowers that are energetically less rewarding than those fed
at by Phoebis. Differences in energetic rewards offered by the
various flower species used by these two butterflies are caused
predominantly by variation in nectar volumes available to
foragers. Mean sugar concentrations of the nectars do not
differ between the resources chosen by the two butterflies.

Although the energy content of nectar in individual flowers is
determined by both volume and sugar concentration, concentration
alone is not correlated with energetic profitability of foraging
in either species. Thus predictions of foraging selectivity
based on nectar concentration and its effect on energy intake
rates during nectar extraction (Kingsolver and Daniel 1979;
Heyneman I983) have little relevance to foraging butterflies,
since other factors such as nectar volume and density of flowers
are much more important in determining overall energy intake
rates than is nectar concentration. Nectar volume, however,
varies tremendously among nectar sources and is the single most
important factor affecting foraging profitability. Differences
in the energetic profitability of foraging between the two
butterflies can thus be attributed mainly to differences in the
average nectar volumes encountered. Phoebis sennae feeds at
flowers that on the average yield greater nectar volumes than do
the flowers visited by Agraulis vanillae. This is because a)
Phoebis is more selective than Agraulis, and avoids low-volume
flower species such as Richardia scabra, Verbena brasiliensis
and Bidens pilosa, which are major nectar sources for Agraulis,
and b) because of its longer proboscis, Phoebis can forage at
high-volume flowers such as Ipomoea spp. from which Agraulis is
morphologically excluded.

Foraging selectivity differs in other aspects as well.
Both species often encounter patches of flowers containing
several flowering plant species differing in their
profitability. In these situations, Phoebis is more successful

1U8

than Agraulis at energy maximization because it discriminates
among flower species and excludes less rewarding flower species
from the diet. Agraulis , however, will alternate visits between
flowers differing significantly in energetic reward, even when
the flower species involved are distinctly different in color
and morphology, and differ by an order of magnitude in energetic
reward (Sida rhomb i folia and Verbena brasiliensis ) . Differences
in selectivity may be due to differences between the butterfly
species in time allocation patterns. Agraulis ' foraging bouts
are shorter and are often interrupted by intraspecific
interactions. Recent theoretical models of time constraints and
their effect on foraging selectivity (Lucas 1983 ) predict that
species that forage in short bouts actually achieve higher
energy intake rates by using a generalized foraging strategy.
Alternatively, Agraulis may be selecting nectar resources on the
basis of factors other than strictly energy content. Water
content is probably not one of these factors, as selection for
water content would result in selection of flowers with greatest
nectar volume and would concomitantly maximize energy intake.
Amino acid content of floral nectars, however, may be involved
in flower selection. Butterfly-visited flowers are known to be
relatively high in amino acid content (Baker and Baker 1975),
and amino acids in the adult diet significantly increase
fecundity of pollen-feeding Heliconius butterflies (Gilbert
1972), although amino acids in the adult diet of a more typical
nymphalid, Euphydryas editha, have relatively minor effects on
fitness (Murphy et al. 1983). Tests of foraging selectivity of

1U9

honey bees (Apis mellifera) have provided little evidence that
these insects select nectar resources on the basis of amino acid
content (inouye and Waller I98U). With regard to the
butterflies and nectar resources studied here, measurement of
amino acid content was impossible with existing technology, so
no conclusions can be made about the importance of amino acids
in the diet and their effects on flower selection.

The lack of selectivity of nectar sources by Agraulis
vanillae may be influenced by several ecological attributes of
this species. These butterflies, like some other nymphalids
(Ehrlich et al. 1975), have quite restricted home ranges. This
may be due in part to the nature of the f oodplant ; Passiflora
incarnata is a rhizomatous perennial that remains available at
any given site for several months. Thus adequate oviposition
sites can apparently be found with relatively little movement.
This has two important consequences for foraging energetics and
floral selectivity. First, total energetic demands are reduced
because of the low travel costs. Second, a given individual
butterfly is probably exposed to only a few potential nectar
sources during its lifetime, so the potential for exercising
selectivity may be quite small. In fact, some populations of
Passiflora used by Agraulis were found to have virtually no
nectar source plants in close proximity. Whether these Agraulis
populations show greater mobility in order to find nectar
sources or simply do without is unknown.

Another ecological factor that may lead to non-selective or
sub-optimal foraging could be the constraints placed on foraging

150

activities by concurrent but conflicting behaviors. Agraulis
does not clearly partition the activity period among different
behaviors. Feeding individuals may simultaneously be searching
for mates or oviposition sites, requiring some modification of
foraging behavior. In addition, these butterflies
thermoregulate by dorsal basking (Clench 1966) and probably
cannot thermoregulate in flight (Heinrich 1981). Frequent
perching may be required to maintain high thoracic temperatures
required for activity, and foraging while basking may be a
secondary goal.

Although Phoebis sennae movement and behavior patterns were
not similarly quantified, it appears from qualitative
observations that this species differs significantly from
Agraulis in these respects. The larval hostplants, Cassia spp.,
are annuals that are much less predictable in time and space
than is Passiflora. Although Cassia plants are available from
May /June through October, individual plants appear to be
relatively short-lived. Thus, the hostplant that a
freshly-emerged Phoebis fed on as a larva may be inadequate for
oviposition, and greater mobility may be required for finding
suitable oviposition sites. The flight behavior of Phoebis is
more rapid, direct, and covers much greater distances in a given
time period than does that of Agraulis. Phoebis is frequently
observed nectaring or flying in areas devoid of the larval
foodplants, suggesting that there may be distinct segregation of
foraging and reproductive activities, which could lead to

151

greater selection for minimizing foraging time or maximizing
energy intake in this species.

Certainly Phoebis is more efficient while foraging at the
same resource arrays as Agraulis. The greater selectivity of
Phoebis has been discussed earlier; Phoebis consistently
restricts visitation to the more energetically rewarding nectar
sources that are available. In addition, Phoebis spends less
time in flight than does Agraulis when foraging at the same
nectar sources. Between flower flights are more direct,
reducing foraging costs and increasing energetic profitability.
The greater floral selectivity of Phoebis , its avoidance of
low-reward flowers, and its more efficient flight behavior
all suggest that this species is subject to greater selection
for energy maximization than is Agraulis vanillae.

The need for profitable adult foraging is further augmented
by resource storage patterns during larval feeding and
metamorphosis. It is not reasonable to argue that larval
feeding strategies have caused the observed differences in adult
foraging strategies; undoubtedly, the feeding strategies during
larval and adult stages are integrated during the evolution of
each species, and modifications in one stage allow or
necessitate changes in the feeding behavior of the other stage.
The integration of larval and adult feeding strategies, as
suggested by Boggs (l98l), is nicely illustrated by Agraulis and
Phoebis. Agraulis individuals eclose from the pupae with
relatively large lipid reserves (12-15% of dry weight in males,
ll+_20% in females ) , and the magnitude of fat storage during

152

metamorphosis has important effects on "both survivorship and
fecundity of these butterflies. Adult foraging appears to
supplement these larval fat stores , but does not always seem
to be necessary for maximizing fitness. Some females of
Agraulis that are fed only water as adults exhibit fecundities
equal to those of females on energy-rich diets. Although energy
intake of adults can reduce the rate at which lipid reserves are
depleted, Agraulis does not store lipids from adult feeding
above the level that is attained at metamorphosis.
Field-collected individuals show a consistent decline in lipid
reserves with age, although this decline may not be linear. If
scale loss is a linear indicator of age, then these
field-collected individuals show a rapid depletion of lipid
reserves during the first few days of life, with the rate of
lipid depletion slowing when lipid levels fall below 7-8% of dry
weight. There appears to be a shift in foraging strategy
accompanying the drop in lipid reserves. Older, lipid-depleted
individuals forage for longer periods than do younger,
lipid-rich butterflies. I suggest that there are correlated
changes in reproductive behavior as well; younger butterflies
may spend a greater proportion of their activity period in mate
search, courtship, and oviposition behaviors than do older
butterflies. Once reproductive reserves have been partially
depleted, foraging time may increase to reduce the rate of lipid
depletion. This would suggest that younger butterflies
may be under greater time constraints, and therefore greater
selection for energy maximization or time minimization while

153

foraging. Age-related differences in foraging selectivity and
energetics would therefore be predicted.

Phoebis sennae exhibits a totally divergent strategy of
adult-larval feeding integration. These butterflies emerge from
the pupae with small lipid reserves (< 5% of dry weight) and
require profitable adult foraging to boost these lipid reserves,
which increases survivability and probably is required for
maximum fecundity as well (Stern and Smith i960 ) .
Field-collected butterflies show a consistent increase in lipid
reserves with age, up to levels as high as 50% of dry weight
(compared to maximum of 20% in Agraulis ) . It is probably
impossible for a butterfly to survive with lipid reserves below
3 or h% of dry weight (no individuals of either species were
found with lipid reserves lower than this), and Phoebis responds
to poor larval feeding conditions not by reducing lipid storage
at metamorphosis, but by not attaining full body size while
keeping the proportion of body weight allocated to lipid within
the 3-5% range. Given this low level of lipid reserves at
eclosion, inefficient or non-profitable adult foraging would be
expected to have serious fitness consequences such as reduced
longevity or low fecundity. Since this species is more mobile,
individuals that do not rapidly acquire lipid reserves
sufficient for lengthy flights may be unable to find other
conspecifics for mating or suitable oviposition sites, and may
therefore not reproduce at all. I therefore suggest that
selection for profitable adult foraging by Phoebis is greater
than in Agraulis.

151*

Adult Foraging in Lepidopterans — A General Hypothesis

Adult foraging in lepidopterans, as illustrated by Agraulis
vanillae and Phoebis sennae, obviously shows a wide range of
variation among species. Although there is probably a continuum
of adult feeding strategies, I suggest that most of these
strategies can be grouped into two general classes: obligate
vs. facultative adult feeders. These adult foraging strategies
are closely linked to larval feeding behavior and energetics.
For those species that are primarily nectarivorous as adults
(and therefore acquire mainly energy through adult foraging),
lipid contents at eclosion may be an excellent general indicator
of adult foraging strategy, as suggested by Boggs (1981). The
relationship between lipid storage at metamorphosis and adult
foraging energetics invites further corroboration.
Obligate Adult Foragers
These species , exemplified by Phoebis sennae, for a variety
of reasons emerge from the pupae with low energy reserves. This
may be due to poor foodplant quality, selection for rapid
development that may be fostered by variable environmental
conditions (rapid foodplant senescence, heavy predation or
parasitism on larvae, etc.), or other undetermined factors.
Large lipid reserves may be required for mobility, mate location
and/or egg production. These species are under heavy and
constant selection pressure for efficient and profitable adult
foraging in order to acquire these required lipid reserves.
Adult fitness in these species is thus most closely related to
adult foraging success. They are expected to exhibit

155

characteristics of optimal foragers, i.e., high selectivity of
nectar resources based on energy content, minimization of
foraging costs through efficient flight patterns while foraging,
and minimization of foraging time at high-volume flowers via
rapid nectar extraction rates. In general, any physiological or
behavioral mechanisms that would reduce energy expenditures on
non-reproductive activities and maximize lipid storage would be
strongly selected for. There may also exist a relationship
between proboscis length and foraging strategy, as suggested by
Opler and Krizek (I98U). I would expect these obligate foragers
to have on the average longer proboscides that would increase
the range of floral resources available to them.

Because of their requirements for highly profitable adult
foraging, these species might be restricted in their ability to
exploit different habitats containing the larval foodplants to
those that contain a variety of floral resources or those that
consistently contain one or more high reward species.
Alternatively, obligate foragers may be selected for high
mobility to maximize exposure to a variety of nectar sources.
It is interesting that over the three field seasons of this
study, the population densities of Phoebis sennae fluctuated
much more dramatically than did those of Agraulis vanillae.
This is a general characteristic of the genus Phoebis (Howe
1975) and may be attributable to fluctuations in nectar plant
availability induced by differences in precipitation, which was
highly variable among seasons.

156

Facultative Adult Foragers
These species, illustrated by Agraulis vanillae, probably
show more variation in feeding strategies than do obligate
foragers, as they may range from species that rarely or never
feed (such as some satyrid butterflies and saturniid moths) to
those for which adult feeding may be of variable importance.
These species in general will emerge from the pupae with large
lipid reserves, and the magnitude of these lipid reserves may be
closely linked to realized adult fitness. Thus in this category
adult fitness is more dependent on larval feeding success than
in the obligate forager category. Adult feeding, where it
occurs, is seen mainly as a buffer mechanism to compensate for
variable environmental conditions encountered by the larvae. In
cases where larval feeding conditions are poor, adult foraging
activity can be increased to compensate for insufficient
reproductive reserves acquired by the larvae. However,
individuals that are successful during larval feeding may
require little or no adult feeding to realize full fecundity or
fitness. Consequently, selection for optimal adult foraging (in
the energy -maximization sense) may be weak or absent, and
probably variable among individuals. I therefore expect these
species to exhibit non-selective adult foraging, inefficient
foraging behavior (such as large proportion of foraging time
spent in flight), or relatively low nectar extraction rates. In
addition, species within this class of foragers may be
characterized by shorter proboscis lengths as access to a wide

157

variety of flowers is unnecessary. These species would be
expected to have the ability to exploit a wider range of
habitats in which the appropriate foodplant occurs, as abundant
nectar resources would not be required for reproduction to take
place .

APPENDIX

A SIMPLE METHOD FOR MEASURING NECTAR

EXTRACTION RATES IN BUTTERFLIES

The rate at which nectarivorous animals extract nectar from
flowers is one of the major parameters determining the
instantaneous rate of energy intake, a quantity that is presumed
to maximized by natural selection (Pyke et al. 1977 )• The rate
of energy intake equals the rate of nectar extraction (ul/s)
multiplied by the energy content of the nectar (joules/ul). The
rate of nectar extraction has been included in theoretical
models of feeding energetics in butterflies (Kingsolver and
Daniel 1979) and nectarivorous animals in general (Heyneman
1983 ) • Although this rate has been measured in hummingbirds and
incorporated into models of feeding energetics (Hainsworth and
Wolf 1972), it has apparently never been measured in butterflies
(Kingsolver and Daniel 1979 )• Here I present a simple technique
for measuring extraction rate in butterflies that may be
applicable to other nectar feeders as well.

Nectar of a known concentration is loaded into a calibrated

microcapillary tube (Drummond Microcaps) that is mounted on a

small balsa platform with a millimeter scale alongside the

158

159

capillary tube. The platform also includes a perch for the
feeding butterfly to grasp. The platform is displaced at a
slight angle from horizontal to cause the nectar column to move
downward as it is removed. Because many butterflies maintain a
body temperature several degrees above ambient (Rawlins 1980),
and because extraction rate in poikilotherms is most likely
temperature dependent, I placed both the butterflies and the
apparatus inside a styrofoam chamber maintained at about 28 C
with a heat lamp.

This technique for measuring extraction rates takes
advantage of the apparently innate feeding response in
butterflies that is released by the contact of the proboscis
with a sugar solution. The butterfly is manually placed onto
the perch and its proboscis is coaxed into contact with the
leading edge of the nectar column in the microcapillary tube.
As nectar extraction proceeds, the meniscus at the trailing edge
of the nectar column can be timed with a stopwatch as it moves
along the scale. I have had best success with 100 ul
microcapillary tubes (as opposed to smaller sizes), because the
most difficult part of the procedure is in establishing the
initial contact between the proboscis and the nectar. Larger
microcapillary tubes have larger internal diameters, thus
facilitating this part of the procedure. However, reducing the
size of the capillary tube would increase the resolution of the
system.

I have used this method with several species of Papilio
(Papilionidae) , Basilarchia archippus and Agraulis vanillae

160

(Nymphalidae) , and Phoebis sennae (Pieridae) with equal success.
All of these species exhibit a similar response to the initial
contact of the proboscis with the sugar solution; the proboscis
begins a series of probing motions that sometimes pull the tip
out of the nectar column. If the tip reestablishes contact with
the nectar within a few seconds, feeding begins. Once the
butterfly begins feeding, it is no longer necessary to restrain
the insect, since it grasps the perch and feeds at it would at a
flower. In some species, there is a characteristic folding and
unfolding of the wings while feeding.

Although my use of this method has been to investigate the
relationship between nectar concentration, viscosity, and
extraction rates (Chapter II ), this technique may also be useful
for studies of adult diet in which the effect of various dietary
constituents on longevity or fecundity are studied. In studies
of this type, researchers often feed the insects to satiation
(e.g., Murphy et al. 1983). Using the method described here,
one can control precisely the volume of nectar imbibed by an
individual insect by regulating the volume placed within the
capillary tube or by simply removing it from the feeding
apparatus once a predetermined volume has been consumed.

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BIOGRAPHICAL SKETCH

Peter Gregory May was born on October 2, 1955, to Rolland L.
and Sally S. May, in Jacksonville, N.C. Most of his childhood was
spent in northern Virginia, where he graduated in 1973 from
Stonewall Jackson High School in Manassas, Virginia. He received
his college education at St. Andrew's Presbyterian College in
Laurinburg, N.C. and George Mason University in Fairfax, Va. ,
where he received his B.S. and M.S. degrees in 1977 and 1979,
respectively. It was during this period that he began to develop
his skills as a hoopster. In 1979, he moved to Gainesville to
enter the Department of Zoology and play short forward for the
North Florida Renegades. Behind his strong shooting from the
field, the Renegades climbed to a ranking of sixth in the nation
in 1983-14. Pete shoots about 70% from the charity stripe and is
deadly from inside 20 feet. Despite these skills he is a totally
unselfish player and excels at the assist. His biological
interests center around avian community and behavioral ecology,
plant reproductive ecology, and insect foraging ecology. Pete's
hobbies include wildlife photography and sky diving.

173

I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree of Doctor of Philosophy.

C(X\AMt^f [I' tfl^/j

'/a«'i

Carmine A. Lanciani, Chairman
Professor of Zoology

I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree bf Doctor of Philosophy.

Lincoln P. Brower, Co-chairman
Professor of Zoology

I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree of Doctor of Philosophy.

H. Dane Brockmann

Associate Professor of Zoology

I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree of Doctor of Philosophy.

1

i « y I

Thomas C. Emmel
Professor of Zoology

I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree of Doctor of Philosophy.

Catherine C. Ewel
Associate Professor of Forest
Resources and Conservation

I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree-^of Doctor of Philosophy.

Hardy
Professor of Zoology

This dissertation was submitted to the Graduate Faculty
of the Department of Zoology in the College of Liberal Arts
and Sciences and to the Graduate School and was accepted as
partial fulfillment of the requirements for the degree of
Doctor of Philosophy.

May, 1985

Dean, Graduate School

UNIVERSITY OF FLORIDA

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