Download mesquite seeds, bruchid beetles, and

FACTORS INFLUENCING POPULATION DYNAMICS AND STABILITY WITHIN
A THREE TROPHIC LEVEL SYSTEM: MESQUITE SEEDS, BRUCHID BEETLES,
AND PARASITIC HYMENOPTERA
by
Robert A. Kistler
.
A Dissertation
Submitted in Partial Fulfillment
of the Requirements for the Degree of
Doctor of Philosophy
in Zoology
Northern Arizona University
May 1985
ABSTRACT
FACTORS INFLUENCING POPULATION DYNAMICS AND STABILITY WITHIN
A THREE TROPHIC LEVEL SYSTEM: MESQUITE SEEDS, BRUCHID
BEETLES, AND PARASITIC HYMENOPTERA
Robert A. Ktstler
A three trophic level ecosystem consisting of the seeds
of velvet mesquite (Prosopis velutina: Leguminosae), four
species of seed beetles (Coleoptera: Bruchidae) and a
complex guild of more than 17 species of parasitoids
(Hymenoptera) was studied in the Verde Valley in central
Arizona.
The phenology of marked trees in six populations
of mesquite was monitored and seed pods were collected from
these trees every two weeks from 1981 through 1983.
The
insects .in the seeds were reared in the laboratory.
Laboratory and field experiments examined the physiological
ecology of the bruchids and parasitoids and the capabilities
of these two guilds to regulate populations of their
respective hosts.
Individual mesquites produced a large pod
crop, consisting of high quality seeds, every two years at
the most.
Apparent energy and nutrient limitations either
inhibited pod production totally in alternate years or
limited seed production severely if pods were produced.
Along with a lack of synchrony in reproduction, this created
a tremendous heterogeneity, in the number and ease of
location, of good seeds which could be used by the bruchids.
This heterogeneity in space and time combined to severely
limit the impact of the seed predators on the seed
populations.
Key factor analysis of ovule and seed
mortality across the six populations indicated that
pre-predation ovule mortality accounted for most of the
decrease in potential reproductive output, while seed
predators were not a significant key factor.
The bruchid
species were differentially adapted to the extreme
temp~ratures
experienced in the field, with Algarobius
prosopis being most tolerant to temperature variation.
Similarly,
!· prosopis was most adapted, via a modified
oviposition strategy, to attack by trichogrammatid egg
parasitoids.
The other three bruchid species, Mimosestes
amicus, Mimosestes protractus and Neltumius arizonensis were
the less successful members of the seed predator guild.
The
diverse community of larval and egg parasitoids possessed a
strong capability to regulate populations of the second
trophic level.
Bruchids were not significant in
t~is
and should exert little or no selective pressure on
reproductive strategies of mesquite.
system
TABLE OF CONTENTS
Page
ABSTRACT
i i
PREFACE .
vi
ACKNOWLEDGMENTS
vi i
LIST OF TABLES
vi i i
LIST OF FIGURES •
X
CHAPTER
1.
2.
3.
Genera 1 In trod u c t i on.
State of Knowledge: Bruchid-Legume Systems.
Literature Cited . .
•
•
•
•
•
•
•
•
•
•
0
•
0
•
Q
Seed Production in Prosopis velutina
(Leguminosae): Variability and the cost of
Reproduction in a .Desert Phreatophyte • .
Introduction
Methods . . .
Study site •
Study methods.
Results . . . . .
Cost of reproduction
. . • . . . . •
Variability in reproductive output •
Discussion
Literature Cited .
Reproductive Strategies in Prosopis velutina
(Leguminosae) and their Effect on Seed Predation
by Bruchid Beetles . . . . . •
Introdu.ction .
Methods
Results
F~lower production and mortality. .
Non-predation ovule and immature seed
mortality . . . . . . . . .
Predation related mortality.
Variation in seed production and predation
by bruchid beetles • • • . •
. . . . .
i v
1
7
12
18
19
23
23
23
26
29
34
44
53
62
63
65
69
69
71
73
77
CHAPTER
Page
Key factor analysis: The relative influence
of factors on seed survivorship •
Discussion
Literature Cited • • • . • . . . • •
4.
99
102
108
113
113
114
117
137
154
The Role of the Third Trophic Level in the
Mesquite-Bruchid Ecosystem . . . • . • . . . .
Introduction . . . . . . . . .
Methods
Results and Discussion
Literature Cited
161
162
163
165
175
General Discussion
Literature Cited
177
184
.
6.
87
The Effect of Temperature on Mesquite Bruchids
(Coleoptera): Physiological Strategies of a
Guild of Seed Predators
Introduction . • .
.
Methods • • • .
Field studies •
Laboratory studies
Results . • • • • .
Discussion
Literature Cited
.......
5.
82
v
PREFACE
11
For the world of science and evolution is far more nameless and
elusive and like a dream than the world of poetry or religion; since
in the latter, images and ideas remain themselves eternally, while it
is the whole idea of evolution that identities melt into each other as
they do in a ni ghtmare 11 •
G. K. Chesterton
The Ball and The Cross
11
lt is interesting to contemplate an entangled bank, clothed with
many plants of many kinds,with birds singing on the bushes, with various
insects flitting about, and with worms crawling through the damp earth,
and to reflect that these elaborately constructed forms, so different
from each other, and dependent on each other in so complex a manner,
have all been produced by laws acting around us
11
•
Charles Darwin
The Origin of Species
vi
---------------------------------------------------------------------------,
ACKNOWLEDGMENTS
I thank Russell Balda, Dean Blinn, Wally Covington, C.D. Johnson,
Peter Price, and Con Slobodchikoff for their help and support as members
of my research committee.
I thank C.D. Johnson for providing research
space and materials and for identifying the bruchids in this study.
I
would especially like to thank Peter Price for taking the time to listen,
for acting as an exemplary ecologist, and for reviewing not only my
dissertation, but also many other manuscripts.
I thank all of my graduate school colleagues, who through interaction
and discussion have been a major part of my graduate training.
I
especially thank Doug Hay, Martin Hetz, Kris Mobley, Bob Graybosch, and
Ken Paige.
I thank the Department of Chemistry, Northern Arizona University,
for the generous loan of their Gilson respirometer, which made a large
part of this work possible.
I dedicate this dissertation to my wife, Candi, my daughter, Kareena,
and my God, without whose support, patience and guidance this all would
not have been possible.
vii
LIST OF TABLES
Table
2-1.
Page
Descriptive data on the. six populations of Prosopis
velutina examined in the study. . . . . . . . . . .
24
Early reproductive structures in P. velutina at six
sites in 1983 . . . . . . . . . . -. . . . .
30
2-3.
Reproductive costs for tree #1 at site 1 in 1983. . .
32
2-4.
Pod and seed production and abortion in P. velutina .
35
2-5.
Two-way analysis of variance of total seeds and total
good seeds by year and site . . . . . . .
36
2-6.
Pod and seed data for e1ach site by year . .
37
3-1.
The number of inflorescences produced and setting fruit
in six populations of f .. velutina in 1983 . . . .
70
Seed mortality in!:_. ve,lutina in six sites over three
years . . . . . . . . . . . . . . . . . . . . . . . .
72
Stage of ovule or seed attacked by Lepidoptera and
Bruch i dae in P. ve 1uti na. . . . . . . . . . . . . .
75
Two-way analysis of variance of bruchid and moth emergence by site and year. . . . . . . . . . . . . . .
76
Correlation coefficients of the number of bruchids
emerging from seed pods with various factors. . . .
78
Key factor analysis of flower, ovule, and seed mortality
in six populations of P. velutina over a three year
period . . . . . . . . - : - · . . . . . . . . . . . . . . .
83
2-2.
3-2.
3-3.
3-4.
3-5.
3-6.
4-1.
4-2.
Relative abundance of b:ruchids in the mesquite seedpredator guild. . . . . . . . . . . . . . . . .
Numbers of bruchids eme,rged from 30 pod
!:_. velutin.a over a three year period. .
sample~
119
of
120
4-3.
Internal temperatures of mesquite pods. . . . .
123
4-4.
Temperature constants for bruchids that attack seeds of
P. velutina. . . . . . . . . . . . . . . . . . . . .
135
Adult weights and percent water for the four members
of the mesquite bruchid guild . . . . . . . . . . . .
138
4-5.
vi i i
Table
Page
4-6.
Egg weights and percent water for the members of the
mesquite bruchid guild . . . . . . . . . . . . .
5-1.
Parasitoids of the mesquite seed predator guild . . . . . . 170
i X
. 139
LIST OF FIGURES
Figure
Page
1-1.
The mesquite-seed predator-parasitoid food web . . . . .
11
2-1.
Phenology of reproduction in six populations of Prosopis
velutina over three years. . .
27
2-2.
Climatic data for 1981 to 1983 for the study sites . . .
28
2-3.
Parental investment in terms of biomass and water in
various stages of flowering and fruiting in f.. velutina.
31
Cost of pod production in terms of dark respiration and
biomass of pods in .!:.:_ _glandulosa . . . . . . . . . .
33
Relationship of pod production with tree size in f..
ve 1uti na . . .
. . . . . . . . . . . . .
. . . . .
38
2-6.
Pod production in f.. ve!l utina over three years
40
2-7.
The number of pods produced per unit volume of tree
foliage as a function of tree size . . . . . .
42
2-8.
Reproductive gain as a function of reproductive investment in P. velutina. . . . . . . . . . . . . . . . .
43
The percent of seeds killed by bruchids in relation
to the total number of :good seeds produced per tree.
79
The proportion of seeds killed by bruchids as a
function of the proportion of good seeds produced
per tree . . . . . . . . . . . . . . . . . . . .
81
Key factor analysis of reproductive mortality in five
populations of f.. velutina in 1983 . . . . . . . .
85
Key factor analysis of post-flowering reproductive
mortality in f.. velutina . .
. . . .
86
2-4.
2-5.
3-1.
3-2.
3-3.
3-4.
4-1.
Temporal patterns of climate and the bruchid and tree
populations. . . . . . . . . . . . . . . . . . .
118
4-2.
Diurnal temperature variation in a mesquite tree . .
122
4-3.
The relationship of metabolic rate and temperature for
adults of the mesquite seed beetle guild . . . . .
125
The relationship of metabolic rate and temperature for
larvae of the mesquite seed beetle guild . . . . .
126
4-4.
X
Figure
4-5.
4-6.
4-7.
Page
Relationship of metaboiic rate with dry weight for
11 species of Bruchidae . . . . . . . . . . . . . .
. 12 7
Relationship of fecundiity and temperature for the
mesquite bruchid guild . . . . . . . . . . . . . .
. 130
Longevity"- temperature relationships for the adult
bruch ids . . . . . . . . . . . . . . . . . . . . .
. . 131
4-8.
Weekly fecundity over the lifespan of the bruchids . . . . 132
4-9.
Developmental rates and times of the egg and larvalpupal stages at the experimental temperatures. . . . .
134
Relative survivorship of larve of the three species of
bruchids . . . . . . . . . . . . . . . . . . . . . .
136
Relation between wet weight and dry weight of adult
bruchids......................
140
4-10.
4-11.
5-1.
Population dynamics of the larval parasitoids and their
host bruchids . . . . . . . . . . . . . . . . . . . . . . . 166
5-2.
Population dynamics of the bruchids, larval parasitoids,
and egg parasitoids in the mesquite ecosystem for 1983
at site 1. . . . . . . . . . . . . . . . .
. 167
5-3.
The relationship between egg densities in the field
and the number of bruchid eggs parasitized . . .
169
The subdivision of the larval bruchids by their
parasitoids. . . . . . . . . . . . . . . . .
171
Differential rates of parasitism of the eggs of three
species of bruchids. . . . . . . . . . . . . . . . . .
172
5-4.
5-5.
xi
CHAPTER 1
GENERAL INTRODUCTION
1
2
Our understanding and knowledge of ecological
communities has recently been questioned.
Lawton and Strong
(1980) reviewed work on insect communities and concluded
that competition may not explain all or most of the patterns
of organization seen in these communities.
Similarly Wiens
(1977) and Connell (1980) questioned the role of competition
in the dynamics of populations within other animal
communities.
Price et al. (1980) stress that most knowledge
of ecological communities is limited to at most two trophic
levels, with a striking void of information on the roles
played by predators and parasitoids in communities, despite
the fact that all three major trophic levels appear to be
tightly linked.
In order to address these problems it is necessary to
examine ecological communities as a unit to elucidate those
factors which regulate the dynamics of the component
species.
Lawton and Strong specifically propose that a
climate which is harsh and variable, host plant phenology,
patchiness of resources and natural enemies must all be
considered to understand community dynamics.
This research
examines a three trophic level system in an attempt to
synthesize a comprehensive picture of _the dynamics of the
system and those factors that are important in the dynamics,
regulation and stability of each of the component trophic
levels.
Regulation of populations has been divided into two
major types.
Andrewartha and Birch (1954) through their
3
work on Thrips imaginis found four climatic factors that
could explain 73% of the population variation.
Morris
(1969) explained much of the variation in northern
populations of the fall web worm (Hyphantria cunea) by
temperatures in the fall feeding period.
I have
demonstrated that temperature may greatly affect fecundity,
development and physiology of a set of desert beetles in the
family Bruchidae (Kistler 1982).
The above examples
demonstrate that abiotic factors, especially in harsh,
variable environments, do have a large impact on insect
populations.
Biotic factors also may regulate populations,
through food limitation (food quality or amount),
competition within a trophic level, predation between
trophic levels and through coevolution both within and
between trophic levels.
The quantity of food is usually not limiting for
herbivorous insects although food quality and accessibility
are largely variable as a result of defensive mechanisms of
plants.
However, food quantities may be directly limiting
to higher trophic levels.
Mechanical defenses of plants may
affect both herbivorous and granivorous insects and their
predators.
Seed pod morphology (thickness and hardness) and
behavior (gum production, indehiscence) may negatively
affect both bruchid beetles that feed in the seeds contained
within the pod (Center and Johnson 1974, Johnson 1981a) and
the parasitoids that oviposit on the larvae developing
within the seeds (Price et al. 1980).
Seed coats may also
4
be a barrier to the entry of bruchid larvae and to
oviposition by parasitoids.
Stator sordidus and S.
Two species of bruchid beetles,
limbatus, could not enter intact
seeds of Cercidium floridum or Parkinsonia aculeata until
after I had removed the seed coat (Kistler unpub. data,
Johnson 1981b).
Defensive chemicals produced by plants may also affect
the dynamics of higher trophic levels.
The optimal defense
theory that has been developed by Feeny (1976), Rhoades and
Cates (1976), and Rhoades (1979) predicts that plants should
be protected by chemicals that either make the entire plant
(or parts of the plant that are most important) inedible or
difficult and expensive to digest.
b~
well protected.
Seeds especially should
Janzen (1977) showed that Callosobruchus
maculatus (F.) larvae die after attempting to eat many
species of non-host seeds.
The mean developmental time of
Stator sordidus is lengthened significantly on certain
non-host seeds (Johnson 1981b).
These chemical defenses may
in turn be detoxified by insects (Rosenthal 1982), and even
used as a defense against predators and parasitoids (Cambell
and Duffey 1979).
The plant, therefore, has an array of
potential defenses against attack, which either may decrease
attack directly by mechanisms like those above or indirectly
by association with other plants in a "defensive guild"
(Atsatt and O'Dowd 1976).
However, each strategy of defense
also may have a negative impact on predators and parasitoids
of the plant-attacking insects.
The optimal strategy must
5
invariably be a compromise solution yielding the highest
possible protection from attack over both ecological and
evolutionary time.
Such plant defenses may be stabilizing
or may result in fluctuations within insect populations
(Haukioja 1980).
Predators and parasitoids may also regulate populations
of insects within a community.
The selective pressure
placed upon insects by their enemies may result in one of
three potential outcomes.
Enemies may (1) strongly suppress
insect populations, leading to local extinctions; (2)
coevolve
~ith
their prey or (3) result in selection for
"enemy free space" (Lawton 1978) in prey populations.
Suppression of prey by enemies may either be stabilizing or
destabilizing within a community.
Paine (1966) demonstrated
that predators are capable of regulating community
composition and dynamics.
Hassell (1978) reviewed the
effects of enemies on insect populations and factors that
determine when relationships will be stabilizing or
destabilizing.
Utida (1957) and Fujii (1983) have shown
that two non-coevolved parasitoids may either stabilize or
destabilize their host bruchid populations.
The
destabilizing parasitoid, Heterospilus prosopidis Viereck
(Hymenoptera:Braconidae) has a very high searching
efficiency and causes violent oscillations of the host
population, resulting in local extinction of the parasitoid.
In contrast, Anisopteromalus calandrae Howard
(Hymenoptera:Pteromalidae) stabilizes the host population
6
resulting in stable coexistence. I examined some major
population parameters of these host and parasitoid
populations and concluded that the major factor responsible
for these different responses was the different functional
responses of the two parasitoids (Kistler 1979, 1985).
Coevolution of enemies with their prey has been
conceptually well developed, but its importance in natural
systems is still largely conjectural.
Pimental (1968) and
Pimental et al. (1978) found that in a laboratory system of
the house fly (Musca domestica) and its parasitoid (Nasonia
vitripennis Walker) the fecundity of the parasitoids
decreased after a few generations.
They concluded that
coevolution in host-parasitoid systems may result in
selection for intermediate rates of increase in the
parasitoid populations.
This phenomenon was also
demonstrated in the rabbit-myxomatosis virus introductions
in Australia and so is possible in semi-natural systems
(Fenner 1971).
Similarly, coevolution has been thought to
be prominent in legume-bruchid systems (Janzen 1969, Center
and Johnson 1974).
This work addresses the role of abiotic factors,
competition, predation, stability and coevolution and their
effects on and importance in ecological communities by a
comprehensive examination of a natural three trophic level
ecosystem.
An examination of a simple, natural, three
trophic level system should provide some possible answers to
questions about community dynamics by linking together for
7
one system all the potential interactions and ecological and
evolutionary responses of all three trophic levels.
Some
potential interactions that might be better understood by
such a comprehensive approach are:
the responses of the
plant to its enemies and to the predators of these enemies,
the responses of the plant eaters to the defenses of the
plant and to its enemies, and the responses of the
parasitoids to the defenses of the herbivores, and to the
attraction mechanisms of the plant.
State of Knowledge:
Bruchid-Legume
Systems
A large store of information is available on
interactions between bruchid beetles and their host seeds.
This provides an excellent conceptual base for two of the
major trophic levels of the legume-bruchid-parasitoid
community examined in this study.
Most of these data and
resulting hypotheses have resulted from the work of D.H.
Janzen, C.D. Johnson, and their students.
Seeds are the most important plant part in that they are
directly related to the reproductive fitness of the plant.
The parent tree should be under strong selection to evolve
the best strategy to produce the most viable
~eeds
and
seedlings at the least possible cost (Rhoades 1979).
At
least four hypotheses have been proposed as to strategies
used by plants to protect their seeds.
Plants may:
(1)
produce many small seeds in an.effort to satiate the local
seed predators (Janzen 1969), (2) produce relatively fewer,
8
more well protected seeds (increased seed size, increased
chemical protection, or increased mechanical protection,
Janzen 1969, Center and Johnson 1974, Rosenthal 1982), (3)
produce seeds that are attractive to dispersal agents which
dis'perse seeds away from the parent plant (Janzen 1972,
1976, Janzen and Martin 1981, Lamprey and Halevy 1974), or
(4) produce such a wide mosaic of seeds and seed pods both
within one tree and in the tree population that seed
predators are unable to attack most seeds (Whitham and
Slobodchikoff 1981).
These strategies may either be
employed by different plants or several strategies may be
used by the same plant or species of plant.
Seed-feeding insects such as bruchid beetles should in
turn be under intense selection to circumvent ·any defensive
mechanism of their host plants.
For the most part, this
selection appears to have resulted in increased specificity
in the Bruchidae.
The majority of bruchids are extremely
host specific, resulting from a hypothesized coevolution of
specific bruchids with specific host plants (Johnson 1981a).
This specificity can result from chemical coevolution with
the seeds of a given plant (Rosenthal 1982) or from a
coevolution with a specific seed dispersal strategy.
Johnson (1981a) described three guilds of bruchids feeding
on legume seeds.
One guild attacked only seeds contained in
indehiscent pods on the parent tree, while another guild
attacked only seeds from partially dehiscent pods and a
9
third only attacked seeds from dehiscent pods which had been
dispersed away from the parent tree.
Some bruchids may
alternately be extreme generalists with a high fecundity and
may attempt to satiate the
legum~
community with eggs, some
subset of which will survive (e.g., Stator limbatus, Kistler
1982).
The strategy chosen by a given bruchid may be due in
large part to physiological constraints on the bruchids or
to selection for enemy-free space.
Parasitoids are the third major trophic level component
in legume-bruchid systems.
Comparatively little is known
about their significance in these systems.
Center (1974)
and Center and Johnson (1976) list many parasites in most of
the legume-bruchid systems that they have examined in
Arizona, and these may have a significant impact on both the
bruchid populations and on the host plants and their
appropriate evolutionary strategies.
There is an extensive theoretical and descriptive data
base on bruchid-legume systems and this makes it feasible
and desirable to examine these communities.
These
communities are simple, in that they consist of:
(1) a
quantifiable seed resource, which is also a potential
measure of the plant's fitness, (2) seed attacking bruchid
beetles, which develop as larvae inside the seeds and are
thus also easily quantifiable, and (3) the parasitoids which
develop on the bruchid larvae within the seeds.
The large
data base on the bruchid-legume interactions will make the
10
task of adding the third trophic level much simpler and will
prove helpful in understanding the function of the
parasitoids in the system.
Five major questions were addressed in the examination
of a three trophic level desert ecosystem in this study
(Fig. 1-1).
1).
What factors regulate seed production
prior to seed dispersal and seed predation?
2). Do bruchid
beetles exert significant selective pressure on reproductive
strategies of the host plant?
3). Does the tree exert any
selective pressure or regulatory action on the populations
of its seed predators?
4). What factors regulate and
organize the complex community of seed predators?
5). Are
the parasitoids, which make up the third trophic level,
important in the regulation or organization of the seed
predator communities or alternately are the parasitoids an
important component of the plant's defensive strategies
against seed predators?
'lliiRD TROPHIC
Mmi
EGG
EARLY lliSTAR
lEVEL
PARASI10Ill3
PARASI10Ill3
PARASI10ID3
. (5)
SECX>ND
(1?)
LATE lliSTAR
PARASI10Ill3
(1+)
TROPHIC
lEVEL
MISC.
(4)
BRUCH IDS
GENERALISTS
MICROLEPIDOPTERA
SPECIALISTS
MIMOSESTES N1ICUS
ALGAROBIUS PROSOPIS
NELTUMIUS ARIZONENSIS
MIMOSESTES PROTRACTUS
FIRST TROPHIC
AL'IERNA1E
lEVEL
HOST
I
MESQUI'IE
SEEll3
SEEll3
Fig. 1-1. The mesquite-seed predator-parasitoid system. The numbers
in parentheses under the parasitoids indicate the minimum number of
species. Miscellaneous parasitoids includes all those species that
attack either all larval stages or for which the stage of attack is
uknown.
.......
.......
12
LITERATURE CITED
Andrewartha, H.G. and L.C. Birch. 1954. The distribution and
abundance of animals.
Chicago, University of Chicago Press.
Atsatt, P.R. and D.J. O'Dowd. 1976. Plant defense guilds.
Science 193:24-29.
Cambell, B.C. and S.S. Duffey. 1979. Tomatine and parasitic
wasps: Potential incompatibility of plant antibiosis with
biological control.
Science 205:700-702.
Center, T.D. 1974. A survey of some legume seed-feeding
insects of Northern Arizona with notes on the life histories
of the Bruchidae (Coleoptera).
Unpublished .M.S. Thesis,
Northern Arizona University, Flagstaff, Arizona, 157pp.
Center, T.D. and C.D. Johnson 1974. Coevolution of some seed
beetles (Coleoptera: Bruchidae) and their hosts.
Ecology
55:1096-1103.
Center, T.D. and C.D. Johnson 1976. Host plants and
parasites of some Arizona seed-feeding insects.
Ann.
Entomol. Soc. Amer. 69:195-200.
Connell, J.H. 1980. Diversity and the coevolution of
competitors, or the ghost of competition past.
35:131-138.
Oikos
13
Feeny, R. 1976. Plant apparency and chemical defense.
pp.
1-39, In; J. Wallace and R. Mansell (eds.) Biochemical
interactions between plants and insects.
Recent Adv. in
Phytochem. 10:1-40.
Fenner, F. 1971. Evolution in action: Myxomatosis in the
Australian wild rabbit.
In: A. Kramer (ed.) Topics in the
study of life. The Bio Source Book. New York, Harper and
Row.
Fujii, K. 1983. Resource dependent stability in an
experimental laboratory resource-herbivore-carnivore system.
Res. Popul. Ecol. Suppl. 3:15-26.
Hassell, M.P. 1978. The dynamics of arthropod predator-prey
systems.
Princeton Univ. Press, Princeton, New Jersey.
Haukioja, E. 1980. On the role of plant defenses in the
fluctuation of herbivore populations.
Oikos 35:202-213.
Janzen, D.H. 1969. Seed-eaters versus seed size, number,
dispersal and toxicity.
Ecology 23:1-27.
Janzen, D.H. 1972. Escape in space by Sterculia apetala
seeds from the bug Dysdercus fasciatus in a Costa Rican
deciduous forest. Ecology 53:350-364.
14
Janzen, D.H. 1975. Interactions of seeds and their insect
predators I parasitoids in a tropical deciduous forest. pp.
154-186, In: P. Price (ed.) Evolutionary strategies of
parasitic insects and mites.
Janzen, D.H. 1977. How southern cowpea weevil larvae
(Bruchidae:
Callosobruchus maculatus) die on nonhost seeds.
Ecology 58:921-927.
Janzen, D.H. and P.S. Martin 1981. Neotropical anachronisms:
The fruit the Gomphotheres ate.
Science 215:19-27.
Johnson, C.D. 1981a. Interactions between bruchid
(Coleoptera) feeding guilds and behavioral patterns of the
Leguminosae.
Environ. Entomol. 10:249-253.
Johnson, C.D. 1981b. Host preferences of Stator in non-host
seeds. Environ. Entomol. 10:857-863.
Kistler, R.A. 1979. A simple host-parasitoid system: An
examination of factors contributing to stability.
Unpublished M.S. Thesis, Purdue University, West Lafayette,
Indiana.
Kistler, R.A. 1982. Effects of temperature on six species of
seed beetles (Coleoptera: Bruchidae: an ecological
perspective. Ann. Entomol. Soc.
Amer. 75:266-271.
15
Kistler, R.A. 1985. Host age structure and parasitism in a
laboratory system of two hymenopterous parasitoids and
larvae of Zabrotes subfasciatus (Coleoptera: Bruchidae).
Environ. Entomol.
in press.
Lamprey, H.F. and 0. Halevy. 1974. Interaction between
Acacia bruchid seed beetles and large herbivores. Afr.
Wildl. J. 12:81-85.
Lawton, J.H. 1978. Host plant influences on insect
diversity: the effects of space and time.
L.A. Mound and N. Waloff, (eds.)
pp. 105-125, In:
Diversity of insect
faunas, Oxford, Blackwell Scientific.
Lawton, J.H. and D.R. Strong. ·1981. Community patterns and
competition in foiivorous insects.
Am. Nat.
118:317-338.
Mares, M.A., F.A. Enders, J.M. Kingsolver, J.L. Neff, and
B.B. Simpson.
1977.
plants and animals.
Prosopis as a niche component of
pp. 123-149, In: B.B. Simpson (ed. ).
Mesquite, its biology in two desert ecosystems. Dowden,
Hutchinson and Ross, Stroudsburg, PA.
Morris, R.F. 1969. Approaches to the study of population
dynamics.
pp. 9-28, In: W.E. Waters (ed.) Forest insect
population dynamics, USDA Forest Serv. Res. Paper, NE-125.
Paine, R.T. 1966. Food web complexity and species diversity.
Am. Nat.100:65-75.
16
Pimental, D. 1968. Population regulation and genetic
feedback. Science 159:1432-1437.
Pimental, D., S.A. Levin and D. Olson 1978. Coevolution and
the stability of exploiter-victim systems.
Am. Nat.
112:119-126.
Price, P.W., C.E. Bouton, P. Bross, B.A. McPheron, J.W.
Thompson, and A.E. Weis. 1980. Interactions among three
trophic levels: Influence of plants on interactions between
insect herbivores and natural enemies. Annu. Rev. Ecol.
Syst. 11:41-65.
Rhoades, D.F. 1979. Evolution of plant chemical defense
against herbivores.
Janzen (eds.)
pp. 3-54, In:· G.A. Rosenthal and D.H.
Herbivores, their interaction with secondary
plant metabolites.
Academic Press, New York.
Rhoades D.F. and R.G. Cates. 1976. Toward a general theory
of plant antiherbivore chemistry.
Recent Adv. Phytochem.
10:168-213.
Rosenthal, G.A. 1982. L-Canavanine, a dietary nitrogen
source for the seed predator Caryedes brasilensis
(Bruchidae).
Sctence 217:353-355.
Utida, S. 1957. Cyclic fluctuations of population density
intrinsic to the host-parasite system.
Ecology 38:442-449.
17
Wiens, J.A. 1977. On competition and variable environments.
Amer. Sci. 165:590-597.
Whitham, T.G. and C.N. Slobodchikoff. 1981. Evolution by
individuals, plant-herbivore interaction and mosaics of
genetic variability: the adaptive significance of somatic
mutations in plants.
Oecologia 49:287-292.
CHAPTER 2
Seed Production in Prosopis velutina (Leguminosae):
Variability and the Cost of Reproduction in a Desert
Phreatophyte
18
19
INTRODUCTION
Reproductive output of a plant species may vary
considerably both spatially and temporally.
This within and
between population variation results from a multitude of
factors that influence the plant on both ecological and
evolutionary time scales.
Thus, a major component of
variation in plant populations is a result of past and
present selective forces that have shaped the current gene
pool for each species.
However, evidence for actual genetic
variability is lacking for many plant populations (Willson
1983, Solbrig and Bawa 1975).
Most evidence for variation
in populations comes from studies of phenotypic variation,
for which the adaptive significance is speculative.
Variations in timing of budbreak, leafing, and flowering are
common both between and within species although the adaptive
significance of such variation is at present uncertain
(Lechowicz 1984).
Studies that address reproductive adapatations and
variability are less ambiguous since the adaptive
significance of reproduction is clearer.
The individual
plant or species that places a larger proportion of fit
seeds into the overall seed pool will have more of its genes
represented in future generations.
Each species of plant
has a distinct set of adaptations to achieve maximal
representation in the overall seed pool.
Timing of
reproduction (Augspurger 1981, Janzen 1967), pollination
20
mechanisms (Paige and Whitham 1985, Pyke 1978 ), the number
and size of seed produced (Janzen 1969, Harper et al. 1970),
defense mechanisms (Janzen 1969, Bell 1978) and adaptations
for dispersal (Smith 1975, Janzen and Martin 1981, Janzen
1972) as well as many other factors are all important parts
of a species• reproductive strategy (Willson 1983, Schaffer
and Gadgil 1975).
Within a species, variation in reproduction will have
its greatest significance, for it is with other
conspecifics, with the same general life history that a
given plant must compete most strongly for the same
nutrients and germination sites.
Each individual plant
controls to some extent the quality and quantity of seeds
that it can produce via selective abortion of flowers,
fruits, and ovules, based upon the resources available for
reproduction within that individual (Stephenson 1981).
By
this method a plant can regulate the amount of energy and
nutrients it expends per unit of time to produce an optimal
number of seeds.
The plant may regulate the genetic quality
of those seeds by aborting less fit seeds and flowers in
some selective process and provide more parental care to a
select number of remaining offspring.
For this reason the
numerical aspects of seed production (flower, fruit, and
seed numbers) tend to vary a great deal more than such
factors as seed size, which is constrained by many factors
(Harper et al. 1970, Willson 1983).
21
A plant that is optimal for an examination of the
adaptive significance of variability in reproduction is the
desert phreatophyte Prosopis velutina Wooten (velvet
mesquite).
P. velutina is a woody legume in the subfamily
Mimosoideae, section Algarobia.
It has been extensively
studied because of its status as a pest plant of range lands
in arid habitats such as the desert Southwest (Simpson 1977)
and its food, fuelwood and crop potential for arid lands
(Felker 1979).
Variability in Prosopis is extreme.
Morphologically
there are three distinctly different forms, single
stem~ed,
many stemmed erect and decumbent running bush, all of which
may be found in a single species (Meyer et al. 1971) or even
in the offspring of a single plant (Felker 1979, Felker et
al. 1981).
Budbreak varies within and between populations
(McMillan and Peacock 1964).
Growth rates vary
significantly between populations, species, offspring of the
same plant and even within clones (Felker et al. 1981).
Flowering phenology varies from year to year, dependent
mainly upon temperature, but it also varies significantly
within a population both within and between years
(Glendening and Paulsen 1955).
Fruit and flower production
varies considerably from year to year and from population to
population (Glendening and Paulsen 1955, Meyer et al. 1971,
Dafni and Negbi 1980).
Most populations produce fruits in
alternate years, but even this is highly variable (Felker et
al. 1984).
Genetic variability is high in this
22
self-incompatible, obligately outcrossing genus (Solbrig and
Bawa 1975, Simon 1979).
Pod and seed composition within one
population may vary considerably (e.g., sucrose content of
pods varies from 13-36%; Felker 1979, Werker et al. 1973).
Most seeds
g~rminate
in one to five years but some may still
be viable after 10 years in the soil (Meyer and Bovey 1982,
Tschirley and Martin 1960, Dafni and Negbi 1978).
Some of
this variation in mesquite is thought to be a result of
adaptation to a harsh desert environment, where nitrogen
(Shearer et al. 1983), water (Nilsen et al. 1983) and
temperature (Dafni and Negbi 1980) are all factors limiting
growth and reproduction.
This study examines the seasonal phenology of seed
production and the cost of and variability in pre-predation
and pre-dispersal seed production within and between six
populations of velvet mesquite from 1981 to 1983.
Reproductive costs and outputs were monitored for these
three years in each population in an effort to document the
range and extent of variability within and between these
populations.
A high level of variability could be a result
of adaptations to a variable abiotic environment or could be
an adaptive mechanism to reduce the impact of seed predators
on reproductive output.
This chapter documents the
variability found in these six populations and addresses the
first possibility.
The possible effects of variation on
populations of seed predators are addressed in chapter 3.
23
METHODS
Study Site
The study was conducted from March, 1981 through March,
1984 in the Verde River Valley in central Arizona, USA.
The
Verde Valley consists of upper Sonoran Desert scrub and
desert grassland vegetation (Lowe 1964).
The major plant
species are Prosopis velutina, Acacia greggii Gray, Larrea
tridentata (DC.) Coville and various grasses.
The majority
of the valley has been intensively grazed by cattle.
Six
populations of mesquite were chosen within an 870 km 2 area.
Only discrete populations were chosen and all were isolated
from other populations.
A general description of the six
study sites is presented in Table 2-1.
Study Methods
Initially five trees were selected from each site, but
as the study progressed more trees were selected at most
sites to gain a representative sampling of reproductive
variability at each site.
The height, cover, distance to
the first and second nearest neighbors, amount of leaf
litter, vegetation under and between the trees, and the
distance to the closest surface water source (if any), were
all recorded for each tree.
Each site was visited every 10 to 14 days from April
through November.
The proportion of sample trees with
leaves, flowers, or pods, the phenological state of each
Table 2-1. Descriptive data on the six populations of Prosopis velutina examined in the study. Number of trees is the
number of trees studied at each site, tree density is an estimate of the number of trees per site, and rank population
size ranks the sites by the number of trees per site.
SITE No. LOCATION! LATITUDE ALTITUDE NEAREST
TREES
(m)
RANGE TNSHIP 0 I
TOWN
12 14
5E
34 38 45
1036 McGuireville
TREE SIZE
X ~ SE
58.9±20.3
2
7
14
5E
34 36 50
1021
Montezuma Castle 37.2±22.1
Na.tional
Monument
3
11
13
5E
34 31 00
1006
9.6 km SE of
Camp Verde
4
10
13
5E
34 31 50
991
5
10S2 13
11N 2
4E
34 33 15
6
12
3E
34 47 00
16
TREE RANK
SITE DESCRIPTION
DENSITY POPN MAJOR PLANTS
HABITAT TYPE
#/Ha SIZE
480 3 Prosop1s-veTUtlna
near riparian
Mimosa biuncifera
(Dry Beaver Creek)
Acacia ~reg~i i
ChTTQps1s l1nearis
64
6 Prosopis velutina
Larrea tridentata
dry wash
22.4! 3.1
119
5 Prosopis velutina
Acacia constricta
Chilopsis linearis
near riparian
(West Clear Creek)
8.0 km SE of
Camp Verde
13.6! 6.9
337
2 Prosopis velutina
Larrea tridentata
flood plain
975
3.2 km SW of
Camp Verde
21.4± 4.5
670
1 Prosopis velutina
Chilopsis linearis
dry wash
(Copper Canyon)
1012
4.8 km N of
Clarkdale
127.3~
3.3
158
4 Prosopis velutina
Populus fremontii
Tamarix pentandra
1Location is based on the legal description of the property (Range and Township; E =east).
2N- Northern Population
S- Southern Population
Riparian-roadside
Verde River
N
+:>
25
tree, the number and stage of inflorescences (racemes) per
branch and the number and stage of fruits (a linear legume
pod, 20 em in length) per branch were recorded.
Just prior
to or after pod fall a random sample of 30 pods was
collected from each tree.
These pods were placed in an
environmental chamber at a thermoperiod of 12 h/30°C and 12
h/25°C for 50 days until all seed-infesting insects had
emerged.
Ten pods from each tree were then dissected and
seeds were classified into three groups:
(1) seeds that
appeared to be healthy, (2) seeds that started development
but failed to completely develop, and (3) seeds that showed
no development at all (possibly unfertilized ovules).
The
healthy seeds were weighed to the nearest 0.01 mg after
being oven dried at 60°C for 48 hours.
For all 30 pods of
each sample, pod length, number of seeds per pod, and number
of seeds damaged by herbivorous insects (mainly Hemipterans,
that suck the seed fluids - Smith and Ueckert 1974,
Kingsolver et al. 1977), grazers (that eat the pods and
seeds, e.g., Orthopterans), and ovule and seed predators
(mainly Lepidoptera:Olethreutidae and Coleoptera: Bruchidae)
were recorded.
For the remaining undissected 20 pods of
each sample, seeds were classified via an external
examination of the pods into one of the three seed classes.
Results of this external classification agreed well with the
results of the actual dissections and in some cases results
were pooled.
26
Levels of pod production and the number of seeds in each
seed class were analyzed by one-way analysis of variance and
if significant F-values were obtained, Scheffe's multiple
range test was utilized to pinpoint significantly different
means.
Two- and three-factor ANOVA and multiple regression
were used to attempt to define which parameters were
important determinants of pod and seed production and
pre-predation seed mortality.
RESULTS
The timing of budbreak, flowering and fruiting varied
between sites within one year and varied to some extent
between years within one site, although the overall pattern
usually remained consistent for each population (Fig. 2-1).
Within each site there was considerable asynchrony in the
phenological timing of adjacent trees, which deviated by a
few days or weeks.
This variation in phenological timing
within and between populations and within and between years
can not be readily explained by climatic patterns (Fig.
2-2).
Interaction between temperature and rainfall may
account for some of the apparent differences between years
at each site, but genetic and historical (reproduction in
previous year or years) factors may also be important
determinants of the within and between site variation.
Substantially more inflorescences, flowers and fruits
were produced than matured.
Most trees in this study
27
100
1983
1981
1983
,.,
1981
I
1981
, '\
I
'
.
\.:
I
..
:\
:
\
\
oL--£~~~----~~~~~+----+----~--~--~L----~~2-~--~~--~·~·~~----+---~----~--~
100
3
1983
,,
I
.·"\·'·~
1961
\
' ' ' ,:
\
\
.
\:
\
~
...
\•
;,1
~
"'
,.,..;.
·::~/\., ......
!\
1961
'!
\
\
........
oL-~~--~i--+~.-~·~--~---+----~--+---~L---+--~----~--~~~~~~~~--~~
A
A
M
MONTH
5
0
N
0
A
M
J
A
5
MONTH
Fig. 2-1. Phenology of reproduction in six populat1ons of Prosopis
velut1na over three years. Each curve represents the proportion of
the population (of trees, flowers, or pods) that were in each state
at a given t1me. Arrows indicate the mean bud-break time for the
populat1on. Flowenng -----; I11111ature green pods ------; f·1ature
dry pods ..•••..• ; Pods on the ground-·-·-·-·-·-·
0
N
0
28
30
u
0
~
0
w
2!
~
0::
:::>
§
1~
0::
t::.
20
~
w
Cl..
~
w
0
t::.
0
§
1-
10
0
t::.
§ ~
0
8
~
0
t::.
0
15
0
~
''
' '
'\
I'
''
0
I '
z
I .. ~
1Cl..
0::
Cl..
I
/f
~
u 5
w
~~
0
0
/
zY: '
\~,8""""oi:
I
J
F
M
~
0
'
0
t::.
'
0
t::.
Jt
+
.....,
+
~
+
<t:
0
-1981
1983
fj =1982
0'
'
t::.~ , '
AM
1-
.....,
0
6
',
0
0
'--'
J
0
J
AS
0
N
0
Fig. 2-2. Climatic data for 1981-1983 from the Beaver Creek Ranger
Station near site 1, at Rimrock, Arizona.(data from Vol. 85-87, Climatological Data, Arizona, National Oceanic and Atmospheric Administration!
National Climatic Data Center, Asheville, N.C.). The lower figure
includes total yearly rainfall and cumulative rainfall for April, May,
June, and July. Other data are monthly means.
29
produced hundreds to thousands of inflorescences every year.
A large proportion (21 to 85%) of the immature
inflorescences were aborted before the flowers had opened
(Table 2-2).
After flowering, further inflorescences were
aborted without ever setting fruit.
There was also some
abortion of immature fruits, although this factor was not
measured.
Fruits were not aborted once pod elongation
(pods>5cm in length) had begun, although ovule and seed
abortion still occurred within a pod.
Cost of Reproduction
Since such high levels of abortion of individual
flowers, entire racemes and early fruit must entail some
cost to a plant, samples of immature and mature racemes, and
all stages of pods were collected, weighed, dried, and then
reweighed to determine the relative cost of these
reproductive units in terms of water and biomass investment.
It was clear that the relative cost of a raceme or immature
pods on a raceme was small, whereas once pod elongation had
begun, the parental investment in each fruit increased
dramatically (Fig. 2-3).
The increase in cost for an entire
tree through the immature pod stage was miniscule (54%) when
compared to the 4200% increase in cost if each raceme
produced only 1.5 pods (the mean number of pods per raceme
in this study) (Table 2-3).
Data on Prosopis glandulosa in
Texas indicate that metabolic costs rapidly decrease after
the second week of pod development, when pod elongation
30
Table 2-2.
Early reproductive structures in Prosopis velutina at six sites in 1983.
#
BRANCHES
PER TREE
SITE
TREE
14
15
16
17
18
19
17
34
90
54
28
38
19
22
26
10
33
50
80
+61
+12
160
+15
75
45
90
55
55
40
80
75
30
60
20
nc
35
nc
nc
30
31
40
10
27
5
100
30
55
130
30
40
1
2
3
4
5
6
7
18
51
40
35
35
12
30
+81
80
80
55
50
70
nc
150
60
nc
17
nc
nc
65
58
40
1
1
20
10
50
1
2
3
4
5
6
7
22
31
20
21
28
23
17
125
135
80
+17
+50
15
40
50
60
45
60
15
25
5
35
0
00
0
0
30
60
43
25
11
10
1
10
55
0
nc
nc
nc
nc
nc
nc
0
0
1
0
1
1
0
0
0
0
97
62
15
100
13
15
35
26
65
40
4D
75
10
35
40
20
100
100
98
100
98
99
100
100
100
100
1
2
3
4
6
7
7A
8
9
10
12
40
26
29
20
17
18
20
23
70
60
50
18
60
50
+60
+70
70
60
100
0
0
0
0
nc
125
75
nc
53
0
0
0
0
0
0
1
3
0
1
0
100
100
100
100
100
100
100
100
100
99
8
10
20
24
46
90
40
55
70
25
40
15
nc
nc
nc
nc
0
40
1
0
1
9
10
lOA
11
2
3
4
1
2
3
4
5
6
7
8
9
5
6
# MATURE % IMMATURE % RACEMES!
#
#
IMMATURE FLOWERING PODS
RACEMES NOT SETTING
PER
NOT
MATURE
RACEMES RACEMES
FLOWERING PODS
/BRANCH /BRANCH BRANCH
12
9
13
16
13
8
11
77
20
0
0
0
62
38
50
84
10
97
22
60
0
45
45
0
25
69
28
50
99
98
60
86
0
38
96
74
100
100
100
100
25
96
12
100
100
98
100
100
0?
98
100
nc - data not collected
1Minumum estimate since more than 1 pod is set per raceme (mean= 2.5 pods/spike).
These values were calculated based on lpod/ spike.
0
0
t5+
I
t3
I
0
;
i
~
~
:s:
I
/
I
II
/0/0
1.0
0
I
2
i
i
0.5
01
0
0
0
0
0
0
0
0
1
2
3
t-F L 0 WE RING - I
4
5
6
7
t----PODS--~
Fig. 2-3. Parental investment in terms of biomass and water in various stages of
flowering and fruiting in Prosopis velutina. Flowering stages: 1-very immature
racemes; 2-immature racemes; 3-mature flowering racemes. Pod stages: 4-very
immature pods plus raceme (based on a mean of five pods per raceme); 5-elongate
pods with undeveloped seeds; 6-green mature pods; 7-dry mature pods.
w
.......
Table 2-3.
spikes
per
tree
850
Reproductive costs in tree LMP01 at site 1 in 1983.
mean
flowers
per raceme
racemes
water biomass
188.6+61.4SD 91.97 41.22
% increase in cost -----------------
cost (grams per tree)
immature pods
mature pods
water biomass
water biomass
141.3
62.9
1764.6 2710
54%
53%
1100% 4200%
w
N
33
0
1.6
4
0
2
3
4
5
6
7
WEEKS
Fig. 2-4. Cost of pod production in terms of dark respiration and
biomass of pods in Prosopis glandulosa. Biomass and respiration
both change most rapidly during the first two weeks of pod development.
Associated with these high and rapidly changing costs is a very high
abortion of immature pods. No abortion occurs after these first two
weeks in P. velutina, when costs decrease. (Data from Wilson et al.
1974).
34
begins (Fig. 2-4; Wilson et al. 1974).
Thus, prior to the
second or third week of pod development, very little
parental investment in biomass and water has occurred and
the cost of maintaining the immature pods was greater than
maintenance costs of more mature pods.
Variability in Reproductive Output
The mean number of pods and viable seeds per tree that
were produced by all populations varied significantly
between years and between populations (Table 2-4).
Two-way
analysis of variance of these factors .by year and site, with
tree size as a covariate, indicated that the mean total
number of pods produced per tree was strongly influenced by
size of the tree, by year and by site effects, and that
there was a significant interaction between year and site
(Table 2-5).
While the total number of seeds produced per
tree differed between sites, there was not an overall year
effect, but again there was a strong year by site
interaction.
and year.
In Table 2-6 the data are presented by site
These data explain the strong year by site
interaction mentioned above.
Not all sites showed similar
variation in pod and seed production between years.
Some
sites showed significant variation between years (sites
4,5,6) while others did not (sites 1,2,3).
Much of the
variation between and within sites was explained by tree
size (Fig. 2-5), with larger trees producing more pods and
seeds and thus sites with older, larger trees produced more
Table 2-4. Pod and seed production and abortion in P. velutina. Data are means+standard errors for
six populations averaged over all all three years and for the average of all -six populations for
each year of the study. The same letter after a value indicates a lack of significant difference
within a column.
SITE
MEAN GOOD SEEDS PER
MEAN PODS PER
TREE
1765.:!:_300b
M3
54.1+9.2b
TREE
M3
% OVULES
# OVULES
PER POD
DEVELOP~lENT
COMPLETING
DEVELOPMENT
DEVELOPING
INTO GOOD SEEDS
STARTING
12715.:!:_4206a
308.6.:!:_56.2a
14.9+0.45a
66.4+5.8b
76.6+3.5
49.7+5,2a
2
861+157a
28.5+7.2ab
8305.:!:_2106a
238.7.:!:_59.4a
13.6+0.62a
73.2+5.61ab
66.3+5.5
47.1+6,12a
3
241+62a
18.0.:!:_3.2a
4154.:!:_1053a
189.8.:!:_40,6a
13.6+0.74a
83,4+3.2a
89.8+2.3
67.1.:!:_3.6b
4
318+65a
23.9+5.2a
5503.:!:_1358a
462.9.:!:_114.6a
17.1+0.52b
83.7+4.0a
81.0+4.8
49.9+5,8a
609+144a
44.6+9.3ab
8596+2006a
520.2+115.2a
14.3.:!:_0.62a
89.1+2.1a
82.8+3.5
69.1+3.9b
2773+699b
32.0+7.2ab
47267+12374b 411.2.:!:_94.4a
15.5+0.34ab
90.2+1.7a
90.3+1.5
79.3+2.3b
1981
1620+410a
34.2+6.8a
-
310+67.2
12.6.:!:_0.46a
79.6+2.4a
74.3+1.4a
60.1+3.4a
1982
1639+31la
50.0+7.1b
17776+5806
16837+5411
333+51.5
16.1+0.30b
62.8+4.5b
81. 9.:!:_1.4b
48.4.:!:_4.5b
1983
545+781b
27.2+4.4ab
10502+1491
409+65.7
15.1.:!:_0.34c
91. 5.:!:_1. 3c
82. 7+0. 7b
71.9.:!:_2.3c
6
YEAR
w
tTl
36
Table 2-5. Two-way analysis of variance of (A) the total number of
pods per tree and (B) the total number of good (apparently viable) seeds
per tree by year and by site, with tree size (foliage volume) as a
covariate. All factors were significant for total pods, but total seeds
were related mainly to tree size and population. The year by site interaction in both cases was a result of the high level of asynchrony
between populations in space and over time.
A. TOTAL PODS PER TREE
Sum of
Squares
Covariate
Size
16483
1
16483
72.5 0.000
Between
Treatments
10635
7
1519
6.7 0.000
3960
6566
4848
2
5
9
1980
1313
539
8.7 0.000
5.8 0.000
2.4 0.017
Error
25223
111
227
Total
57190
128
447
Year
Site
Interaction
B.
Degrees of
Freedom
p
Source of
Variation
Mean
Square
F
TOTAL GOOD SEEDS PER TREE
Sum of
Squares
Degrees of
Freedom
Covariate
Size
180029
1
180029
54.7 0.000
Between
Treatments
51231
7
7319
2.2 0.039
855
50269
103619
2
5
8
428
10054
12952
0.1 0.878
3.1 0.013
3.9 0.000
Error
305893
93
3289
Total
640772
109
5879
Year
Site
Interaction
fv1ean
Square
F
p
Source of
Variation
Table 2-6.
YEAR
Pod and seed data for each site by year ( mean~ SE) for 6 populations of Prosopis velutina.
MEAN PODS PER
TREE
MEAN GOOD SEEDS PER
M3
TREE
M3
I OVULES
PER POD
SITE
1981
2200+760
51.9~12.9
22343~12393
1962
2035+363
75.6~22.8
3769~1005
1983
1082+238
36.6+9.8
12095+2712
18.0~4.5
5611+2643
138+53.9
43.6~19.6
7082+3419
268+134.3
14854+5260
370+111.3
:t OVULES
STARTING
DEVELOPMENT
COMPLETING
DEVELOPI·IENT
DEVELOPING
INTO GOOD SEEDS
457.6~102.4
13.7+0.9
83.0~3.0
80.2~4.8
66.4+4.6
99.2~32.3*
16.2+0.7
13.7~3.3*
66.5+9.5
10.6+3.0*
14.9+0.6
85.2+2.0
79.7+3.6
68.3+4.0
12.3+0.7
72.4+6.0
61.5+10.5
47.3+9.8
15.1+0.9
49.1+13.7
64.1+8.0
33.8+10.2
14.0+1.8
83.9+2.5
79.0+5.2
66.6+6.1
10.8~1.1*
65.4~6.1a
92.3~4.8
60.8+7.3
363.5~104
••
SITE 2
1981
704+267
1982
1032~230
1983
84 7+335
23.8~7.5
SITE 3
1981
88+30
1982
394+113
l5.8~3.4
5820+1018
279+59.2
15.9~0.8
72.4~4.7ab
92.0+2.7
67.0+5.8
1983
212+98.8
18.3~5.0
4495+2085
200+58.6
14.6~0.8
85.7~2.3b
85.4~3.7
73.6+5.0
1982
710~111*
55.7~6.3*
6078~1838
17.1~0.7
57.3~6.3
77.8~6.3
45.8+7:2
1983
111~52.2
0.3~0.2*
(4064~1284)
17.2.:~0.2
68.4~10.8
89.1~4.2
60.0!_8.4
1984
212+97.2
15.7~6.1*
11.4+0.9*
81.3+4.6
69.2+6.8*
56.0+6.0a
607.6+218.8
.16.1+0.7
-
76.7+4.5
92.7~2.5
71. 4+5. 5ab
8590+2948ab 718.8+171.2
15.3+0.8
88.8+3.7
86.6+4.8
77.6+6.3b
4.3~0.4*
699+283*
20.3+4.2*
SITE 4
SITE
1981
219+92
8.5~3.8*
1457+766
-
57.9+34.3*
-
1982
1374+316*
55.1~21.4
1983
335+138
57.6+12.0
1981
5149+1168
64.2~19.3*
60856.!_14042
775~245
15.6~0.4
83.9+3.4
90.6+1.6
76.0+3.5
1982
3891+1543
24.2~7.5
62538~25347
341~113
15.8+0.5
87.6+2.5
92.1+1.9
81.0+3.7
1983
996+348*
20.9~9.6
17847+4869
262+140
15.1+0.7
88.3+3.3
89.9+3.4
79.3+4.3
14553+3763b
-
-
SITE 6
*a6~- Different letters or a * indicate a significant differenc~
between years within one site (Scheffe's multiple range test P=0.05).
1- Numbers in parentheses are based on only the trees that produced
pods within .that site in that year.
w
.......
Y=16.7 X+ 317.6
0
R2 = 0.515
0
0
3000
0
2000
0
(./)
0
0
£l..
0
z
0
I
0
0
0
0
1000.l
0
0
oA
6
0
6
~
0
D.
Q
6
606
~Q
6
40
80
TREE SIZE
120
160
(m3l
Fig. 2-5. Relationship of pod production wi~h tree size (foliage volume) in
P. velutina. The symbols represent the six different populations. Site 1 - 0 ;
Site 2 - D ; Site 3 - ~ ; Site 4 - 0; Site 5 - 0 ; Site 6 - 0 . Over 50% of the
variation in pod production is explained by tree size.
w
co
39
pods and seeds.
There was also an apparent alternate year
pod production pattern (Fig. 2-6).
Trees that produced few
pods in 1981 produced a greater number of pods in 1982 and
trees that produced high numbers of pods in 1982 similarly
produced few to no pods in 1983.
A comparison of production
by trees in 1981 and 1983 comes closer to a one to one
correspondence between how many pods each tree produced in
1981 and 1983.
Thus trees that produced high numbers of
pods in a good year (1982) produced few or no pods in the
prior (1981) and succeeding (1983) years, while pod
production in both poor years was equivalent.
Tree size and
alternate year production by individual trees and
populations explains 36 to 58% of the variation in seed and
pod production in Prosopis velutina.
Much of the remaining variation was due to between-tree
variation within a site.
Synchrony of flower, fruit and
seed production was relatively high within each site, but a
few trees at each site either produced every year or were
simply out of synchrony with the majority of the population
and produced large seed crops in "off" years.
All trees at
site 1 (McGuireville) produced pods consistently every year
(although seed abortion rates still cycled on an alternate
year basis).
At site 3 (West Clear Creek) trees 1 and 2
produced heavily in 1980 and 1983 while the rest of the
population had high pod production in 1982 and produced no
pods in 1983.
40
r :.462
p :.005
N=30
5600
4200
~
2800
1400
......
0
1982
r:.404
p:,OI 2
N=31
5600
4200
~ 2800
1400
0
.
1983
r ~.43 7
p =.001
N =51
4200
2800
N
00
2:'
1400 •
..
0
0
1400
2800
4200
5600
1983
Fig, 2-6. Pod product1on in Prosop1s velutina over three years. These
year aga1nst year plots demonstrate the alternate year pod production
pattern for ind1vidual trees. r~ote that in 1981 and 1983, the relationship 1s close to 1:1 and that trees that produced no pods in one
year exhlbited a h1gh pod product1on the following and/or prev1ous
year.
41
The above data indicate some proximal causes for
intersite and interyear variation in fruit and seed
production, but it would be more meaningful to seek the
ultimate causes for these reproductive patterns.
These
ultimate causes appear to be linked to the resource
relations of each individual tree, since other factors such
as rainfall and tree density (i.e., climatic and population
parameters) were poorly related to seed production.
Although tree size was significantly related to pod and seed
production (Fig. 2-5), the relationship was not direct as
might be expected.
Instead, as tree size increased, fewer
pods were produced per unit volume of tree, so that smaller
trees were actually more productive per unit volume (Fig.
2-7).
This indicates a cost involved in the maintenance of
larger tree biomass and a tradeoff in maintenance and
reproductive costs.
There was also a distinct tradeoff between growth and
reproduction, with trees that produced pods rarely producing
any new growth after leafing.
Trees that did not produce
pods would often have branch growth of up to 60 ern.
Finally, these trees showed a distinct inability to
mature either all ovules (assuming fertilization was not
limiting - see discussion) or even to mature all seeds that
began development.
There was a consistent relationship
between reproductive investment and reproductive gain (Fig.
2-8) for most trees.
However, those trees which produced
pods every year, such as those at site 1 in 1982, showed a
•
160
Y= 0.62 X+ 44.42
p <0.05
r =0.2 7
1'0
E
120
0::
w
•
I
a_
l/)
0
0
a_
80
I
z
<(
w
~
40
•
•
,~
I
Ot_
0
.
•
•
•
•
• •
• ••
•• • •
••
• •
••
•
••
• •
•
•
•
•
•
•
•
•
60
•
••
120
180
240
TREE SIZE (m3)
Fig. 2-7. The number of pods produced per unit volume of tree foliage (m3)
as a function of tree size. As tree size increased there was a significant
decrease in the number of pods produced per unit volume of tree foliage.
.j:::>
N
~OBSERVED:•
·
•
•
1200
r2=.872
•
•
r0
E
'800
(./)
0
w
w
(./)
400
I
I
!:J'
.,.
•
•
SITE 1: 82:o
r2=.875
•
'
0
•
0
0
•
100
PODS 1m3
0
200
Fig. 2-8. Reproductive gain (number of good seeds produced) as a function of
reproductive investment (pod production) in P. velutina. Most of the outliers
(open circles) were trees at site 1 in 1982,-where trees produced many pods but
very few seeds matured successfully (these points were excluded from the observed
regression). All points lie below the maximal reproduction expected if all seeds
developed successfully. Regression equations: Exp.-Y=16.8X; Obs.-Y=10.1X; Site 1
1982 - Y=1.22X.
+::>
w
44
much lower benefit in seeds produced for a similar
investment in pod material compared to 1981 and 1983.
This
drop in proportion of good seeds produced did not occur in
the other populations where pod production varied more
between years (Fig. 2-8).
The proportion of ovules that
began development into seeds was ususally lower and more
variable (Tables 2-4,2-6) than was the proportion of these
ovules that completed development into viable seeds.
This
seems to indicate that once a commitment was made by the
parent tree to develop a seed, that the seed had a high
probability of successful development.
Variation in the
proportion of seeds that failed to develop once development
was initiated was most likely due to herbivore damage and
probably was less a result of active abortion by the parent
plant (see chapter 3).
DISCUSSION
This study indicates three aspects of flowering in
Prosopis velutina that may be of evolutionary and adaptive
significance.
First, flowering phenology was more variable
than all other reproductive parameters.
Flowers were
produced by almost every tree in every year but there was a
wide fluctuation within and between populations as to the
number of inflorescences initiated and the timing and length
of the major flowering period.
Flowering was typically
initiated in association with spring budbreak and growth
- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - -
45
after the soil temperature exceeded 18°C (Meyer et al. 1973,
Simpson et al. 1977).
This temperature was reached in
mid-April in 1981, but usually does not occur before
mid-May.
As a result most all populations flowered earlier
in 1981 than in other years.
Site 5 (Copper Canyon) did not
follow this pattern but showed a high consistency of
initiation of flowering in the last half of May over all
three years.
Site 6 (Cottonwood) produced pods much later
in 1981 than all other sites.
Flowering typically lasted
for about 30 days but in several cases extended over a 45
day period.
Reproductive synchrony is the norm for mass-flowering,
obligately-outcrossing, insect-pollinated trees and shrubs.
Flowering out of sequence with the rest of the population or
populations lowers pollinator attraction and constancy,
increases flower and seed predation and increases intraplant
resource competition (Augsperger 1981, Doust and Eaton
1982).
Thus in species like Prosopis velutina, reproductive
consistency should be under intense selection.
This raises
the question as to why synchrony of flowering was so sloppy
in this system.
Synchrony is much tighter in other species
of mesquite which live in much harsher environments (Simpson
et al. 1977).
Variability in flowering needs to be examined
more rigorously to further address this question.
Secondly, the trees in these populations consistently
produced many more flowers than they were physiologically or
structurally able to mature into fruits and seeds.
Such
46
apparently wasteful flower production is common in the
legume subfamily Mimosoideae (Solbrig and Cantina 1975) and
in many other plant groups (Augsberger 1981).
The major
hypotheses dealing with this phenomenon have to do with the
attraction of insect pollinators to ensure adequate
outcrossing (Solbrig and Cantina 1975, Willson 1983, Willson
et al. 1979), thereby increasing associated seed production.
However, such large floral displays may also function to
increase male reproductive success (Sutherland and Delph
1984).
Since pollinators are probably not limiting in
mesquite and pollen viability is high (75% in Prosopis
farcata in Israel - Dafni and Negbi 1980), it is likely that
such large and varied amoun·ts of pollen might increase male
fitness.
Alternately, since a large proportion of flowers
(or racemes) never produce fruit, the plant may select for
certain pollen-ovule combinations (Willson 1983).
Thirdly, there must be a considerable cost involved in
flower production.
In all populations a large number of
racemes were dropped by trees even before flowering.
Although herbivores may account for some of this abortion,
herbivore damage was often absent.
This occured more
commonly in years following a large seed crop the previous
year.
Pre-flowering raceme drop was most prominent in dry,
hot spring weather when rainfall was scarce and nitrogen is
most limiting (Glendening and Paulsen 1955, Shearer et al.
1983).
Thus, the tree must reach some point at which costs
exceed available resources. At this point, pre-flowering
47
racemes, which are relatively cheap (see Table 2-3, Fig.
2-3), are aborted before parental investment costs can
accumulate.
Sometimes a successful reproductive bout is
then attempted later when nutrient reserves have increased
and water is more plentiful.
Supra-annual fruiting patterns, such as those seen in
mesquite in this study, are thought to be a response to
either insect seed predators (Silvertown 1980, Janzen 1969,
Johnson and Slobodchikoff 1979) or to the necessary
accumulation of resources required to produce an optimal
seed crop or both (Stephenson 1981, 1984).
In the first
case, there is a high level of synchrony of seed production
within a population (Sork 1983, Silvertown 1980, DeStephen
1982).
The lack of significant differences for many of the
parameters in Tables 2-4 and 2-6 are an indication of the
extreme lack of synchrony within these mesquite populations.
Trees that produced out of synchrony produced just as many
pods, and viable seeds, while the synchronous portion of the
population produced no fruit at all.
This asynchrony
resulted in_ high levels of inter- and intra-population
variablity in fruit and seed production and in fruit and
seed abortion.
This seems to point to a relative
unimportance of seed predators as selective agents in
mesquite reproductive. strategies (see chapter 3).
At the
same time, it supports the alternative energy limitation
hypothesis, which proposes that each plant must accumulate a
given amount of resources to reproduce.
48
Many potential selective factors may also act against
synchrony.
According to Silvertown (1980), synchrony is not
to be expected in a species with animal dispersed, fleshy
fruits.
Mesquite produces a highly edible nutritious pod
with seeds that are dispersed (and seed germination
improved) mainly by passage through a vertebrate digestive
tract (endochory) (Glendening and Paulsen 1955, Janzen and
Martin 1981, Felker et al. 1984).
Thus any selection for
synchrony might be counterbalanced by selection for the
maintenance of a population of dispersal agents.
production of pods, which
con~ain
The
no or few viable seeds, by
the mesquite trees in this study (especially site 1 in 1982)
might circumvent this problem by providing maintenance of
dispersal agents at a much lower cost (no seed production)·
and yet still allow a relatively high level of synchrony in
seed production in alternate years.
This variation in
itself might also serve to decrease the effects of seed
predators in off-years, by increasing the uncertainty of
finding fruits in any given population or on any given tree,
or even of finding a suitable host seed within any given
pod, where only 1 or 2 seeds out of 15 may be suitable
hosts.
Some of these alternative explanations for
variability in seed production are discussed in chapter 3.
A large number of plants are able to match fruit and
seed number with available resources over an extremely wide
range of environmental conditions.
Thus the production of
flowers every year and the subsequent abortion of flower
49
buds, flowers, racemes, fruits, and ovules and seeds might
represent a bet-hedging strategy for seed production in a
variable and highly unpredictable desert environment
(Stephenson 1981, Stearns 1976, Wilbur et al. 1974).
Evidence for Environmental Limitation in Mesquite
Evidence points to both water and nutrient stress in
several species of mesquite.
In this study there was an
obvious tradeoff between growth and reproduction.
Trees
that produced large numbers of fruits did not grow
significantly.
Turner et al. (1963) also found that radial
growth was depressed during fruiting.
Seed production per
unit volume of tree also decreased significantly as size of
the tree increased.
Mature mesquite trees suffer heavy
mortality in periods of drought (Carter 1964, Judd et al.
1971).
Thus as tree size increases, the cost of maintenance
apparently decreases the amount of energy that can be
allocated to reproduction.
Even the cost of maintenance can
be excessively high under extended stress conditions,
resulting in tree death.
Water stress, which is the major limiting factor in a
desert environment, has been well documented in several
Prosopis species.
In southern Arizona, extensive mesquite
stands cause a 30mm diurnal variation in the water table
(Tremble, 1977).
Severe water stress is common from May to
August in Prosopis glandulosa in the Sonoran Desert in
southern California, even though soil water content at a
50
depth of 5.5 m remains constant (Nilsen et al. 1981, 1983,
1984).
The high levels of evapotranspiration required for
maintenance may cause water to be limiting for other plant
functions such as flowering and pod production (Meyer et al.
1973, Strain 1970).
Even the extensive lateral and deep tap
root systems of Prosopis which allow use of underground
water (Phillips 1963) may not allow a phreatophytic plant
like mesquite to be free of water stress in these harsh
desert environments.
They must use water as it becomes
available and then go into a stage of limited metabolic
activity until more water becomes available (Felker et al.
1980, 1984).
Nutrients are also limiting in many semi-arid,
overgrazed ecosystems common to the desert Southwest (Felker
et al. 1980).
Next to water, nitrogen is probably the next
most important limiting factor in desert ecosystems.
Prosopis species are to some extent free from nitrogen
limitation by their ability to form nodules with nitrogen
fixing bacteria (Felker and Clark 1980, Eskew and Ting
1978).
Thus nitrogen under mesquite trees is often much
higher than in areas surrounding mesquite populations
(Tiedemann and Klemmedson 1973, Virginia et al. 1982).
Much
of this litter and soil nitrogen is unavailable to the trees
because of the low leaching and mineralization rate due to
low rainfall of desert areas (Virginia and Jarrell 1983}.
Studies of the use of nitrogen from soil ·and fixation
(atmospheric nitrogen} indicate a high use of soil nitrogen
51
(not stored or fixed) for spring flower and leaf production,
while the nitrogen used for pod and seed production is
mostly fixed (Shearer et al. 1983).
Therefore Prosopis
species in the desert Southwest may be nitrogen limited in
the spring when rainfall is low and nitrogen is taken mainly
from nitrogen leached to the roots by winter and spring
rainfall, before soil temperatures increase enough to allow
fixation by the associated symbiotic bacteria.
In years
with extremely low spring rainfall, water and nitrogen
limitation may act together to limit both growth and
reproduction in mesquite.
Photosynthetically produced carbohydrates may also
significantly limit growth and reproduction in mesquite.
Photosynthesis by pods and leaves of Prosopis glandulosa in
Texas only produces one-third of the necessary photosynthate
necessary for the growth and energy demands of the
developing fruits alone.
Trees with many developing pods
show a rapid depletion of available stored root
carbohydrates (Wilson et al. 1974).
Further studies have
shown that bud break, flowering and seed formation are all
strongly dependent on stored carbohydrates (Wilson et al.
1975, Fick and Sosebee 1981).
All these studies strongly support the hypothesis that
flower, pod, and seed production is an expensive energy and
nutrient drain on the individual tree and that these factors
play an important role in both the variability in fruit and
seed production in
t·
velutina and in the extensive and
52
variable abortion of flower buds, inflorescences, fruits,
and seeds as well as in the imperfect alternate year seed
production patterns noted in this study.
The high
variability which was prominent fn the mesquite populations
in this study indicates that the highly uncertain
environment may have selected for a bet-hedging strategy in
these plants.
The cost of flower production was relatively
cheap, and so a strategy of producing flowers every year,
and then only maturing as many fruits and seeds as
environmental and resource limitations will allow, could be
optimal. If these limitations are extreme then the tree
might not be able to reproduce at all.
Since environmental
predictability is low in desert ecosystems this might be a
safer strategy than a strictly synchronous alternate year
production strategy.
Conversely, such a strong
environmental-resource role in determining reproductive
stategies in Prosopis velutina would tend to minimize the
role of seed predators as agents of selection on
reproductive processes, and also indicate a relatively
important role for dispersal agents as a selective force on
mesquite reproductive strategies.
53
LITERATURE CITED
Augspurger, C.K. 1981. Reproductive synchrony of a tropical
shrub:
Experimental studies on effects of pollinators and
seed predators on Hybanthus prunifolius (Violaceae}. Ecology
62:775-788.
Bell, E.A. 1978. Toxins in seeds.
Harborne (ed).
pp. 143-161, In: J.B.
Biochemical aspects of plant and animal
coevolution. Academic Press, New York.
Carter, M.G. 1964. Effects of drouth on mesquite. J. Range
Manage. 17:275-276.
Dafni, A. and M. Negbi. 1978. Variability in Prosopis farcta
in Israel:
seed germination as affected by temperature and
salinity. Isr. J. Bot. 27:147-154.
Dafni, A. and M. Negbi. 1980. Variability in Prosopis farcta
in Israel: fertility and seed production in populations from
different habitats. Acta Oecol. Oecol. Plant. 1:335-344.
DeStephen, D. 1982.
Seed production and seed mortality in a
temperate forest shrub (witch hazel, Hamamelis virginiana).
J. Ecol. 70:437-443.
Doust, J.L. and B.W. Eaton. 1982. Demographic aspects of
flower and fruit production in bean plants, Phaseolus
vulgaris L. Amer. J. Bot. 69:1156-1164.
54
Eskew, D.L. and I.P. Ting. 1978.
Nitrogen fixation by
legumes and blue-green algal-lichen crusts in a Colorado
desert environment.
Amer. J. Bot. 65:850-856.
Felker, P.H. 1979. Mesquite: an all-purpose Leguminous arid
land tree.
p. 89-132, In: G. A. Ritchie (ed). New
Agricultural Crops, Westview Press, Boulder, Colorado.
Felker, P. and P.R. Clark. 1980. Nitrogen fixation
(acetylene reduction) and cross inoculation in 12 Prosopis
(mesquite) species. Plant and Soil 57:177-186.
Felker, P., P.R. Clark, J. Osborn, and G.H. Cannell. 1980.
Nitrogen cycling-water use efficiency interactions in
semi-arid ecosystems in relation to management of tree
legumes (Prosopis).
Unpub. mss. presented at International
Symposium on browse in Africa, International Livestock
Center for Africa, Addis Abba, Ethiopia, April 1980.
Felker, P., P.R. Clark, J.F. Osborn, and G.H. Cannell. 1984.
Prosopis pod production-composition of North American, South
American, Hawaiian, and African germ plasm in young
plantations.
Econ. Bot. 38:36-51.
55
Fick, W.H. and R.E. Sosebee. 1981. Translocation and storage
of 14C-labeled total nonstructural carbohydrates in honey
mesquite.
J. Range Manage. 34:205-208.
Glendening, G.E. and H.A. Paulsen. 1955. Reproduction and
establishment of velvet mesquite, as related to invasion of
semidesert grasslands.
U.S. Dept. Agric. Tech. Bull.
1127:1-50.
Harper, J.L., P.H. Lovell, and K.G. Moore. 1970.
The shapes
and sizes of seeds. Annu. Rev. Ecol. Syst. 1:327-356.
Janzen, D.H. 1967. Synchronization of sexual reproduction of
trees within the dry season in Central America. Evolution
21:620-637.
Janzen, D.H. 1969. Seed-eaters versus seed size, number,
toxicity, and dispersal. Evolution 23:1-27.
Janzen, D.H. 1972. Escape in space by Sterculia apetala
seeds from the bug Dysdercus fasciatus in a Costa Rican
deciduous forest. Ecology 53:350-361.
Janzen, D.H. and P.S. Martin. 1981. Neotropical
anachronisms: the fruits the gomphotheres ate. Science
215:19-27.
Johnson, C.D. and C.N. Slobodchikoff. 1979.
Coevolution of
Cassia (Leguminosae) and its seed beetle predators
(Bruchidae). Environ. Entomol. 8:1059-1064.
56
Judd, B. I., J.M. Lauglin, H.R. Guenther and R. Handegarde.
1971.
The lethal decline of mesquite on the Casa Grande
National Monument. Great Basin Nat. 31:153-159.
Kingsolver, J.M., C.D. Johnson, S.A.Swier and ·A. Teran.
1977.
Prosopis fruits as a resource for invertebrates. pp.
108-122, In:
B.B. Simpson (ed). Mesquite, its biology in
two desert scrub ecosystems. Dowden, Hutchinson and Ross,
Stroudsburg, PA.
Lechowicz, M.J. 1984. Why do temperate deciduous trees leaf
out at different times? Adaptation and ecology of forest
communities. Am. Nat. 124:821-842.
Lowe, C.H. 1964. Arizona•s Natural Environment; landscapes
and habitats. Univ. Arizona Press, Tucson, 136 pp.
McMillan, C. and J.T. Peacock. 1964. Bud-bursting in diverse
populations of mesquite (Prosopis:Leguminosae) under uniform
conditions. Southwestern Nat. 9:181-188.
Meyer, R.E. and R.W. Bovey. 1982. Establishment of honey
mesquite and huisache on a native pasture. J. Range Manage.
35:548-550.
Meyer, R.E., R.H. Haas, and C.W. Wendt. 1973. lnteraction of
environmental variables on growth and development of honey
mesquite Bot. Gaz. 134:173-178.
57
Meyer, R.E., H.L. Morton, R.H. Haas, E.D. Robison, and T.E.
Riley. 1971.
Morphology and anatomy of honey mesquite. U.S.
Dept. Agric. Tech. Bull. 1423:1-186.
Nilsen, E.T., P.W. Rundel and M.R. Sharifi. 1981. Summer
water relations of the desert phreatophyte Prosopis
glandulosa in the Sonoran Desert of southern California.
Oecologia 50:271-276.
Nilsen, E.T., M.R. Sharifi, and P.W. Rundel. 1984.
Comparative water relations of phreatophytes in the Sonoran
Desert of California. Ecology 65:767-778.
Nilsen, E.T., M.R. Sharifi, P.W. Rundel, W.M. Jarrell, and
R.A. Virginia. 1983.
Diurnal and seasonal water
re~ations
of the desert phreatophyte, Prosopis g~andulosa (honey
mesquite) in the Sonoran Desert of California. Ecology
64:1381-1393.
Paige, K.N. and T.G. Whitham. 1985. Individual and
population shifts in flower color by scarlet gilia: a
mechanism for pollinator tracking.
Science 227:315-317.
Phillips, W.S. 1963. Depth of roots in soil. Ecology 44:424.
Pyke, G.H. 1978. Optimal foraging in bumble bees and
coevolution with their plants. Oecologia 36:281-291.
58
Schaffer, W.M. and M. Gadgil. 1975. Selection for optimal
life histories in plants.
pp. 142-157, In: M.L. Cody and
J.M. Diamond (eds. ). Ecology and evolution of communities.
Belknap Press, Cambridge, Massachusetts.
Shearer, G., D.H. Kohl, R.A. Virginia, B.A. Bryan,
J.L.Steeters, E.T. Nilsen, M.R. Sharifi and P.W. Rundel.
1983. Estimates of N -fixation from variation in the natural
2
abundance of lSN in Sonoran Desert ecosystems. Oecologia
56:365-373.
Silvertown, J.W. 1980. The evolutionary ecology of mast
seeding in trees. Biol. J. Linn. Soc. 14:235-250.
Simon, J.-P. 1979. Cqmparative serology of a disjunct
species group:
complex.
The Prosopis juliflora - Prosopis chilensis
Aliso 9:483-497.
Simpson, B.B. 1977a. Breeding systems of dominant perennial
plants in two disjunct warm desert ecosystems. Oecologia
27:203-236.
Simpson, B.B. (ed). 1977b. Mesquite, its biology in two
desert scrub ecosystems. Dowden, Hutchinson and Ross,
Stroudsburg, PA.
Simpson, B.B., J.L. Neff, and A.R. Moldenke. 1977. Prosopis
flowers as a resource.
pp. 84-107, In: B.B. Simpson (ed).
Mesquite, its biology in two desert scrub ecosystems.
Dowden, Hutchinson and Ross, Stroudsburg, PA.
59
Smith, C.C. 1975. The coevolution of plants and seed
predators.
(eds).
pp. 53-77, In: L.E. Gilbert and P.H. Raven
Coevolution of Animals and Plants. Univ. Texas
Press, Austin.
Smith, L.L. and D.N. Ueckert. 1974. Influence of insects on
mesquite production. J. Range Manage. 27:61-65.
Solbrig, O.T. and K.S. Bawa. 1975. Isozyme variation in
Prosopis (Leguminosae). J. Arn. Arb. Harvard Univ.
56:398-412.
Solbrig, O.T. and P.O. Cantino. 1975. Reproductive
adaptations in Prosopis (Leguminosae, Mimosoideae). J. Arn.
Arb. Harvard Univ. 56:185-210.
Sork, V.L. 1983. Mast fruiting in hickories and availability
of nuts.
Am. Midl. Nat. 109:81-88.
Stearns, S.C. 1976. Life-history tactics: a review of the
ideas.
Quart. Rev. Biol. 51:3-47.
Stephenson, A.G. 1981. Flower and fruit abortion:
proximate
causes and ultimate functions. Annu. Rev. Ecol. Syst.
12:253-279.
Stephenson, A.G. 1984. The cost of over-initiating fruit.
Am. Midl. Nat. 112:379-386.
60
Strain, B.R. 1970. Field measurements of tissue water
potential and carbon dioxide exchange in the desert shrubs
Prosopis julifera and Larrea divaricata. Photosynthetica
4:118-122.
Sutherland, S. and L.F. Delph. 1984. On the importance of
male fitness in plants: patterns of fruit-set. Ecology
65:1093-1104.
Tiedemann, A.R. and J.O. Klemmedson. 1973. Nutrient
availability in desert grassland soils under mesquite
(Prosopis juliflora) trees and adjacent areas. Soil Sci.
Soc. Amer. Proc. 37:107-111.
Tromble, J.M. 1977. Water requirements for mesquite (Prospis
juliflora).
J. Hydrology 34:171-179.
Tschirley, F.H. and S.C. Martin. 1960. Germination and
longevity of velvet mesquite seed in soil. J. Range Manage.
13:94-97.
Turner, R.M. 1963.
Growth in four species of Sonoran Desert
trees. Ecology 44:760-675.
Virginia, R.A. and W.M. Jarrell.
1983. Soil properties in a
mesquite dominated Sonoran Desert ecosystem. Soil Sci. Soc.
Am. J. 47:138-144.
61
Virginia, R.A., W.M. Jarrell, and E. Franco-Vizcaino. 198l.
Direct measurement of denitrification in a Prosopis
(mesquite) dominated Sonoran Desert ecosystem. Oecologia
53:120-122.
Werker, E., A. Dafni, and M. Negbi. 1973. Variability in
Prosopis farcta in Israel: anatomical features of the seed.
Bot. J. Linn. Soc. 66:223-232.
Wilbur, H.M., D.W. Tinkle and J.P. Collins. 1974.
Environmental certainty, trophic level, and resource
availability in life history evolution.
Am. Nat.
108:805-817.
Willson, M.F. 1983. Plant reproductive ecology. John Wiley
and Sons, New York, 282pp.
Willson, M.F., L.J. Miller and B.J. Rathcke. 1979. Floral
display in Phlox and Geranium: adaptive aspects. Evolution
33:52-63.
Wilson, R.T., B.E. Dahl and D.R. Krieg. 1974.
A
physiological study of developing pods and leaves of honey
mesquite. J. Range Manage. 27:202-203.
Wilson, R.T., B.E. Dahl, and D.R. Krieg. 1975. Carbohydrate
concentrations in honey mesquite roots in relation to
phenological development and reproductive condition. J.
Range Manage. 28:286-288.
CHAPTER 3
Reproductive Strategies in Prosopis velutina (Leguminosae)
and Their Effect on Seed Predation
62
by
Bruchid Beetles
63
INTRODUCTION
Mortality, of flowers, fruits and seeds, caused by
animals has long been thought to play a very important role
in the evolution of reproductive strategies in plants.
Inflorescence and flower structure, numbers and phenology
are strongly influenced by animals
~hat
act as either
pollinators or as predators of pollen, nectar, and
flower-ovule tissues (Willson 1983, Heithaus et al. 1982,
Willson and Price 1977, Willson and Rathcke 1974).
Fruit
herbivores and seed predators have also been hypothesized to
be important selective agents affecting plant population
parameters such as spacing, seedling recruitment, and plant
diversity (Louda 1982, Clark and Clark 1984, Risch 1977,
Vandermeer 1974, Wilson and Janzen 1972, Janzen 1970, 1971),
as well as the timing and extent of seed production (Sork
1983, Silvertown 1980, Janzen 1976, Green and Palmblad
1975).
These predators supposedly also influence the
allocation of resources to reproduction by selecting for
chemical, morphological or numerical defenses of the host
plants (Bradford and Smith 1977, Hare 1980, Janzen 1969,
1983, Mitchell 1977, Moore 1978b) or for mechanisms of
dispersal to escape predation (Janzen 1983, Solbrig and
Cantino 1975).
Plants thus possess a large variety of
population and individual traits that seem to decrease the
effects of predators upon their reproductive output.
64
The relative value of insect seed predators as selective
agents on plants and their reproductive strategies has
rarely been examined in context with other, perhaps more
-important, selective forces acting on plant reproductive
output.
These other factors may either constrain, oppose or
outweigh evolutionary responses of plants to selection by
seed predators.
Such factors may include growth rates, seed
germination, seedling survival, physiological responses to
environmental variables, and nutrient or resource
limitation.
All of these may strongly influence
reproductive strategies.
Willson (1983) and Heithaus et al.
(1982) attempt to place all of these diverse selective
forces into perspective and discuss alternative ways of
dealing with seed production strategies.
Heithaus et al.
(1982) examined multiple mortality factors affecting seed
production in Bauhinia ungulata (Leguminosae) in one of the
few comprehensive studies.
They found that seed predators
were fourth out of seven factors in their importance to seed
and fruit mortality.
Further comprehensive studies are
required to provide more evidence for the selective
importance of seed predators in the evolution of plant
reproductive strategies.
The Bruchidae (Coleoptera) have been repeatedly assumed
to be or have been in the past a potent selective force on
their host plants.
These beetles are obligate seed
predators and are highly host specific, mainly attacking
seeds of plants in the family Leguminosae (Johnson 1981a,
65
Janzen 1980).
Intense coevolutionary interactions have been
hypothesized to have occurred as a result of this highly
specialized seed predation (Center and Johnson 1974, Janzen
1969, Johnson and Slobodchikoff 1979, Johnson 1981b, Johnson
and Kistler 1985, Kistler 1982).
This study addresses two questions dealing with the
relative importance of seed predation by a guild of four
desert bruchids on seeds of velvet mesquite (Prosopis
velutina Wooten), a phreatophytic desert tree or shrub.
The
primary question was whether seed predation by these
bruchids was a significant factor, when examined both by
itself and in relation with other potential selective forces
acting on the reproductive output of mesquite.
A secondary
question was whether reproductive strategies of mesquite
have a negative impact upon bruchid or other seed predators
that might limit the bruchid populations and their evolution
as significant seed predators.
METHODS
The study was conducted in the Verde Valley of central
Arizona, USA, from April, 1981, to December, 1983.
The
Verde Valley is an area of upper Sonoran Desert scrub and
desert grassland (Lowe 1964).
A more detailed description
of the area can be found in chapter 2.
Prosopis velutina ranges in size from a small shrub to a
moderate sized tree and grows mainly along dry washes,
66
adjacent to riparian areas, or in flood plains, where water
is relatively abundant.
Mesquite is a phreatophyte with
root systems often extending 80 meters to reach abundant
sources of ground water.
As a result it can be highly
affected by periods of low rainfall (Carter 1964, Nilsen et
al. 1983, Solbrig and Cantino 1975).
Flowering and fruit
production generally occur in the spring, soon after air
temperatures exceed 67 0 F (Meyer et al. 1971).
self-incompatible (Simpson et al. 1977).
Flowers are
Of the
approximately 150 - 200 flowers that occur on each
inflorescence (raceme), fewer than seven will set fruit and
less than half of these will survive to produce mature
seeds •.
Of the several thousand racemes on any one tree, a
large proportion fail to produce any fruits.
The flowers
are insect pollinated and attract pollinators to the very
rich source of pollen and nectar.
Thus pollination is not
thought to limit fruit set (Simpson et al. 1977).
The fruit
is an indehiscent legume pod with 10-25 ovules per pod.
These pods contain large amounts of sucrose (13-36%) and
thus attract numerous vertebrate dispersal agents which
consume the pods and pass the seeds through the gut,
providing both
dispers~l
away from the parent tree and
increased germination success (Felker 1979, Kingsolver et
al. 1977).
Flowering and fruit set were monitored during 1983.
Each population was visited every two weeks throughout the
season.
The number of racemes per tree was estimated by
-
67
averaging the number on four branches and multiplying by the
number of branches per tree.
In this manner the number of
racemes produced, the number that eventually flowered (>50%
flowering) and the number of pods produced per tree were
recorded.
Seed set and predation were monitored for three years
(1981-1983).
Thirty pods were collected at random from each
tree (5-10 trees/site), at each site, every 7-14 days after
the seeds began to mature in the pods.
Each 30 pod sample
was placed into a one quart mason jar with a paper towel
top, impregnated with 1% Kelthane to prevent infestation by
pyemotid mites.
Emergence of all seed insects was monitored
weekly for 50 days after collection.
All samples collected
from each tree in one year were grouped together to
determine a mean predation rate for each tree in each year.
This mean value should give the most accurate estimate of
the number of seeds that were destroyed ·by the seed
predators, over the entire season, since predation rate
increased as the resource pool was decreased by pod
dispersal.
One sample collected from each tree just prior to or
after pod fall was examined in detail after the 50-day
emergence period.
All 30 pods of each sample were visually
examined and the number of seeds destroyed by Bruchidae,
Lepidoptera, and miscellaneous herbivores was recorded.
The
number of ovules per pod was counted, and each ovule was
classified (based mainly on pod thickness) as showing either
68
no development, some development or completed development
into a mature seed.
A subsample of pods from each site was
dissected and again each seed-ovule was classified into one
of these three classes.
Although there was good agreement
between the visually examined and the dissected samples the
dissection data provided a more accurate estimate of the
stage to which an ovule had developed or the cause of death.
Through a field bioassay, I examined whether there was
evidence of selection by seed predators for synchrony of pod
production within a population.
Site 5 (Copper Canyon)
consisted of two discrete populations with one-half of the
entire population producing pods each year.
In 1983, the
southern population failed to produce any pods (<100 pods
/site), while over 90% of the northern population which is
directly adjacent, produced numerous pods per tree.
To
examine what levels of seed predation might occur in the
seeds of a tree that produced pods out of synchrony with the
rest of the population, five hardware cloth cages (.635 em
mesh) each containing 15 pods from the 1982 crop of tree #4
at site 5, were hung within the canopy of tree #4, a tree in
the middle of the southern (no pod) population, in 1983.
other pods were present within 1 km.
No
These cages were left
in the tree for 30 days and were then collected and the seed
predators reared as described above.
69
RESULTS
Flower Production and Mortality
Some trees failed to initiate flower poduction in some
years, but, on the whole, the majority of trees did initiate
production of inflorescences every year.
Flowering usually
occured in late April to May and was highly synchronous
within a population of trees.
There was, however, a very
wide range of numbers of racemes produced by a tree.
This
number varied between years, even within the same tree.
In
1983, the number of racemes per tree ranged from 80 to 4480
and the number per branch ranged from 10 to 150.
Although
the loss in·potential reproductive output, resulting from
producing fewer than the maximum number of inflorescences
possible every year, may be an important part of the plant•s
reproductive strategy (via conservation of resources for
subsequent reproduction), it was not quantified in this
study.
Once inflorescences had been initiated the chance of a
given raceme actually producing fruits was less than 50%.
The tree often aborted entire racemes even before the
flowering buds had matured and in 1983 up to 100% of all
pre-flowering racemes were aborted from trees at sites 4 and
5, although the
(Table 3-1).
~ite
means only ranged from 21.4 - 85.3%
Some of this abortion may be due to
herbivores, especially curculionid beetles, but a larger
portion seems to be based on resource limitation in the
Table 3-1. The number of inflorescences produced and setting fruit in six populations of Prosopis velutina in 1983.
Values are means of the mean value for each tree.
SITE
DENSITY
#/Ha
X TREE
SIZE
(m3)
MEAN NUMBER
IMMATURE
RACEMES/TREE
MEAN NUMBER ·No. MATURE
FLOWERING RACEMES SETTING
RACEMES/TREE
FRUIT
% RACEMES
LOST BEFORE
FLOWERING
% RACEMES
% FLOWERING
LOST BEFORE RACEMES LOST BEFORE
SETTING FRUIT SETTING FRUIT
480
58.9
1742
1369
768
21.4%
55.9%
43.9%
2
64
37.2
2124
1126
633
47.0%
70.2%
43.8%
3
119
22.4
1741
1163
261
33.2%
85.0%
77.6%
4
337
13.6
464
146
2
68.5%
99.5%
98.6%
5
670
21.4
1918
282
13
85.3%
99.3%
95.4%
6
158
127.3
1974
503
no data
74.5%
no data
no data
......,
0
71
individual parent plant (chapter 2).
Of those
inflorescences that actually flowered, 44-99% failed to set
any fruit.
These values are minimum estimates, since each
raceme produced on the average 1 •. 5 mature fruits and these
values include both the number of racemes dropped without
setting any fruit and the number of immature pods dropped
during the first two weeks of fruit development, when fruit
abortion occured (chapter 2).
Non-predation Ovule and Immature Seed Mortality
Only data from the pods actually dissected were used to
obtain the estimates of ovule mortality.
falls into two classes.
A significant number of ovules
failed to initiate development (95% CI:
ovules).
Such mortality
30.0-35.8% of all
One-way analysis of variance indicates that this
factor varied both between sites (F=20.3; df=5, 825;
P<.OOl), between years within sites (Table 3-2), and even
within one site in the same year (chapter 2).
Most of this
mortality appeared to have no herbivore related cause and
was probably a result of pollination failure or resource
limited ovule abortion by the plant.
A smaller proportion
of ovules (8.89%) failed to mature into viable seeds once
they had begun to develop (95% CI: 8.5-9.9% of all ovules).
A
par~
of this mortality was a result of herbivory which
will be discussed below.
The failure of an ovule to
complete its development was relatively low and constant but
there were still significant differences between sites
(one-way ANOVA: F= 7.57; df=5, 825; P<.OOl).
Table 3-2. Seed mortality in Prosopis velutina in six sites over three years. Values are means. The ~umber of
pods per tree includes trees that produced no pods, in order to give an estimate of overall pod product10n levels
per site. F-values from one-way ANOVA and significance levels are given below the data.
SITE
YEAR
# of PODS ovules 3
per
examined
(dissected) pod
pods 3
per
tree
% SEEDS LOST TO
# SURVIVING SEEDS
% OVULES 1
per
per
lllC.
no
2
4
3
develop. develop. herbivore
moths bruchids
pod
plant
1981
1982
1983
MEAN
228(34)
100{100)
273(40)
13.7
16.2
14.9
14.9
2200
2035
1082
1772
16.9
86.0
11.6
38.2
4.6
3.2
15.1
7.6
1981
1982
1983
MEAN
127(30)
60(60)
150(30)
12.3
15 .1
14.0
13.6
704
1032
847
861
15.9
50.3
13.1
26.4
10.0
15.1
15.3
13.5
1981
1982
1983
MEAN
31(31)
50!50l
181 31
10.8
15.9
14.6
13.6
88
394
212
231
35.5
27.8
U.4
24.9
3.2
5.5
3.6
4.1
6.0
6.0
1981
1982
1983
MEAN
100{100)
90(30)
17.1
17.2
14.1
710
112
411
43.0
43.2
43.1
ll.5
10.1
10.8
0.4
0.4
5
1981
1982
1983
MEAN
74(40)
60(60)
250(40)
11.4
16.1
15.3
14.3
219
1374
335
643
17 .o
23.5
6.8
15.8
6
1981
1982
1983
MEAN
58(28)
80(80)
191(40)
15.6
15.8
15.1
15.5
5149
3891
996
3345
18.5
13.4
14.1
15.3
F
df
1981
-
10.0***
4,512
-
5.4***
4,164
8.7***
4,164
1.2NS
3,343
14.8***
4,512
3.2*
4,37
F
df
1982
-
2.4*
5,444
-
24.9***
5,444
9.0***
5,444
-
5.3***
5,444
23. 9***
5,47
F
1983
-
8.5***
5,1129
-
16 .8***
5,205
3.44**
5,205
22. i***
5,918
13.1***
5,1129
2.7*
5,46
ALL YEARS
-
22.5***
5,2097
-
20.3***
5,825
7.5***
5,825
12.5***
5,1266
19.5***
5,2097
3.9**
5,141
2
3
4
df
F
df
5.4
1.8
7.8
5.0
9.5
0.77
8.7
6.3
8.3
1.1
8.1
5.8
18260
2548
8764
9857
13.7
0.6
13.2
9.2
5.1
1.3
6.1
4.2
6.5
5.0
7.2
6.2
4555
6593
6078
5742
12.5
2.6
8.6
7.9
5.1
5.3
9.8
6.7
4.7
8.5
8.8
7.3
415
4704
1866
2328
-
1.0
10.6
5.8
1.7
5.0
3.4
7.4
5.3
6.4
5583
594
3088
24.9
5.2
7.1
12.4
4.9
1.1
5.9
0.4
4.9
3.7
5.9
7.3
7.1
6.8
4.7
9.3
11.2
8.5
1029
12358
3742
5710
8.5
6.9
7.2
7.5
5.4
3.7
2.9
7.6
4.7
7.9
3.3
11.9
7.7
8.7
11.5
8.9
9.7
44982
57102
8821
36968
2.9
-
2.5
2.7
2.7
-
1.0
1.6
-
-
1.6
-
0.6
1.4
*- P<.05; ** p <.01; *** P< .001;
1
Based on data from dissected pods only. 2 Based on data•from visually observed pods only.
3 Based on total data.
4 Based on emergence data.
'I
N
73
Predation Related Ovule and Seed Mortality
Lepidoptera, Hemiptera, Curculionidae, and Orthoptera
all act as herbivores in mesquite in the Southwest
(Kingsolver et al. 1977, Johnson 1983).
In this study the
curculionids were not apparent as important external feeders
but Hemiptera were locally abundant, with densities up to 10
per pod in 1982, when pods were abundant.
these herbivores were virtually absent.
In 1981 and 1983
These fluid-feeding
insects mainly suck nutrients from the pod and developing
seeds (Kingsolver et al. 1977) and either kill the seed
outright or cause it to be aborted.
Damage by these kinds
of herbivores was indistinguishable from plant initiated
ovule abortion discussed above.
In contrast, chewing
insects leave a distinct record of the number of seeds they
have eaten or caused to be aborted, by the damage done to
the pod structure.
This type of mortality was divided into
that caused by unidentified herbivores and that caused by
Lepidoptera (mainly Olethreutidae: Ofatulena duodecemstriata
(Walsh)).
Unidentified herbivores destroyed up to 84% of
the seeds in some pods but the overall level of damage by
this group was very small (95% CI: 2.06-2.78% of all
ovules).
Unidentified herbivory was greater in 1981 than in
1983 (3.29% vs 2.1%; T=2.87, df=1269, P<.005) and was higher
at site 3 than in all other sites.
Lepidoptera ate pod material, ovules and mature seeds,
but the majority of their damage was to ovules and immature
74
seeds (Table 3-3).
An average of one seed per pod was
destroyed or damaged as a result of feeding by Lepidoptera
(95% CI: 6.22 - 7.11% of all ovules), but damage was
actually quite clumped, with up to a mean maximum of 58.8%
of seeds per pod being destroyed in some pods.
Moth damage
was lower in 1982 (a good pod year) than in 1981 and 1983
(oneway ANOVA: F=74.1; df=2, 2099; P<.001)(Table 3-2).
The largest group of seed predators consisted of a guild
of bruchid beetles which ranked in order of abundance were;
(1) Algarobius prosospis (LeConte), (2) Mimosestes amicus
(Horn), (3) Neltumius arizonensis (Schaeffer), and (4)
Mimosestes protractus (Horn) (chapter 4).
These species
mainly attacked mature or almost mature seeds and all four
species combined, destroyed even fewer seeds than the
Lepidoptera (95% CI: 5.36 - 6.88% of all ovules).
Destruction ranged as high as 88% of the total number of
seeds in a pod, although it was usually much less.
In 1982,
sites 3 and 5 had higher bruchid predation than all the
other sites.
In the poorer pod production years, 1981 and
1983, there were no differences between sites.
Differences
also occurred between years within the same sites (Table
3-2).
Two-way analysis of variance of predation by moths and
bruchids by site and year showed a year effect, site effect
and year-site interaction for bruchids but for moth
predation only the year effect was significant (Table 3-4).
Table 3-3. Stage of ovule or seed attacked by Lepidoptera and Bruchidae in
Prosopis velutina. Values are the percent of insects in each seed class.
MATURING PODS
ovules imm. seeds
Moths
Bruchi ds
MATURE PODS
mature seeds
50.0%
49.0%
1.0%
0.1%
10.5%
89.4%
-...J
U1
76
Tab.le 3-4. Two way analysis of variance of bruchid and moth emergence
by site and year.
A.
BRUCH IDS
p
Source of
Variation
Sum of
.Sguares.
Between
Treatments
19569
7
2795
11.7
0.000
Site
5449
Year
12083
Interaction 10806
5
2
9
1089
6042
1201
4.6
25.3
5.0
0.001
0.000
0.000
Degrees of Mean
Freedom
Sguare
Error
31057
130
239
Total
61433
146
420
B.
F
LEPIDOPTERA
Source of
Variation
Sum of
Squares
Between
Treatments
25.95
7
8.68
16.92
6.66
Site
Year
Interaction
Degrees of
Freedom
Mean
Square
F
p
3.71
2.5
0.018
5
2
9
1. 74
8.46
0.74
1.2
5.8
0.5
0.319
0.004
0.868
Error
190.3
130
1.46
Total
222.88
146
1.53
77
Variation in Seed Production and Predation by Bruchids
Individual trees in the same site or even adjacent to
each other exhibited distinctly different levels of seed
predation.
Three out of six sites showed a significant
correlation of predation with individual tree (Table 3-5).
This variation in attack rate within a population strongly
indicates variation in resource quality between trees even
within the same population.
All the remaining variables with which predation by
bruchids was correlated (Table 3-5) deal with either the
environment (rainfall in April through July, see chapter 4),
or with factors associated with seed quality and the
variability in seed quality within a tree or population.
Bruchid seed predation was correlated with:
(1) the number
of good seeds per pod (r=0.356), (2) the number of ovules
failing to initiate development (r=-0.374), (3) the number
of ovules failing to complete development (r=-0.156), (4)
the percent of ovules failing to start or complete
development (r= -0.458), (5) the number of good seeds per
tree (r=0.189) and (6) the percent of seeds per pod that are
good (apparently viable) (r=0.426).
The main significant
variables deal not with the total number of good seeds per
tree or per site but with the proportion of seeds per pod or
per tree that was good or bad (Fig. 3-1).
There was a very
strong significant positive relationship between the percent
of seeds destroyed by bruchids and the percent of good seeds
78
Table 3-5. Pearson's correlation coefficients of number of bruchids emerging from seed
pods with each factor in six populations of Prosopis velutina.
FACTOR
SITE 1
SITE 2
SITE 3
SITE 4
SITE 5
SITE 6
.104
SITE
YEAR
ALL SITES
-.308
-.404*
-.001
.592*
.037
.224
.090
.592*
.179
.188
.389***
RAINFALL
.586***
.455*
.145
MEAN NEAREST
NEIGHBOR DISTANCE
.023
.111
-.511*
-.290
-.211
-.352
-.131
TREE SIZE
-.051
.240
.150
.370
-.136
.179
.035
PODS/TREE
.008
-.035
.012
-.189
.236
.121
.003
PODS/m3
.058
-.202
-.303
-.667*
.224
-.081
-.099
GOOD SEED/m3
.496**
.119
-.054
.006
.237
-.098
.132
GOOD SEED/TREE
.433**
.222
.012
.237
.202
-.130
.189*
OVULES/POD
.132
-.101
.018
.186
.134
-.188
NO. GOOD SEED/pod
.663***
.334
.249
.465
.022
-.164
-.032
. 356***
NO. SEEDS FAILING
TO COMPLETE DEVEL.
-.084
-.132
-.198
-.163
-.059
-.246
NO. OVULES NOT
DEVELOPING AT ALL
-.456**
-.436*
-.569**
-. 466*
.167
.175
-.374***
.277
.177
.407
-.004
-.285
.307***
-.615*** -.507*
-.612**
-.521*
.011
.041
-.458***
% GOOD SEEDS PER
.594*** .479*
.434*
.520*
-.032
-.082
.426***
TREE
.141
.555**
.492*
.194
.320***
NO.OVULES STARTING
DEVELOPMENT
% OVULES NOT DEVEL.
TO MATURE SEEDS
.561***
- .156*
POD OR PER TREE
.005
.398*
Fig. 3-1. The percent of seeds killed by bruchids in relation to the
total number of good (apparently viable) seeds produced per tree in six
populations of mesquite over a three year period. There was no significant relationship between the total number of good seeds per tree and
the number of those seeds that were killed by bruchids.
~
1.0)
80
per pod (Fig. 3-2), indicating that variability in resource
quality may strongly limit seed predation by bruchid beetles
on mesquite.
To further examine this effect of variation on seed
predator~.
I divided all trees into groups depending upon
seed production (high numbers of pods with a high proportion
of good seeds (good production) versus low number of pods or
with a low proportion of good seeds (bad production)) and
synchrony of pod-seed production (whether pod or seed
production during the previous year was good or bad).
Trees
that produced high numbers of pods and good seeds had a
greater number of seeds killed by bruchids (high = 29.6 +
1.74SE vs low= 19.7 + 3.4; T=2.88, df=141, p<.005).
previous year•s seed production was good, bruchid
If the
~redation
was lower than if the previous year•s pod production was
poor (good = 19.5
~
4.26SE vs poor = 34.7 + 2.47SE
bruchids/30 pods, T=3.04, df=62, P=.003).
This last result
was most likely a result of alternate year production
patterns.
If the previous year was good then the present
year will usually be poor in seed production and seed
predation will also be poor.
To get around this, I further
divided the data into three subgroups.
If the previous
year•s seed production was good and the present year•s
production was also good (two good years in a row), bruchids
destroyed more seeds (25.5
~
4.31) than in the second year
of a good year to bad year sequence (16.2
~
6.11;
T=1.05,df=29,P=.304) but not significantly so.
However, in
.14
0
(./)
0
I
u
.10
0
:::::>
0::
0
0
0
en
>-
0
(I)
0
w
.06
_j
_j
0
:X::
(./)
0
0
w
w
(./) .0 2
0
0
0.2
0.4
0.6
0.8
GOOD SEEDS
Fig. 3-2. The proportion of good seeds produced by a tree was a strong
determinant of the porportion of mesquite seeds that were killed by bruchid
beetles. Bruchids were negatively affected by a low proportion of good
s2e~s per pod on a tr:e. The r:gression equation is: Y = 0.119X - 0.017,
r - 0.585, F(1, 15) - 21.1, P- .001.
co
,_.
82
a bad to good sequence of years, bruchid seed predation was
significantly higher than in a good to bad sequence (34.02 +
2.92 vs 16.2
~
6.11) and non-significantly greater than in a
good-good series of years (Scheffe multiple range test,
P<.05; ANOVA, F= 4.704; df=2, 58; P=.013).
To further determine the effect of alternate year
production strategies of mesquite on bruchid populations, I
placed cages containing mature mesquite pods in a population
in which no pods were present.
The five test cages had
almost four times as many seeds destroyed by bruchids as
either an adjacent population in the same year (cages = 3.95
+ 0.673SE bruchids/pod vs CR north population = 1.17
~
0.096/pod) or the same population in the previous year
(1.081
~
0.153 bruchids/pod in 1982; T=5.83, df=14, P<.001).
Key Factor Analysis: The Relative Influence of Factors on
Seed Survivorship
Eight factors reduced reproductive output of Prosopis
velutina.
Table 3-6 expresses these mortalities as
percentages of the racemes or ovules lost out of those which
survived the previous stage.
The largest measured source of
loss was due to the failure of mature inflorescences to set
fruit (59% of racemes failed to initiate fruit).
Since each
raceme has approximately 188 flowers, a tremendous number of
ovules and potential seeds were lost at this stage.
The
abortion of immature inflorescences was second (49% of all
immature racemes failed to reach flowering stage).
There
may also be a large number of immature pods aborted, but
Table 3-6. Key factor analysis of flower, ovule and seed mortality in six populations of Prosopis velutina
over a three year period.
1983
1982
FACTOR
MEAN1 SLOPE
MORT.
IMMATURE RACEME
DROP
.438 2.73
5.2*
P=.OS
--
MATURE RACEME
DROP
.590 1.40 .981 158.1*
P=.001
IMMATURE POD
ABORTION
. 700
(est.)
-
r2
.638
-
1981
r2
F
-
-
-
-
-
-
-
-
- --
-
-
-
F
MEAN1 SLOPE
MORT.
MEAN OF 1981 - 1983
r2
F
-
-
-
-
-
-
-
-
-
-
-
-
MEAN1 SLOPE
MORT.
r2
F
DENSITY
DEPEND.
-
-
-
No
-
-
-
-
Yes
-
-
-
-
?
.421
2;2 .271
P=.24
1.12
.354
1.6 .085 2.38
P=.29
.097
1.6 No
P=.15
MEAN1 SLOPE
MORT.
NO DEVELOPMENT
OF OVULES
.174 1. 52
.908 39.4* .407 1.20 . 995 807. 0* . 203 0.96
P=.003
P=.001
HERBIVORES
.026 -3.19
.077
MOTHS
.111 4.95
.837 20.5* .039 14.22
P=.Oll
. 744
INCOMPLETE
SEED DEVELOP.
.126 2.69
.591
5.8* .167 4.52
P=.07
.516
4.3
P=.1
.503
.167
0.6
P=.S
.144 2.81
.365
8.6* No
P=.01
BRUCH IDS
.129 2.66
.087
0.4 .066 5.03
P=.57
.038
0.2 .111 -3.15
P=. 7L
.123
0.4 .102 -.172
P=.56
.018
0.3 No
P=.61
1
*
.938 228.0* No
P=.001
0.3
P=.59
11.6* .108 1.32
P=.027
.139
Mean mortality - the number of racemes or ovules lost after the action of all previous mortality factors.
Indicates significant key factors.
CX>
w
84
since sample sizes for this factor were small, it was not
included in the analysis, even though up to 70% of immature
pods (newly formed less than two weeks) may be aborted (see
chapter 2).
Once pods have been formed, seed mortality was
mainly a result of the failure of ovules to initiate
development (27.1% of all ovules), and the incomplete
development of seeds (12.4 % of all zygotes that started
failed to complete development).
The remaining predation
related factors were less important (bruchids 10.2%, moths
8.5%, and herbivores 2.6%).
The relative contribution of each factor to potential
seed mortality in these populations of mesquite was examined
using key factor analysis.
Heithaus et al. (1982) modified
key factor analysis techniques for the examination of
variation in subpopulations in space instead of the usual
analysis of one population through time (Varley et al. 1974,
Podoler and Rogers 1975, Manly 1978).
I used the method of
Heithaus et al. (1982) to examine the relative importance of
reproductive mortality in six populations of mesquite over a
three-year period.
In this analysis, the losses due to
factor k 1 are regressed on total losses K, with different
sites and years all as replicates:
k; = log 10 N(i-1)- loglO N;
(1)
and
K = k1 + k2 + k3 + ••• + kn
where Ni is the number of ovules or racemes present after
85
3
0
~
0 K
2
o·
~k2
~
0~
>-
11-
~
a:
~
ok1
0
/0
/
o---- o-- 0~<>~
....J
<(
0
o~
0
0.1
k3
o-~~
·~:-K•7f_:\
Q
0
~
k7
Bks
~ k4
~
0
3
2
4
5
SITE
Fig. 3-3. Key factor analysis of reproductive mortality in five
populations of Prosopis velutina in 1983. K - total mortality;
k1 - preflowering raceme loss; k2 - post-flowering raceme loss;
k3 - loss due to the failure of ovules to initiate development;
k4 - loss due to predation by Lepidoptera; k5 - loss due to the
failure of seeds to fully deve 1op; k7 - loss due to predation by
four species of bruchids; k6 - losses due to herbivores were very
minor and were not included.
85
.5
0
0
.4
0
~
.3
>-
f_J
0
<(
f-
Q
a:
0
~
0
.2
Q----
~OK
Q
.1
2
3
4
5
6
SITE
Fig. 3-4. Key factor analysis of post-flowering reproductive
mortality in six populations of P. velutina over a three year
period. K - total mortality; k3-- loss due to the failure of
ovules to initiate development; k4 - loss due to predation by
~epidoptera; k5 - loss due to the failure of seeds to fully
develop; k7 - loss due to predation by four species of bruchids.
87
the effects of factor i (Podoler and Rogers 1975). The
analysis was broken into two sections, with flowering based
upon raceme mortality (the functional flower unit) and seed
production based upon the total number of ovules per pod.
A
slope, r2 and F-values are presented for each regression for
all sites 1981 through 1983 and for all years combined
(Table 3-6).
If the F-value for the regression was not
significant the slope that is shown is not significantly
different from zero and there is no reliable relationship
between K and ki.
If the regression F-value is significant
the slopes and r2 values may be used to compare the relative
influence of each factor, with larger slopes indicating a
greater influence of k; on K.
In 1981 there were no clear
key factors, but the incomplete development of ovules was
most significant when examined graphically (4/5 of all
points show a strong linear relationship).
In 1982 and 1983
the failure of ovules to initiate development and predation
by Lepidoptera and in 1983 mature inflorescence abortion
were the major factors explaining variation in reproductive
output among the different years and populations (Fig. 3-3
and 3-4).
DISCUSSION
Fruit and seed production in mesquite populations appear
to be more a result of environmental and resource limitation
than a coevolved interactive system of seeds and seed
88
predators.
In chapter two, I clearly demonstrated that
flower and immature fruit development entails very little
relative investment costs compared to the investment in a
mature fruit with mature seeds, although the greatest cost
per unit time (in terms of water and respiratory
expenditures) is invested during these early flowering and
fruiting stages.
The basic reproductive strategy of
mesquite thus appears to be a type of bet-hedging in which
each tree almost always attempts to reproduce maximally but
then restricts the number of fruits and seeds that it
eventually matures based upon an allocational strategy by
the individual plant.
There is a definite cost involved in
such a strategy (Stephenson 1984) but in mesquite in a harsh
unpredictable desert environment evidently the benefits
outweigh the costs.
The abortion of (1) inflorescences after they have
flowered but before setting fruit, (2) inflorescences prior
to flowering,
(3) newly-formed immature pods, and of (4)
ovules, all of which are the predominant losses in potential
reproductive output in mesquite in this study, thus are
relatively inexpensive in comparison with the potential gain
that might be achieved if conditions for reproduction are
optimal in a given year.
These stages all occur during the
harshest period of the year, between April and July, when
rainfall is minimal and temperatures are extreme.
Trees may
be severely stressed by environmental conditions during the
period of production of flowers, pollen, nectar, and
89
immature fruits.
However, the tree may be constrained to
begin reproduction during this period by even stricter
requirements for seed germination and seedling survival
(Dafni and Negbi 1978, Meyer and Bovey 1982, Scifres and
Brock 1969, 1972, Tschirley and Martin 1960, Ueckert et al.
1979).
While some of this early mortality may be a result of
pollen limitation and herbivory of flowers, inflorescences
and ovules, other studies have indicated that these factors
may be of little significance (Willson 1983, Simpson et al.
1977, Dafni and Negbi 1980).
The abundance of pollinators
on mesquite in this study and the high levels of pollen and
nectar produced by Prosopis velutina (Simpson et al. 1977)
seem to decrease the probability of pollen limitation
playing a major role in reproductive mortality, although
selection for specific pollen-ovule combinations (pollen
quality) is highly likely in a selective abortion process
(Willson 1983, Heithaus et al. 1982).
Flower and ovule
feeding Coleoptera and Thysanoptera were sometimes abundant
on inflorescences in these populations of mesquite but no
'
quantitative measure of the damage caused by these insects
was attempted.
The relative importance of these
flower-feeding insects as a potential cause of flower and
raceme abortion needs further study.
Whatever the causes,
these early losses result in the greatest decrease in
reproductive output.
Therefore, these factors will be the
most likely to influence (or have influenced) the evolution
of reproductive strategies in mesquite.
90
Since Janzen's (1969) seminal paper on the importance of
seed predation as a potential selective force on plant
reproduction, many systems have been examined.
Seed
predators and especially specialists like bruchid beetles,
have been implicated as potent evolutionary forces acting on
plants resulting in a very tight coevolutionary link between
the two trophic levels (i.e., via the Red Queen hypothesis,
Van Valen 1973, Center and Johnson 1974, Green and Palmblad
1975, Hare 1980, Johnson 1981a, Johnson and Slobodchikoff
1979, Moore 1978a, Janzen 1977, 1983, Solbrig and Cantina
1975).
However, the majority of these studies have examined
only seed predation and often only one group of potential
seed predators.
Examination of the data in these studies
shows that seed predation is not consistently the potent
evolutionary selective force that had been hypothesized.
Seed predation levels range from very low (Janzen 1969,
Johnson and Slobodchikoff 1979, C. D. Johnson pers. comm.)
in a majority of systems to as high as 100% in a few cases
(Janzen 1969).
High levels of seed predation need not mean
that seed predators are important agents in plant evolution.
Janzen (1978) hints that other factors might be important
selective agents in plant reproductive strategies but he
still fails to determine the relative importance of bruchid
seed predators in the evolutionary dynamics of the host
plants.
Only one other study (Heithaus et al. 1982) has
intensively examined the multitude of factors that might
influence flower and fruit production in a plant species.
91
They examined five populations of Bauhinia ungulata
(Leguminosae) and found that seed predators were fourth out
of six factors that affected reproductive output.
In sharp contrast to all of these studies the present
study on mesquite intensively examines differential seed
mortality over a three-year period.
Even Heithaus et al.
(1982) was only a one-year study in which they assumed that
relative mortality levels remained constant between years.
This seems unlikely and is certainly not supported by the
data presented in this study.
I have also examined levels
of flower production prior to seed set for one year to
determine relative decreases in potential reproductive
output at each stage of reproduction.(with qualitative data
for two more years).
Herbivorous chewing insects destroyed
only 0.41 to 6.0% of all ovules, seed- and pod-eating
Lepidoptera resulted in the direct or indirect death of 0.42
to 13.2% of all ovules, and the bruchid guild destroyed only
0.77 to 11.9% of all ovules in any population over the three
years of the study.
Thus, although individual trees were
attacked to a greater extent, the overall effect of insect
caused seed mortality within a population appears to be
relatively unimportant.
The results of the key factor analysis indicated that
the relative importance of the ovule-seed mortality factors
varied dynamically from year to year.
In 1981 and 1983,
immature and mature inflorescence abortion was predominant
at some sites, while in 1982 these two factors accounted for
92
a much lower proportionate decrease in reproductive output.
The failure of ovules to develop and mortality caused by
moths were respectively the two most significant key factors
in 1982 and 1983, but in 1981 no factor explained a
significant amount of the variation in mortality among the
populations.
Over all three years seed predation failed to
explain any significant amount of the spatial and temporal
variation in total losses in potential seed production,
while the failure of ovules to initiate or complete
development were significant key factors.
Therefore, at
least in the Verde Valley of central Arizona, bruchid
beetles and probably all seed and pod predators and
herbivores should have_ very little, if any, influence on the
reproductive output of Prosopis velutina.
As potential
evolutionary forces it appears that these insects hold
little or no selective sway over mesquite populations.
Several other studies have shown relatively high levels
of seed destruction by bruchids in mesquite (Glendening and
Paulsen 1955, Kingsolver et al 1977, Johnson 1983).
However, closer examination of either the data or the
collection and rearing techniques used shows that these
studies may have exaggerated the importance of bruchids.
Solbrig and Cantina (1975) examined damage by bruchids in 15
species of Prosopis and found that only a mean of 10.5% of
all ovules were destroyed (range 1-25%), while 17.1% of all
ovules were underdeveloped (range 7- 25%).
Glendening and
Paulsen (1955) have shown that up to 80% of the seeds may be
93
destroyed by bruchids if the pods remained undispersed under
the parent tree, but predation levels were very low (<10% of
all ovules) for over two months after the pods had reached
maturity.
Many or most of the pods of mesquite are
dispersed within this time period and removed from
predation, and so after this time predation rates would only
be expected to rise dramatically because of the smaller
resource pool for bruchids to attack.
Thus, most maximum
estimates of bruchid predation may be a result of this
resource concentration as pods are dispersed.
This is
indicated in the data of Janzen (1969), Solbrig and Cantina
(1975), and Glendening and Paulsen (1955), although in some
cases the loss of major dispersal agents may have increased
the apparent importance of bruchid beetles in contemporary
time to the point where they might be potentially important
selective agents.
The methods used in this study minimized
the effects of dispersal and resource concentration, by
using mean emergence levels of bruchids throughout the
season).
This provided more accurate estimates of the true
population levels of bruchid seed predators.
Therefore, in
reality, most studies of mesquite indicate that bruchid
beetles destroy relatively few seeds and that other factors
may usually be more important than these seed predators.
The variability within and between pods, trees and
populations may, however, have a significant effect upon
bruchid populations.
Bruchid predation shows no density
dependent relationship with the total number of resources
94
within a population, but does show a significant
relationship with measures of resouce quality within a
population (Fig. 3-2).
Also in contrast with other studies
that show an increase in seed predation in years of poor
seed production, due to a numerical response in good years
(DeStephen 1981, 1982, Sork 1983) and a decrease in
predation in years of high seed production (mast species;
Janzen 1976, Silvertown 1980) due to predator satiation,
this study indicates the opposite.
In good years seed
predation is higher than in years of poor seed production.
Similarly, if a tree produces a large number of pods and
seeds two years in a row, the number of seeds destroyed by
bruchids does not increase significantly, indicating a
relatively constant level of bruchid populations.
The low
level of attack in years of poor pod and seed production,
followed by a higher level of attack in years of good pod
and seed production, may indicate that bruchids limit
oviposition in a poor resource year instead of attempting
either to emigrate to another mesquite population or to
waste energy and eggs attempting to locate a few good seeds
in a very heterogenous environment of pods with a low
percent of good seeds.
This strategy correlates well with
life history data presented in a previous paper (Kistler
1982) and in chapter 4.
Some Mimosestes amicus, the second
most abundant member of the bruchid guild on mesquite, will
often not oviposit on pods in the laboratory and as a result
may live for a very long period of time (> 200 days at 35
95
C).
Those that oviposit freely live a much shorter period.
The high levels of bruchids found in a population without
pods, in the cage study and the lack of a difference in seed
and pod predation by Lepidoptera, which act mainly as
herbivores and not obligate seed predators, all support this
idea.
This is, however, only one explanation for the higher
attack rate in good years.
Such a strategy would entail a
physiological cost (decreased reproductive output in second
year bruchids) and a potentially large mortality cost due to
predation (Kingsolver et al. 1977), but would explain the
relative constancy of population levels in mesquite bruchids
in spite of alternate year pod production and widely
separated populations of mesquite.
Another possiblity is
that in good pod years dispersal of seeds and pods takes
longer (satiates dispersal agents) allowing a greater
buildup of bruchid populations.
This, however, fails to
explain why population levels would be higher in a bad to
good year sequence than in a good to good year sequence of
pod production.
Variation in seed quality and variation in seed and pod
production thus seems to strongly limit populations of
bruchids and their potential to act as selective forces on
mesquite reproductive strategies.
Of course these
strategies might be an evolutionary response to intense seed
predation pressure by these bruchids in the evolutionary
history of mesquite.
Janzen (1975,1978) hypothesized that
such is the case in Hymenaea courbaril in Costa Rica, but
96
such ideas cannot be tested and it seems that if bruchid
predation is minor today in the absence of many coevolved
dispersal agents (Janzen and Martin 1982), then the
evolutionary importance of bruchi.ds in the past seems
unlikely.
Perhaps for these reasons we should begin to look
away from seed predators to other factors for an explanation
for many plant reproductive strategies.
Another alternative hypothesis which might explain
levels of seed predation by bruchids is that bruchid
populations are regulated by a third trophic level of
parasitic Hymenoptera.
In the present paper all larval
parasitoids were included as a part of the total bruchid
predation.
However, trichogrammatid (Hymenoptera:
Trichogrammatidae) egg parasites destroyed a large number of
the eggs laid by all members of the bruchid guild (chapter
5).
If parasitoid populations are more adversely affected
by alternate year pod production, this could explain the
differences between seed predation between years of good and
bad pod production.
After a good year, parasitoid
population levels should be higher and so bruchid
populations would be lower in a subsequent poor pod
production year.
Then in a subsequent good pod year bruchid
populations might be released from parasitism due to a poor
parasitoid numerical response the previous poor pod year,
and the resulting seed predation by bruchids would be much
higher.
This possibility is improbable based on data
presented in chapter 5, but there is a strong possibility
97
that these populations of bruchids might be strongly
regulated by parasitoids (Kistler 1979, 1985).
Janzen (1969) and Center and Johnson (1974) describe
numerous traits of the Leguminosae and coadaptations of
their seed predatars that may function to either decrease
the level of bruchid attack on the seeds of a plant or
conversely allow the bruchid seed predators to counter the
plant's anti-seed predator strategies.
Twelve of the 31
traits mentioned by Janzen are found in Prosopis velutina
and four of these 12 traits deal with timing and synchrony
of pod production as methods to decrease bruchid
predators.
~eed
Neither of these papers, or for that matter many
other studies of seed predator-plant interactions, have
actually demonstrated that these are actually coevolved
responses of the two trophic levels as is implied in these
works (for possible exceptions see Bradford and Smith 1977,
Green and Palmblad 1975, Hare 1980, Hare and Futuyma 1978,
Janzen 1975).
However, even in those studies that
demonstrate that seed predators and their hosts might have
evolved coadapted responses to decrease seed predation or
void plant defenses, for the most part they have all failed
to show the importance of seed predation relative to other
potential plant reproductive mortality factors, which might
counter or override evolutionary responses to bruchids by
the host plant.
This study of Prosopis velutina and its
diverse guild of at least five seed predators (four bruchids
and at least one lepidopteran) clearly demonstrates that at
98
least at the present time these seed predators do not exert
a strong selective pressure on plants and their reproductive
strategies.
In these populations of mesquite reproduction
was more strongly influenced by flower abortion (resulting
from pollination processes, herbivores, and environmental
parameters), and ovule abortion (again related to
pollination, environmental or plant resource parameters).
Conversely, evidence is presented that reproductive
strategies of mesquite do negatively affect populations of
bruchids and possibly of their parasitoids as well.
These
data provide evidence that immature fruit and seed abortion
may, in opposition to a statement by Janzen (1983), actually
act as a direct defense.
The plant can lower the intensity
of seed attack by greatly increasing the variability faced
by seed predators in searching for host seeds capable of
supporting the development of these specialized seed
predators.
99
LITERATURE CITED
Bradford, D.F. and C.C. Smith. 1977. Seed predation and seed
number in Scheelea palm fruits. Ecology 58:667-673.
Carter, M.G. 1964. Effects of drouth on mesquite. J. Range.
Manage. 17:275-276.
Clark, D. A. and D. B. Clark. 1984.
Spacing dynamics of a
tropical rain forest tree: evaluation of the Janzen-Cannell
model. Am. Nat.
124:769-788.
Center, T. D. and C. D. Johnson. 1974. Coevolution of some
seed beetles (Coleoptera:Bruchidae) and their hosts.
Ecology 55:1096-1103.
Dafni, A. and M. Negbi. 1978. Variability in Prosopis
farcata in Israel: seed germination as affected by
temperature and salinity.
Isr. J. Bot. 27:147-159.
Dafni, A. and M. Negbi. 1980. Variability in Prosopis
farcata in Israel:
fertility and seed production in
populations from different habitats.
Acta Oecol. Oecol.
Plant. 1:335-344.
DeStephen, D. 1981. Abundance and survival of a
seed-infesting weevil, Pseudanthonomus hamamelidis
(Coleoptera:Curculionidae) on its variable-fruiting host
plant, witch-hazel (Hamamelis virginiana ). Ecol. Entomol.
6:387-396.
100
DeStephen, D. 1982. Seed production and seed mortality in a
temperate forest shrub (witch-hazel, Hamamelis virginiana).
J. Ecol. 70:437-443.
Felker, P. 1979. Mesquite: an all-purpose leguminous arid
land tree.
pp 89-132, In: G.A. Ritchie (ed.) New
Agricultural Crops. AAAS Selected Symposium 38. Westview
Press, Boulder, Colorado.
Glendening, G.E. and H.A. Paulsen, Jr. 1955. Reproduction
and establishment of velvet mesquite as related to invasion
of semidesert grasslands.
U.S. Dept. Agric. Tech. Bull.
1127:1-50.
Green, T.W. and I.G. Palmblad. 1975. Effects of insect seed
predators on Astragalus cibarius and Astragalus utahensis
(leguminosae). Ecology 56:1436-1440.
Hare, J.D. 1980. Variation in fruit size and susceptibility
to seed predation among and within populations of the
cocklebur, Xanthium strumarium l. Oecologia 46:217-222.
Hare, J.D. and D. J. Futuyma. 1978. Different effects of
variation in Xanthium strumarium L. (Compositae) on two
insect seed predators. Oecologia 37:109-120.
Heithaus, E.R., E. Stashko and P.K. Anderson. 1982.
Cumulative effects of plant-animal interactions on seed
production by Bauhinia ungulata, a neotropical legume.
Ecology 63:1294-1302.
101
Janzen, D.H. 1969. Seed-eaters versus seed size, number,
toxicity and dispersal. Evolution 23:1-27.
Janzen, D.H. 1970. Herbivores and the number of tree species
in tropical forests. Am. Nat. 104:501-528.
Janzen, D.H. 1971. Seed predation by animals. Annu. Rev.
Ecol. Syst. 2:465-492.
Janzen, D. H. 1975. Behavior of Hymenaea courbaril when its
predispersal seed predator is absent. Science 189:145-147.
Janzen, D.H. 1976. Why bamboos wait so long to flower. Annu.
Rev. Ecol. Syst. 7:347-391.
Janzen, D. H. 1978. Seeding patterns of tropical trees.
83-128, In:
pp
P.B. Tomlinson and M.G.Zimmermann (eds.).
Tropical Trees as Living Systems, Cambridge Univ. Press, New
York.
Janzen, D.H. 1980. Specificity of seed-attacking beetles in
a Costa Rican deciduous forest. J. Ecology 68:929-952.
Janzen, D.H. 1983. Physiological ecology of fruits and their
seeds.
pp 625 - 655, In: O.L.Lange, P.S.Nobel, C.B. Osmond,
H. Ziegler (eds).
Physiological Plant Ecology III. Springer
Verlag, New York.
Janzen, D.H. and P.S. Martin. 1982. Neotropical
anachronisms: the fruits the gomphotheres ate. Science
215:19-27.
102
Johnson, C.D. 1981a. Seed beetle host specificity and the
systematics of the Leguminosae.
Polhill and P.H. Raven (eds).
Systematics.
pp. 995-1027, In: R.M.
Advances in Legume
Royal Botanic Gardens, Kew.
Johnson, C.D. 1981b. Interaction between bruchid
(Coleoptera) feeding guilds and behavioral patterns of pods
of the Leguminosae.
Environ. Entomol. 10:249-253.
Johnson, C.D. 1983. Handbook on seed insects of Prosopis
species, ecology, control and identification of
seed-infesting insects of New World Prosopis (Leguminosae).
The Food and Agricultural Oranization of the United Nations,
Rome.
Johnson, C.D. and C.N. Slobodchikoff. 1979. Coevolution of
Cassia (Leguminosae) and its seed beetle predators
(Bruchidae). Environ. Entomol. 8:1059-1064.
Johnson, C.D. and R.A. Kistler. 1985. Nutritional ecology of
Bruchid beetles, In: F. Slansky and J.G. Rodriguez (eds).
Nutritional Ecology of Insects, Mites and Spiders, John
Wiley and Sons, New York, accepted.
Kingsolver, J. M., C.D. Johnson, S.R. Swier and A. Teran.
1977.
Prosopis fruits as a resource for invertebrates.
109-122, In:
pp.
B.B. Simpson (ed. ). Mesquite: its biology in
two desert scrub ecosystems, Dowden, Hutchinson and Ross,
Stroudsburg, Pennsylvania, USA.
103
Kistler, R.A. 1979. A simple host-parasitoid system: an
examination of factors contributing to stability. M.S.
thesis, Purdue University, West Lafayette, Indiana, USA.
Kistler, R.A. 1982.
Effects of temperature on six species
of seed beetles (Coleoptera:Bruchidae): an ecological
perspective. Ann. Entomol. Soc. Amer. 75:266-271.
Kistler, R.A. 1985. Host age structure and parasitism in a
laboratory system of two hymenopterous parasitoids and
larvae of Zabrotes subfasciatus (Coleoptera:Bruchidae).
Environ. Entomol. in press.
Louda, S.M. 1982. Distribution Ecology: variation in plant
recruitment over a gradient irr relation to insect seed
predation. Ecol. Monogr. 52:25-41.
Lowe, C.H. Arizona's Natural Environment; landscapes and
habitats, University of Arizona Press, Tucson.
Manly, B.F.J. 1978. The determination of key factors from
life table data. Oecologia 31:111-117.
Meyer, R.E. and R.W. Bovey 1982. Establishment of honey
mesquite and huisache on a native pasture. J. Range. Manage.
35:548-550.
Meyer, R.E., H.L. Morton, R.H. Haas, E.D. Robison, and T.E.
Riley.
1971. Morphology and anatomy of honey mesquite. U.S.
Dept. Agric. Tech. Bull. 1423.
104
Mitchell, R. 1977. Bruchid beetles and seed packaging by
Palo Verde. Ecology 58: 644-651.
Moore, L.R. 1978a. Seed predation in the legume, Crotalaria
I.
Intensity and variability of seed predation in native
and introduced populations of C. pallida Ait. Oecologia
24:185-202.
Moore, L.R. 1978b. Seed predation in the legume Crotalaria
II.
Correlates of interplant variability in predation
intensity~
Oecologia 24:203-223.
Nilsen, E.T., M.R. Sharifi, P.W. Rundel, W.M. Jarrell and
R.A. Virginia. 1983.
Diurnal and seasonal water relations
of the desert phreatophyte Prosopis glandulosa (honey
mesquite) in the Sonoran Desert of California. Ecology
64:1381-1393.
Podoler, H, and D. Rogers. 1975. A new method for the
identification of key factors from life table data.
J.
Anim. Ecology 44:85-114.
Risch, S. 1977. Effect of relative isolation of hollyhocks
(Althaea rosea) on seed predation by a curculionid beetle
(Apion longirostre) (Coleoptera:Curculionidae). J. Kansas
Entomol. Soc. 50:149-156.
Scifres, C.J. and J.H. Brock. 1969. Moisture-temperature
interactions in germination and early seedling development
of mesquite. J. Range. Manage. 22:334-337.
105
Scifres, C.J. and J. H. Brock. 1972. Emergence of honey
mesquite seedlings relative to planting depth and soil
temperature. J. Range. Manage. 25:217-219.
Silvertown, J.W. 1980. The evolutionary ecology of mast
seeding trees. Biol. J. Linn. Soc. 14:235-250.
Simpson, B.B., J.L. Neff, and A.R. Moldenke. 1977. Prosopis
flowers as a resource. pp. 84-107, In:
B.B. Simpson (ed. ).
Mesquite: its biology in two desert ecosystems, Dowden,
Hutchinson and Ross, Stroudsburg ,Pa.
Solbrig, O.T. and P.D. Cantina. 1975. Reproductive
adaptations in Pr.osopis (Leguminosae,Mimosoideae) J. Arnold
Arb. Harvard University. 56:185-210.
Sork, V.L. 1983.
Mast-fruiting in hickories and availability of nuts.
Am.
Midl. Nat. 109:81-88.
Stephenson, A.G. 1981. Flower and fruit abortion:
proximate
causes and ultimate functions. Annu. Rev. Ecol. Syst.
12:253-279.
Stephenson, A.G. 1984. The cost of over-initiating fruit.
Am. Midl. Nat. 112:379-386.
Tschirley, F.H. and S.C. Martin. 1960. Germination and
longevity of velvet mesquite seed in soil. J. Range Manage.
13:94-97.
106
Ueckert, D.N., L.L. Smith and B.L. Allen. 1979.
Emergence
and survival of honey mesquite seedlings in several soils in
West Texas. J. Range Manage. 32:284-287.
Vandermeer, J.H. 1974. Relative isolation and seed predation
in Calliandra grandiflora, a mimosaceous legume from the
highlands of Guatemala. Biotropica 6:267-268.
Van Valen, L. 1973. A new evolutionary law. Evol. Theory.
1:1-30.
Varley, G.C., G.R. Gradwell and M.P. Hassell. 1974.
Insect
Population Ecology, an analytical approach, Univ. Calif.
Press Berkley, California, 212pp.
Willson, M.F. 1983. Plant reproductive ecology, John Wiley
and Sons, New York, 282pp.
Willson, M.F. and P.W. Price. 1977. The evolution of
inflorescence size in Asclepias (Asclepiadaceae). Evolution
31:495-511.
~illson,
M.F. and B.J. Rathcke. 1974. Adaptive design of
floral display in Asclepias syriaca L. Am. Midl. Nat.
92:47-57.
Wilson, D.E. and D.H. Janzen. 1972. Predation on Scheelea
palm seeds by bruchid beetles: seed density and distance
from the parent palm. Ecology 53:954-959.
CHAPTER 4
The Effect of Temperature on Mesquite Bruchids (Coleoptera):
Physiological
~trategies
of a Guild of Seed Predators
107
108
INTRODUCTION
The recent deemphasis of competition as an important
organizing factor in ecological communities (Lawton and
Strong 1981, Simberloff and Connor 1981, Wiens 1977) has
prompted ecologists to search for alternative factors that
may play a role in community organization.
overlap is common in insect communities.
High resource
However, insects
are small and short lived, highly sensitive to spatial and
temporal variation, and their populations are rarely at
equilibrium.
Thus, competition is less likely to
~e
an
effective selective force in these communities (Rathcke
1976).
Studies of community interactions indicate temperature
and other major abiotic variables to be very important
factors in insect community interactions.
Two coexisting
populations of featherwing beetles (Ptinella) in Southern
England are distinguished mainly by differential temperature
adaptations, due not to competitive niche separation but to
evolution in different environments (Taylor 1980).
The
outcome of competition between two species of Tribolium can
be reversed by changing temperature and humidity conditions
(Park 1954).
Two species of stored product Bruchidae are
similar, in that competitive extinction of two species of
Callosobruchus is determined by ambient temperature (Fujii
1967).
Eggs of two species of Bruchidae, Mimosestes amicus
(Horn) and Stator limbatus( .Horn), which attack seeds of
109
Cercidium floridum Bentham (Leguminosae), are adversely
affected by environmental stresses.
Abiotic factors may be
strong determinants of oviposition strategies in these two
beetles (Mitchell 1977).
In a community of water striders
(Gerridae) the differential effects of temperature influence
the community through effects on developmental rates and
fecundities of the component species (Spence et al. 1980).
Microgeographic races of a coastal dune beetle, Coelus
ciliatus (Tenebrionidae), differ in temperature preferences,
population density and body size due to adaptation to
different environmental regimes (Doyen and Slobodchikoff
1984).
Temperature relations of four species of Stator
(Bruchidae) closely correspond to the feeding guild (Johnson
1981b) to which each species belongs (Kistler 1982).
These
and other studies implicate the importance of temperature to
insect populations (Clarke 1967, Mutchmor 1967, Bursell
1964, May 1979, Keister and Buck 1974).
All these studies
suggest that insect community dynamics might be strongly
regulated by the abiotic environment, limiting the potential
for inter- and intra-species interactions and perhaps even
limiting coevolution with host plants.
Thus niche
differences between sympatric species sharing the same·
resource might be due, in large part, to different
evolutionary responses to physical differences in the
environment.
Four species of seed beetles (Coleoptera:Bruchidae)
Algarobius prosopis (LeConte), Mimosestes amicus (Horn),
110
Mimosestes protractus (Horn) and Neltumius arizonensis
(Schaeffer) attack the seeds of mesquite, Prosopis velutina
Wooten in Arizona.
Three of these species feed only on the
seeds oft. velutina,
hosts.
~·
while~·
amicus uses several alternate
prosopis is the most abundant species and has
been hypothesized to have been the selective agent (via
competitive interactions) responsible for the observed
community structure.
The other species have been selected
for temporal or spatial displacement in order to coexist
with this dominant species (Swier 1974, Kingsolver et al.
1977, Pfaffenberger and Johnson 1976).
The objectives of this study were to assess the degree
of similarity of the physiological responses to temperature
variation which, since these are desert-adapted populations,
may potentially play an important part in the population
dynamics and coexistence of this guild of seed predators.
Since these four species feed on the same resource at
roughly the same times and have comparable ranges, they
could be expected to have very similar physiological
capabilities, with regard to body size, water relations,
host utilization efficiencies, fecundity, and responses to
temperature.
Temperature was singled out as an important
variable because it is the most variable and prominent
factor in desert ecosystems and other parameters (i.e.,
water) are an inherent part of the bruchid-seed self
contained ecosystem.
utilization.
Selection should be for optimal host
Differences could be attributed to
111
differential adaptation (divergent evolution) to a similar
environment based on genetic, ecological and evolutionary
constraints in each species and need not be due to
competitive divergence.
The questions being addressed are;
(1) Are these bruchids limited by the abiotic environment?
(2) If so, are there differences in the responses of these
four species to environmental variables which might explain
their abundances and differential host utilization patterns?
These questions will be assessed by examining the
comparative physiological ecology of the mesquite bruchid
guild and the resulting evolutionary strategies of the
member bruchid species.
Bruchid beetles are highly specialized seed predators
attacking seeds mainly in the family Leguminosae (Johnson
198la).
The species in the mesquite guild attack mesquite
seeds which are contained inside a woody indehiscent pod.
~·
amicus, N. arizonensis and M.protractus females attach
their eggs individually to the pod surface, while A.
prosopis oviposits either in damaged areas, cracks or
crevices on the pod, or in the exit holes formed by either
other bruchids or by pod and seed feeding Lepidoptera
(Kunhikannan 1923, chapter 5).
The larvae of the former
species burrow into a seed directly below the egg, while
larvae
of~·
prosopis possess well developed legs and may
travel either over the surface of the pod or through the
intra-pod matrix to choose a host seed (Pfaffenberger and
Johnson 1976).
After boring into the seed, the larvae pass
112
through about 5 instars (Wightman 1978b), pupate in the
seed, and emerge as a mature adult from the seed.
The
adults probably feed on pollen and nectar of mesquite and
other plants (Kingsolver et al. 1977, Johnson and Kistler
1985).
All species
in mature pods.
except~·
~·
protractus mainly attack seeds
protractus is morphologically
specialized for attacking green-immature pods.
Larval
thoracic appendages are replaced by decurved spines to aid
in entering the soft pods without impeding movement in the
sappy pulp of the immature pod (Pfaffenberger and Johnson
1976).
M. protractus is an aberrant member of its genus.
It is the only member of the Protractus group, and feeds
only on two species of Prosopis (Kingsolver and Johnson
1978). This species is the rarest member of the guild but
may be locally abundant (Conway 1980).
N. arizonensis ·is the second rarest member of the guild.
This genus does not appear to be related to any of the other
recognized species groupings in the new world.
It is
restricted to the Sonoran Desert of the United States and
Mexico, and is a specialist on Prosopis species (Kingsolver
1964, Johnson 1978).
M. amicus is the second most abundant member of the
guild.
It is a member of the Mimosae group of Mimosestes,
which is probably the youngest and most actively evolving
group within the genus.
It is the only generalist in the
guild and feeds on a variety of seeds, mainly species of
113
Acacia, Cercidium, and Prosopis (Kingsolver and Johnson
1978).
A·
prosopis is the most abundant member of the mesquite
bruchid guild.
Its oviposition behavior and its mobile
first instar set it aside from the other three species in
the guild.
These traits and larval characteristics are
similar to those found in the closely related genus
Acanthoscelides (Pfaffenberger and Johnson 1976).
Because
these traits are found in several closely related genera,
they are probably not specific adaptations to the Prosopis
ecosystem, although they might very well be pre-adapatations
to successful utilization of Prosopis as a resource.
METHODS
Field Studies
Bruchid populations were studied in a population of
mesquite near McGuireville in the Verde Valley, in central
Arizona.
This population is relatively undisturbed and
cattle have not been present during the study period.
Ten
trees were monitored every 7 to 14 days from May, 1981,
through October, 1983, and the phenological state of each
tree was recorded.
After initiation of pod development a 30
pod sample (approximately 450 seeds) was collected at random
from each tree every 7 to 14 days.
These samples
wer~
placed in quart mason jars with paper towel lids and reared
in a laboratory culture room at a thermoperiod of 30°
114
C-12h/25°C-12h.
All insects that emerged from these pods
were removed and counted every 7 days for 50 days.
Laboratory Studies
All four species were reared from pods of
f.
velutina
collected in the Verde Valley, and with the exception of M.
protractus were reared for at least one generation in the
laboratory at a thermoperiod of 30°C/25°C on pods from the
same tree, to avoid all acclimation responses and host seed
differences.
li· protractus will not breed in the laboratory
and so reared adults were maintained on a 10% solution of
sucrose for approximately 30 days prior to the experiment.
Temperature ranges were chosen for the experiments based
upon climatological data from the Beaver Creek Ranger
Station at Rimrock, Yavapai County, Arizona, and from
surface and internal temperature measurements of pods using
a Bailey thermoprobe.
The oxygen consumption of adults of all four species and
larvae of all but li· protractus, was measured with a
20-station Gilson differential respirometer, using the
method described by Kistler (1982).
Ten adults (5 forM.
protractus) less than 24 hours old, or approximately 15
larvae (23 days old, 1 larva/seed) in their host seeds were
placed in 15-ml respirometer flasks.
The larvae were all
tested in one experiment and all adults were tested in a
second experiment.
Respiration (oxygen consumption) was
measured at temperatures of 20 to 50°C in 5-degree
115
intervals.
Four replicates were used for each species for
adults and 5 for the larval trials.
Four control flasks
were used, consisting of 15 uninfested host seeds per flask
for the larval trials or four empty flasks for the adult
trials.
After the experiments, the adults and the larvae
inside the seeds were dried for 48 hours at 60°C.
The
larvae were then dissected out of the seeds and dried for
another 48 hours, prior to weighing.
Oxygen consumption was
calculated at STPD (0°C, 760mmHg, dry gas) in microliters of
oxygen per milligram dry weight per hour.
Adult fecundity was determined at four temperatures: 20,
25, 30, and 35°C.
Virgin pairs (male and female) were
placed in quart or pint jars, with paper towel tops treated
with 1% Kelthane to protect against pyemotid mite
infestation, along with 20 mesquite pods and a piece of
sponge soaked in a 10% sucrose solution.
These cultures
were placed into environmental chambers maintained at the
given temperature and at a humidity of approximately 70%.
Pods were replaced and the eggs were counted weekly.
Because of the secretive oviposition behavior of A.
prosopis, counting eggs of this species was unreliable and
so the number of emerging adults was used as the only
available estimate of fecundity.
Since larval survival was
relatively high for all species this should be an accurate
estimate of fecundity.
After each week the egg-containing
pods were placed at 30°C to facilitate larval development.
Four or more replicates were used for each species at each
116
temperature.
Longevity was also recorded for each beetle
used in these experiments.
Developmental rates were determined by placing 20 pairs
of adults on 30 pods for 3 days at 30°C.
Two replicates for
each species were then placed at each temperature (20, 25,
0
30, 35 C).
The emergence of adults was then monitored daily
to achieve an estimate of rate and pattern of emergence.
Larval survivorship was also estimated from these
experiments.
Since all replicates were identical and
assigned randomly to each temperature group, the total
number emerged at each temperature was divided by the
maximum number emerged at any temperature to give a relative
estimate of larval mortality at each temperature.
Thirty virgin adults
(~5
of each sex) and 30 eggs less
than 48 hours old, of each species, were weighed, dried at
60°C for 48 hours, and then reweighed on a Cahn
electrobalance to determine weight and water content
differences between species.
All data were subjected to one-way analysis of variance
across temperatures for each species and across species for
each temperature.
Pairwise contrasts and orthogonal
contrasts (Scheffe and LSD) were used where appropriate to
examine group means.
117
RESULTS
The phenological timing of the trees and the bruchid
species, and the climatological data are shown in Fig. 4-1.
The peak of oviposition (left arrow)
for~·
protractus
clearly indicates strong utilization of green pods.
This
species is most active during the hottest and driest part of
the season and drops out as green pods become unavailable.
The oviposition (center arrow) and emergence peaks
for~·
prosopis and M. amicus are almost totally overlapping and
coincide with the peak in mature pod (pods containing mature
seeds) numbers.
The curve for
~·
prosopis is broader,
indicating a broad seasonal activity and resource use.
Most
of these first three species emerge prior to pod fall.
N.
arizonensis appears to prefer to oviposit on dry (right
arrow), mature pods and thus occurs later in the season than
all the other species.
Temperature and moisture stress have
decreased by late summer when this species is actively
ovipositing and developing.
The phenological timing of two
of the four species is thus distinctly different.
During these three years, the relative abundance of the
four species remained relatively constant (Table 4-1).
absolute abundances,
1982.
howe~er,
The
were drastically reduced in
This was due to a small proportion of viable seeds
being produced (chapters 2, 3), and resulted in the
disappearance of the two rare species (Table 4-2).
These
data not only clearly indicate the numerical dominance of A.
0-0
A
~MA
30
I
\
I
\
I
\
I
\
oro~i~
·a.
I
w
~20
w
t9
0::
w
~ 10
w
l
l
~
\0
\6, \
AP 1/'o-o
o'-'\o
~~,
I
6~
01
1
/6o----- n - -
'
___
o~
~o
~~ooi
FLR
_,
8
I
/
I
5
/
c
,'
'
DRY
'
•
'
I
;;_52
~0
GREEN
/
0
\
'--
I
------,'
I
1-..
I
I
'
I
3
',
' "-
I
/
15
/
""
"
""
I
I
........ "
M
J
J
"
I
\
I
\ I
I
0
A
,/
", .... ,, /
I
zu~:=~-~--f,.......~~~~~
s
---
'
',
I
I
0
GRD
25
-
\
--@.:-=-::@
',·6~
I
'
//
0
o ~bNA
I
'
I
' .... --- .... '
',
0
A
0
N
D
J
Fig. 4-1. The temporal patterns of (A) emergence of the four species of bruchids, (B) phenology of reproducUon
in Prosopis velutina, and (C) temperature and rainfall patterns for the study site (Beaver Creek Ranger Station,
National Oceanic and Atmospheric Administration, Asheville, N.C.). All figures represent means of three years
of data. See text for explanation.
t-•
1--'
OJ
Table 4-1. Relative abundance of bruchids in the mesquite seed predator guild.
The ratio of the abundances as well as the percentofeach species in the total
bruchid population are given.
YEAR
RATIO
PERCENT
A. prbsopi s !1_. amuu-s !!_.- arTzonens1 s M.-protractus AP:NA:NA:MP
1981
91.2%
7.2%
1.01%
0.60%
1982
91.6
8.4
0
0
1983
91.4
7.14
0.50
0.94
238:18:4:1
AP:MA
12.8:1
11.0:1
183:14:1:2
12.8:1
~
~
\.0
-
.
Table 4-2. Numbers of bruchids emerged from 30-pod samples of Prosopis velutina
over a three year period.
DATE
VI-24-81
VII- 7-81
VII-22-81
VIII-3 -81
VIII-12-81
VIII-21-81
IX- 4-81
IX-16-81
IX-26-81
X-10-81
VIII- 3-82
VIII-18-82
VIII-26-82
IX- 1-82
IX-16-82
IX-30-82
X-14-82
X-28-82
XI-20-82
VII-30-83
VI II -13-83
VIII-22-83
IX- 1-83
IX-13-83
IX-22-83
X- 3-83
X-17-83
A. prosopi s
MEAN SD
0
4.8
19.2
34.0
24.2
27.0
35.1
33
77.5
20
1
0.5
0
1.44
5.4
4.17
2,75
3.78
5.25
15.7
48.8
33.7
34.6
31.4
40.8
36.9
50.6
6.9
9.6
20.0
10.7
14.5
22.0
57.6
0.7
1,42
5.6
3.83
2.76
2.95
3.40
9.5
22.0
23.0
23.6
13.6
22.3
15.8
25.0
M. amicus
MEAN
SD
N.arizonensis
MEAN SD
0
0
1.1
1.4
4.5 10.8
2.8 3.4
2.6
3.0
2.1
3.1
1
1.5 1.0
4
0
0
0
0.07
0.10
0.33
1.12
1
2.5
8
0
0.5 0.7
0
0
0.26 0.44
0
0
0.33 0.50
0
0
0
0
0
0
0
0
0
0
0
2.25
0.45
2.79
1.94
1.87
1.60
2.50
0
0.5
0
0
0.01
0.13
0.30
0.38
0.96
0.69
4.20
2.10
1. 50
1.60
1.80
0.27
0.27
0.85
0.83
3.0
1.0
0.24
0.35
0.48
0.74
M.protractus NUMBER
MEAN SD OF TREES
0
1.4
1
0.5 1.0
0.36 0.84
0
0
0
0
0
0
4
5
4
14
20
13
8
1
4
1
0
0
0
0
0
0
0
0
0
1
2
2
8
16
12
8
9
4
5.0 2.0
0
0.27 0.47
0
0.12 0.33
0
0
0
3
4
11
14
17
15
10
8
I-'
N
0
121
prosopis and M. amicus in the mesquite guild, but also that
all of the species combined only destroy a very small
proportion of the total seed crop.
Even considering
cumulative attack, much less than 33% of all the seeds were
destroyed by the bruchids and these infestation levels are
much greater than those actually found in the field (chapter
3, 5).
Mesquite seeds are thus an abundant resource at all
times and are not a limiting resource.
The mean monthly temperatures during the period of
greatest bruchid activity (July to September) are around 25°
C.
Diurnally temperatures vary greatly, ranging from 10°C
to 40+ C (Fig. 4-2).
vary diurnally.
Similarly pod and seed temperatures
The bruchid larvae thus develop in a
constantly changing thermal environment.
The internal pod
temperatures vary depending upon the phenological state of
the host pod (Table 4-3).
Temperatures of green pods did
not vary significantly from ambient air temperature (T =
0.86, df= 7, P=0.419).
Temperatures of dry pods averaged
1.6°C above ambient in full sunlight.
The internal
temperature of pods on the ground was best estimated by the
mean of ground surface temperature and the air temperature 1
em above the ground.
The temperature of these pods was
buffered to some extent by the soil mass but still reached
temperatures as hig~ as 50°C in September.
50 .
w
0::
~30
<(
0::
w
0..
~
w
..___
10
TIME
DATE
6PM
9-16
6PM
9-17
6AM
6PM
9-18
6AM
6PM
9-19
Fig. 4-~. The daily temperature variation in the lower crown of a mesquite tree for
four days in September, 1982.
1-'
r.J
r.J
Table 4-3. Internal temperatures of mesquite pods, for green
and dry pods on the tree, and for pods on the ground.
pod state
description
De vi ati on from
ambient °C
GREEN
AMBIENT
.500 + .582
DRY
t1EAN 0 F SHADE AND SUN
1.594 + .517
GROUND
MEAN OF GROUND TEMP
AND AIR TEMP AT 1 em
11.19 + 1.86
.......
N
w
124
Respiration
The metabolic rate in adults of these four species
increased significantly with temperature.
The rates of
increase fall into two groups (Fig. 4-3).
The metabolic
rates of Mimosestes amicus
and~·
protractus are only very
slightly affected by changes in temperature, while those of
A·
prosopis and N. arizonensis are affected to a much
greater extent, indicating a greater degree of homeostasis
in the former.
The metabolic rate of M. protractus is lower
overall than all the other species at most temperatures,
while that of M. amicus is higher at temperatures below 35°
C.
These re spon s·e.s are simi 1 a r to those that have been
reported for other desert bruchid species (Kistler 1982) and
for other insects (Keister and Buck 1974).
A major
difference in the responses of these adults to temperature
is the relatively strong negative effect of higher
temperatures on!· arizonensis.
Adult bruchid beetles show a significant positive
relationship of metabolic rate with body weight (Fig. 4-4).
The cost of living forM. protractus again falls below the
regression line, while the per beetle oxygen consumption of
~·
amicus is much greater than expected.
These metabolic
rate curves for adults are not related to either body weight
or abundance.
M. amicus and N. arizonensis have a similar
body size but are both larger than
significantly larger
than~·
A·
prosopis and all are
protractus. (Tables 1, 5).
125
8
0
6
w
f<(
a::
4
u
...J
0
co
~
w
~2
20
30
40
50
TEMPERATURE (°C l
Fig. 4-3. Metabolic rate -temperature relationships for adults of
the mesquite seed beetle guild. All species show a significant
increase in oxygen consumption with temperature to 40 or 45°C.
There are three distinct groups based on the slopes of the increasing
portions of the curves. All slopes are greater than zero (both t
and F statistics) and are ranked in the following manner; M. amicus
(MA) = f1. protractus (MP)< fl. prosopis (AP)< ~· arizonensis (NA).
126
80
w
I-
<
c:
~
....J
40
0
CD
~
w
~
20
30
TEMPERATURE
40
50
( °C)
Fig. 4-4. Metabolic rate - temperature relationships for larvae of
the mesquite seed beetle guild. All species show a significant (t
and F; P 0.05) increase in oxygen consumption with temperature to
35 or 40°C. The slopes of the increasing portions of the curves are
ranked in the following order (95% confidence intervals): ~· prosopis
(0.13-1.31) = ~· arizonensis (0.44-1.18) < M. amicus (1.02-2.76).
127
=
Y 2.2 7 X + 2.1 8
r2 = 0.698
16
MA
NA
12
w
~
<(
0::
lAP
j/
u
_J
0
~MA-C
SG9
I-
ccf
8
co
~
SP¢
w
~
zs
4
~
I
SL ~AP
tMP
SS?
I
2
DRY
4
6
WEIGHT (mgl
Fig. 4-5. Relationship of metabolic rate at 30°C with dry weight for
11 species of Bruchidae. Of the four species examined in this study,
~· protractus (MP) falls significantly below the line, while~· amicus (MA)
falls significantly above the regression line. Plot is of means ± std.
error. The regression is based on data from Kistler (1982), the present
study, and from unpublished data. (AP)-~. prosopis; (NA)-R. arizonensis;
(CC)-Callosobruchus chinensis; (MA-C)-M. amicus in seeds of Cercidium
floridum; (SG)-Stator generalis; (SP)-~. pru1n1nus; (SS)-~. sordidus;
(ZS)-Zabrotes subfasciatus.
128
The larvae of the three species examined also show
significant increases in metabolic rate with temperature
(Fig. 4-5}.
The rates of increase again differ with species
and fall into two groups.
larvae of M. amicus are affected
by temperature to a greater extent than the other two
species.
larvae of M. amicus also have the highest
metabolic rate at almost all temperatures.
N. arizonensis
larvae have the lowest metabolic rate at all temperatures,
while A. prosopis is intermediate.
larval metabolic rates
are also unrelated to adult body size, abundance, or
developmental rates, and thus must be related to the cost of
resource utilization, the cost of development, or a cost of
differing energy utilization and storage strategies.
Three measures of reproductive capabilities clearly show
that~·
amicus has a potential for producing far more eggs
than either of the other two species at all temperatures
(Fig. 4-6}.
This species also shows the greatest variation
with temperature.
~·
prosopis and N. arizonensis have very
similar reproductive capabilities, which are influenced very
little by temperature.
This lack of an effect of
temperature on fecundity is unusual for bruchids, which
usually show a curve more similar to that of M. amicus
(Kistler 1982, Howe and Curie 1964}.
The greatest effect of
temperature. on fecundity appears to be an increase in the
pre-reproductive period as temperatures decrease.
effect is most pronounced in M. amicus
and~-
This
arizonensis,
but is of little consequence to A. prosopis (Figs. 6a, 8).
Fig. 4-6. A). Curves of mean fecundity for weeks 1-3. Both 111. amicus
and N. ari zonensi s show a significant increase in the number of eg·gs
laid-as temperature increases (Mean± Standard Error).
Much of this
increase is due to a decrease in the pre-reproductive period, with
increasing temperature. This effect is absent in A. roso is, which
shows no significant change with temperature (F(3,-12 = 2.53; P>O.l).
B). The maximum number of eggs produced ina single week by each species.
C). The total number of eggs laid per lifetime by an average female.
Both total and maximum fecundities of~· prosopis and~· arizonensis
show no change with temperature, except N. arizonensis shows a
significant decrease in total fecundity at 35°C. All three measures
show that the fecundity of 1~. amicus is strongly reduced by low
temperatures.
-
130
~t~ ..
so
......"'
60
~
...
a:
Q.
40
/1----__1"
6
?
Ap
I
20
~120
25
i-
35
30
-f----~
Ma
---aNa
,_ _ _ ]lAp
~~-·
300
240
I
...J
~
0
>- 120
I
----f~
Ap
1
t-----9~?<
60
¢ Na
I
20
25
30
TEMPERATURE I'Cl
35
131
180
140
<f)
>-
100
<.(
0
>-
I-
>
w
~
z
60
0
.....J
0
¢ ~
----~
20
20
25
TEMPERATURE
30
(0
35
()
Fig. 4-7. Longevity - temperature relationships for the adult
bruchids. The open symbols represent mean values for individuals
of all three species that mated and laid eggs. M. amicus often
do not lay eggs in the laboratory and their lifespan is increased
when this occu.rs (closed triangles). The data points are mean
values. Representative error bars are also shown (± 1 std. error).
132
Ap
50
0 20
c 25
<>30
A35
30
10
Na
50
>-
5z 30
~
v
.......
10
'140
c
·~
100
GO
20
Ma
c
\\
__ -o ___
2
--·-- '·o
<>~<>-o
--o...
,o\~----o'
---
3
4
5
6
'
7
8
9
WEEKS
Fig. 4-8. Weekly fecundity per lifetime at temperatures from 20°C
to 35°C for~- prosopis (Ap), ~- amicus (Ma), and~- arizonensis (Na).
Low fecundity during week one represents the effect of temperature
on the pre-reproductive period. This was most pronounced in M. amicus
at all temperatures, but was totally absent from N. arizonens1s and
~- prosopis at higher temperatures.
133
Longevity of adult beetles increased similarly with
decreasing temperature in all three species (Fig. 4-7).
~-
Females in general lived longer than males.
prosopis
lived longer than the other species at most temperatures.
N. arizonensis seems again to be adversely affected at
higher temperatures.
Approximately 15 pairs
of~·
amicus
failed to produce eggs and had a significantly longer life
span at all temperatures than those pairs that produced
offspring.
Increased lifespan at lower temperatures
counterbalanced any decrease in number of eggs laid per unit
time resulting in equivalent total reproductive output over
all temperatures (Fig. 4-8).
Developmental rate curves were significantly different
for all three species, but all showed a similar pattern of a
decrease in developmental rate with decreasing temperature
(Fig. 4-9).
0
The linearity of these curves below 30 C
allowed an accurate determination of the developmental
thresholds (Table 4-4).
The thermal constant shown in Table
4-4, is the amount of heat required over time for an insect
to complete its development (Messenger 1970).
arizonensis requires the most heat,
while~-
N.
prosopis
0
requires the least at temperatures greater than 20 C.
Larval survivorship appears to be high at temperatures
0
greater than 25 C.
However N. arizonensis
and~·
prosopis
have a very rapid rise in mortality as temperatures drop
0
below 25 C (Fig. 4-10) and again
!· arizonensis is the most
negatively affected at higher temperatures.
134
4
160
o Ap
c:. Ma
o Na
0
fT1
<
fT1
r
(\J
3
0
0
iJ
$:
z
\
~
\
w
0
fT1
\
X
r
\
f<(
0::
120
\
-i
\
2
80
\
$:
fT1
.....J
~
0
z
w
)>
-<
:E
(j')
Q..
0
_j
w
a
40
">
w
0
0
20
25
TEMPERATURE
30
(°
35
Cl
Fig. 4-9. Developmental rates and times of the egg and larvalpupal stages at the experimental temperatures. The developmental
rate of M. amicus was most affected by higher temperatures, while
~- prosopis exhibited the most rapid decrease in developmental
rate with decreasing temperature. The standard error of the
mean for each value plotted is in all cases less than the size
of the symbol depicting that mean.
135
Table 4-4. Temperature constants for bruchids that attack seeds of
Prosopis velutina.
ESTIMATED DEVELOPMENTAL
THRESHOLD (°C)a
THERMAL CONSTANT
Algarobius prosopis
15.1
698
Mimosestes amicus
12.9
742
Neltumius arizonensis
14.9
820
SPECIES
(dd/50)b
acaculated by extending the lines in Fig. 4-9 to the abscissa.
bcalculated from the mean of the developmental times at 25, 30, and 35°C.
136
1.0
6Ma
oNa
a..
I
(f)
23 0.5
>
>
0:::
:::::)
(f)
0
20
25
TEMPERATURE
30
(°
35
Cl
Fig. 4-10. Relative survivorship of larvae at the experimental
temperatures.
137
The adult body weights of these four species were
different (Table 4-5).
The proportion of total weight that
was water ranged from a low of 39.1% in M. amicus to about
43% in N. arizonensis
and~·
prosopis.
These values are
lower than those reported for CallosobruchHs analis and
lower than water content values for many insects (Wightman
1978a).
Similarly there were differences in weights of eggs
produced by these species.
Neltumius arizonensis produces
an egg that is significantly larger than the other two
species examined, although the water content of the eggs of
all three species was around 50%, a value very similar to
that found for C. analis (Wightman 1978a) (Table 4-6, Fig.
4-11).
The biomass of eggs produced by each species
accounted for from 30% to 68% of the total initial adult
biomass.
Wightman found that egg biomass accounted for only
about 10% of initial adult body weight in unfed C. analis.
Therefore, in beetles fed on only a sucrose solution, a much
greater proportion of initial energy and materials' was
expended in egg production.
DISCUSSION
Previous studies on physiological ecology of the
Bruchidae have examined mainly ovarian production, realized
fecundity and development of economic species.
In most of
these studies, the beetles have been dented access to food
Table 4-5. Adult weights and percent water for the four members of the mesquite bruchid guild.
The regression coefficients for the relationshlp between wet and dry weights are given.
mean+SD
mean+SD
Algarobius prosopis
mean+SD
mea
6 .06+1. 76*
3. 46+1.04*
43.20+2.46
REGRESSION COEFFICIENTS
wet ::: B dry + B0
1
R2
B1 .!_ SE
s0 .!_ SE
1.68+0.037
0. 236+0 .132
0.985
Mimosestes amicus
8.07+2.81
4.95+1.80
39 .10+2. 31 *
1.56+0.022*
Neltumius arizonensis
8.04+1.60
4.82+0.90.
42. 57+1. 92
1.75+0.060
-0.029+0.294
Mimosestes erotractus
-
2.92+0.18*
12.42
13.90
31.64
.001
.001
.001
.05
.01
SPECIES
AN OVA F(2 ,97}
p
Scheffe (P:::0.05}
WET WEIGHT
*Apd1acNa
DRY· WEIGHT
*Mp:::Ap Ma:::Na
PERCENT WATER
0. 358+0 .115*
0.994
0.963
*Ma<Ap:::Na
.......
w
(X)
Table 4-6.
Egg weights and percent water for the members of the mesqu1te bruchia guild.
SPECIES
DRY WEIGHT
PERCENT WATER
mean+sd
.0217+.00178
.01052
. 513+ .0398
.304
1.12
Mimosestes amicus
{N-40)
.0224+.00195
.0118
.471+.0460
.679
3.02
Neltumius arizonensis
(N=50)
.0502+.00123*
.02615
.478+.0127
.472
2.09
451.7
-
1.72
Algarobi us
{N-40)
prosopi~
--
~--
ANOVA F{2,10)
p
* .001
-
RAnol
WATER2
USED (mg)
WET WEIGHT
mean+sd
N.S.
1Ratio of mean total lifetime egg weight (dry)/mean dry body weight.
2The amount of water (weight) expended in egg production for each species.
.......
w
1.0
15 ..
o
6
0
Ap
Ma
Na
6
6
6
'a
ooo
{))
Do
00
E 9
cfbo6DA
a:aoa
II
o
<..?
o~
w
3:
0
0
0
1-
0
w
3:
6
0
3
~$
DDAA
6
6
A
A
Ai:Z>
6
A
A
oX~
~OA
0
0
0
A
0
3
DRY
5
7
9
WEIGHT (mgl
Fig. 4-11. Relation between wet weight and dry weight of adults. The
slope of the relationship forM. amicus is significantly less than that for the other
two species, indicating that this species has a lower water content than the other
two species. Regression equations and statistics are given in Table 4-5.
.......
"""
0
141
or water, and only one species has been examined.
The basis
for such studies rests on the assumption that when adult
beetles emerge from their host seeds, they contain
sufficient potential energy and nutrients to initiate the
next generation.
Even though this assumption has a limited
truth in the real world, some significant results have
emerged from such studies.
Ripe pods or seeds stimulate
oogenesis in females and receptivity to mating attempts by
males, depending on whether eggs are laid on pods or seeds
in nature (Pierre 1980, Sandner and Pankanin 1973, Pimbert
and Pierre 1983).
There is an unclear interplay between
reproductive costs and longevity (Bushnell and Boughton
1940, Gokhale and Srivastava 1975, Huignard and Biemont
1978, Leroi 1980).
Temperature mainly affects longevity- of
adults and this effect varies between species (Sharma et al.
1979, Utida 1971), but may also affect both male and female
reproductive capacities (Huignard and Biemont 1974, Hamed
1981).
More recent studies have shown that food may be very
important to female bruchids, affecting both longevity and
reproductive capabilities (Leroi 1978, Pesho and VanHouten
1982).
Male copulatory secretions may also play a role in
female nutrition (Huignard 1983).
Studies involving
bruchids fed with mixtures of pollen, honey and water have
demonstrated that there is no significant relationship
between adult longevity and the number of offspring produced
(Leroi 1978).
142
This study is an attempt to examine the comparative
physiological ecology of a single guild of bruchid beetles
that attack the same host seeds.
Adults were provided
unlimited access to food to simulate field nutritional
conditions where access to pollen and nectar may be
unlimited.
In the following discussion I shall discuss the
responses of each species separately and then show how these
different responses may affect the guild structure as a
whole.
Algarobius prosopis is the most abundant member of the
mesquite seed beetle guild, destroying over 90% of all
attacked seeds (Swier 1974, Conway 1980, Table 4-1).
There
are four outstanding features in the physiological
capabilities of this species.
Adults live longer than the
other species at all temperatures.
Reproduction is more
independent of temperature than all other species.
The
metabolic rates of larvae are least affected by temperature
and their developmental rate is most rapid at the
temperatures usually experienced in the field.
These
factors undoubtedly play an important role in the successful
strategy
ad~ptive.
of~·
prosopis, while other factors seem to be less
Adult metabolic rate is largely dependent on
external temperature, but this limitation may be
circumvented by diurnal activity patterns.
Adult fecundity
is very low and in two out of three of the measures of
fecundity it is lower than all the other species.
Females
expend less of their initial biomass in egg production than
143
the other species.
Larvae appear to be intermediate in
their efficiency of utilization of host seeds, based on
larval metabolic rates. The larvae are more efficient than
~.
amicus but less so than !· ari.zonensis.
These apparently
negative factors may be less important since fecundity is
often unrelated to success (Price 1974), as it is often
outweighed by such factors as survival of young and
longevity.
Also,
~·
prosopis is more physiologically
efficient in host seed utilization than its closest
potential competitor, M. amicus.
Mimosestes amicus is the only member of the guild that
is not a specialist on mesquite seeds and yet it is the
second most abundant species.
The most unique feature of
this species was its tremendous reproductive capacity.
It
is capable of producing and laying three times as many eggs
as the other two species.
Adults are able to regulate their
metabolism at a fairly constant level regardless of external
temperatures.
This may be important for a generalist
species attacking hosts with widely varied phenologies,
spanning a wide temporal range throughout the growing season
in a desert habitat.
Furthermore, adults in the absence of
appropriate hosts may live for extended periods of time
(>160 days in this study) irrespective of external
temperatures.
This capability was not evident in any of the
other species and may again be related to their wide use of
resources with different phenologies.
M. amicus larvae
develop rapidly (intermediate) but were more successful at
144
developing at all temperatures than the other two species as
evidenced by both their low developmental threshold and
their low larval mortality.
In contrast to these successful adaptations are several
that appear to have a negative impact.
Adults have a very
low water content, but expend on the average 3.02 mg of
water (97% of initial water content) and 68% of initial
biomass in egg production.
Associated with the longer
preovipositional period (Fig. 4-8) and the fact that
oviposition rarely occurs in the absence of food, these
three factors point to an extreme dependence on external
sources of food and water.
In contrast to the adults,
larvae are more sensitive to temperature.
Larvae are also
the least efficient at use of P. velutina as a resource,
based on their significantly higher metabolic rate, which
indicates a very high relative cost of total development.
M. amicus thus appears to have a different set of
environmental limitations
than~·
prosopis, mainly based on
a high apparent metabolic and nutrient cost of resource
utilization by both adults and larvae, but also appears to
be more adapted in
reprodu~tive
capabilities, survival and
development of larvae.
Neltumius arizonensis is one of two rare species that
are members of the guild.
The only striking feature
apparent from this study is the very low metabolic rate of
its larval stage.
Part of this low respiration rate might
be due to the slower developmental rate.
However, when this
145
is taken into account development still takes considerably
less total energy than that of
~·
amicus or A. prosopis.
The metabolic rate of the larval stage is also not greatly
affected by temperature.
Thus, I conclude that N.
arizonensis is the most efficient at feeding in seeds of P.
velutina.
Adults and larvae, however, are more temperature
dependent than the other species.
Temperature has a more
consistently negative effect on fecundity in this species.
Developmental rate is significantly slower at all
temperatures and both adults and larvae are more negatively
affected by both high and low temperatures.
N. arizonensis
thus appears to be more limited by abiotic factors than
either
~·
amicus
or~·
prosopis.
Mimosestes protractus is the least abundant member of
the guild in north-central Arizona, although it may be more
abundant (but still minor) further south at lower elevations
(Conway 1980).
Because it attacks only green pods and is
most likely univoltine, very little data are available.
has the lowest adult metabolic rate.
It
This may be due to a
decrease in metabolism to a diapause-like state, in the
absence of appropriate hosts (i.e., green pods).
Natural selection should favor optimal adaptation to
environmental and host characteristics.
Developmental rate
should be maximized to decrease exposure to the environment,
parasitoids, predators and competitors (Spence et al. 1980).
The cost of development should however, be minimized, as
should the cost of response to environmental variation.
146
Production of eggs need not be maximized, but the intrinsic
rate of increase, r, should be maximized.
The environment
(the seed) is identical for the three most abundant species
that attack mature seeds and pods.
This study, however,
shows that beetles in the mesquite seed beetle guild possess
no single optimal solution to environmental and host
adaptation, even though this might be expected.
As a
generalist, M. amicus appears to have sacrificed some
resource adaptation for a more maximal environmental
adaptation.
Maximal reproductive output allows it to
utilize many hosts and although the generalist larvae are
less efficient, their overall success is high.
undoubtedly limits the abundance
of~·
This
amicus on any one
resource but its overall abundance in the environment across
all of its hosts and across time may be considerably higher.
Cercidium floridum Bentham is a more preferred host forM.
amicus.
The metabolic cost of development is much less on
seeds of this plant
and~·
amicus is the most abundant
bruchid on this host, indicating that larval utilization
efficiency might be important in determining abundance in
the bruchid guild (Johnson and Kistler 1985).
Mimosestes protractus has become an extreme resource
specialist.
It has decreased its metabolic costs and body
size, and specialized its larval morphology so that it may
efficiently utilize a smaller (i.e., less well developed
seed) but less utilized resource.
(A.
prosopis is the only
other species that purportedly can attack green pods
147
(Kingsolver et al. 1977} but Fig. 4-1 clearly indicates that
more mature green pods are preferred}.
However, this
strategy limits it to one or at most two generations per
year and thus although it may be successful (i.e., have
relatively constant populations} it will be less abundant
than the other species.
Although the cost of development appears to be lowest
for N. arizonensis in seeds of mesquite, it appears to be
the least adapted to the extreme environmental variation
that it must face in this desert ecosystem.
Adults and
larval stages both are more adversely affected by high
temperatures (e.g., decreased larval survivorship, decreased
developmental rate, decreased longevity, decreased
fecundity, and increased metftbolic rate at temperatures
0
greater than 30 C).
These physiological limitations may be
the reasons that its population peak occurs in
Octob~r
through December, when high temperatures are not as extreme.
In support of this temperature limitation hypothesis is the
absence of this species from site 5 in 1982, where pods were
produced during July and were mostly gone by mid-August.
All other species were abundant. Also this species is often
absent from samples taken from more southerly populations
(Conway 1980, chapter 5}.
Late in the summer when this
species is most active, the resource (number of pods) is
decreasing as pods fall from the tree (N. arizonensis and M.
amicus do not oviposit on pods after they have fallen to the
ground).
Thus the decreased resource availability and
148
decreased period of potential resource use may result in the
rarity of N. arizonensis in the mesquite seed beetle guild.
The large eggs produced by!· arizonensis may also
contribute to its relatively low .abundance and to its shift
to oviposition in late summer.
eggs, of
~·
Mitchell (1977) found that
amicus, which were laid under other eggs, and of
Stator limbatus, which were laid inside a seed pod of
Cercidium floridum, had only a 15 to 20% mortality rate due
to heat and desiccation, while eggs exposed on the pod
surface suffered a much higher temperature related mortality
(23 to 50%).
Eggs of N. arizonensis are more than twice as
large as the eggs of any of the other species and because of
their larger overall surface area, heat
o~
desiccation
related death of the eggs might be even greater than the
high levels found by Mitchell.
By shifting its resource
utilization to late summer it could avoid temperature
extremes that would increase mortality of adults, larvae and
eggs.
The more rapid developmental rate, longer adult life,
relative independence of temperature effects on oviposition
and on larval metabolic rates, and smaller adult body size
all indicate
that~·
prosopis is relatively more adapted
~o
utilization of mesquite as a resource, as well as being more
adapted to the harsh diurnal temperature fluctuations and
seasonal extremes faced by these bruchids.
This species
seems to be especially adapted to higher temperatures (35°C)
common during the peak of the pod population in July and
149
August.
However, just these physiological factors alone do
not make a convincing picture as to
successful.
why~·
prosopis is so
The major difference between this species and
the other three is their distinctly different oviposition
behavior.
Oviposition in crevices on the pods, and
emergence holes of other bruchids significantly decreases
temperature related egg mortality (Mitchell (1977) in other
bruchid species and so is likely to reduce egg mortality in
~·
prosopis also.
~-
prosopis also inserts eggs into the
matrix structure of the pod wall, which could reduce
abiotically induced mortality even more.
Factors other than temperature-related phenomena may
also influence the structure of this guild of bruchids.
There is a large amount of spatial and temporal variability
in mesquite seed numbers and quality (chapters 2, 3).
This
variation is equal for all species and so should not cause
the observed differences in relative abundance and timing of
the bruchids, but it may contribute to a maintenance of rare
species (e.g., the absence of the two rare species from
samples in 1982) as rare species.
Parasitoids of the larvae
attack all four species but may preferentially attack the
larger larvae of M. amicus
and~·
arizonensis, while they
may be relatively less able to locate the smaller larvae of
~-
prosopis (chapter 5).
Simil~rly,
the larger eggs of N.
arizonensis may be more apparent to parasitoids that attack
the eggs, as well as to other egg predators, whereas the
"secretive" oviposition strategy
of~-
prosopis
150
significantly decreases egg parasitism relative to the
exposed eggs of the other species (Bridwell 1918, chapter
5)•
Abundance must be a function of resource availability
and predictability, and fecundity-mortality events,
influenced to some extent by larval developmental rates.
As
was mentioned above, resource availability and
predictability should be equal for all species in the
mesquite guild and so should not play an important role in
the species abundances (except as morphological and
physiological parameters restrict them to smaller subsets of
the total resource pool).
Fecundity of the species in the
guild is independent of the observed abundances (i.e., the
most fecund is not the most abundant). Population growth
rates and abundances thus must be due to mortality events
(real or potential) due to predation or abiotic limitations,
such as differential tolerances to temperature and moisture
stresses imposed on the populations by the harsh and
unpredictable desert environment.
This study was designed
to address the abiotic factors that might limit these
populations, while other papers deal with resource variation
and parasitoids and their effects on the bruchids (chapters
3, 5).
Temperature was chosen as the variable most likely
to limit these
popul~tions
since moisture stress should only
occur at the egg and adult stages, because the larvae
survive on seed water content and metabolic water and are
surrounded by an impermeable seed coat during development.
151
The data indicate that life history parameters
(fecundity, longevity, survivorship)
of~·
prosopis are
least affected by high temperatures such as those that occur
during the peak of pod production.
Associated with this
resistance to high temperatures is a significantly greater
0
developmental rate at all temperatures greater than 25 C.
!· arizonensis is negatively affected by high temperatures
more than any of the other two more abundant species (large
egg size, survivorship, growth rate, fecundity, longevity,
adult metabolic rate) and develops more slowly at all
temperatures.
M. amicus lies between these two extremes,
showing negative effects of temperature on larval metabolic
rates and fecundity and an intermediate developmental rate.
All of these species are thus affected by temperature and,
the degree of adaptation to high temperatures and to rapid
temperature changes seems to be associated with the
abundance of the species.
It is not clear from these data
that temperature is the main factor limiting overall
abundance of the species.
Studies need to be done to
examine abiotically caused egg mortalities in the different
species to complete this picture.
A second purpose of this study was to see if temperature
limitation might be able to explain the temporal
distribution of the species abundance curves (Fig. 4-1),
which had previously been attributed to competitive
interactions.
M. protractus utilizes only green pods as a
resource and does not attack the other two pod stages.
This
152
factor alone explains its abundance peak being shifted to
the left of all the other species.
During this early green
pod stage, it may constitute up to 30% of the total bruchid
population, demonstrating its effective utilization of an
under-utilized resource, while at the same time allowing it
to attack before parasitoids of its eggs and larvae have a
chance to build up their populations.
Green pods are also a
much more abundant and predictable resource but pod abortion
increases the chances of a wasted oviposition at these early
stages (chapter 2).
Since internal temperatures of green
pods are equivalent to ambient temperatures, temperature
stress on these pods at this hottest time of the year will
probably not be any greater than that experienced by the
other species in dry pods later in the summer.
The peak of the populations
of~·
prosopis and M. amicus
occur during the peak of resource abundance.
The relative
temperature independence of these two species allows them to
utilize this resource peak.
The low total abundance of
bruchids even during periods of low resource abundance (pods
and seeds), apparently allows both species to share this
temporal niche with little or no apparent selection for
competitive divergence.
Since~·
amicus is a generalist
with other potential host species, switching to mesquite as
a host would be most beneficial during the resource peak.
Thus, its timing may be simply a result of its generalist
strategy.
Examination of the population dynamics and
phenology of M. amicus on its alternattve hosts would
153
provide insight into its overall strategy and population
abundance.
Lastly, the population peak of N. arizonensis
appears to be shifted toward the cooler months of the summer
(and early spring).
This shift
~ppears
to be caused largely
by its inability to tolerate high temperatures which
negatively affect egg survival and other life history
parameters.
At the same time, this shift may reduce the
probability of potential competitive interactions between
larvae of this species and the two more abundant species.
The inability to tolerate high temperatures may limit the
numbers of this species due to decreased resource abundance,
a limitation of population growth rates by lower
temperatures, and a build up of parasitoid populations by
this time in the season.
be an optimal strategy for
This definitely does not appear to
~·
arizonensis.
Its continued
existence in the mesquite bruchid guild argues strongly
against a competitive explanation for the temporal
distributions and abundances within the guild.
Temperature related phenomena can thus strongly
influence species abundances and temporal distributions in
this guild of bruchid beetles.
It may also maintain
populations of all of these species below levels where
interspecies interactions and competition might occur.
154
LITERATURE CITED
Bridwell, J. C. 1918. Notes on the Bruchidae and their
parasitoids in the Hawaiian Islands.
Entomol. Soc.
Proc. Hawaiian
3:465-509~
Bursell, E. 1964. Environmental aspects:
283- 321.
In:
temperature.
pp.
M. Rockstein (ed.). Vol. 1, The physiology
of Insecta, Academic Press, New York.
Bushnell, R. J. and D. C. Boughton. 1940. Longevity and egg
production in the common bean weevil, Acanthoscelides
obtectus.
Ann. Entomol. Soc. Amer.
Clarke, K. U. 1967.
In:
33:361-370.
Insects and temperature.
pp. 293-352.
A. H. Rose, Thermobiology, Academic Press, New York.
Conway, R. 1980. A comparative study of the
bruchid-parasitoid complexes found in some Arizona legumes.
Unpub. M.S. Thesis, Northern Arizona University, 99pp.
Doyen, J.T. and C.N. Slobodchikoff. 1984. Evolution of
microgeographic races without isolation in a coastal dune
beetle. J. Biogeog. 11:13-25.
Fujii, K. 1967. Studies on interspecies competition between
the Azuki bean weevil, Callosobruchus chinensis , and the
Southern cowpea weevil, C. maculatus. II.
different environmental conditions.
9:192-200.
Competition under
Res. Popul. Ecol.
155
Gokhale, V. G. and B. K. Srivastava. 1975. Ovipositional
behavior of Callosobruchus maculatus (Fabricius)
(Coleoptera:Bruchidae). I. Distribution of eggs and relative
ovipositional preference on several leguminous seeds.
Indian J. Entomol. 37:122-128.
Hamed, M.S. 1981. Effect of heat on the fecundity of the
bean weevil Acanthoscelides obtectus (Coleoptera,
Bruchidae). Z. Angew. Entomol. 91:368-374.
Howe, R. W. and J. E. Currie. 1964. Some laboratory
observations on the rates of development, mortality and
oviposition of several species of Bruchidae breeding in
stored pulses.
Bull. Entomol. Res. 55:437-477.
Huignard, J. 1983. Transfer and fate of male secretions
deposited in the spermatorphore of females of
Acanthoscelides obtectus Say (Coleoptera, Bruchidae).
J.
Insect Physiol. 29:55-63.
Huignard, J. and J.
c.
Biemont. 1974. Effect of an increase
of temperature on the male reproductive capacity of
Acanthoscelides obtectus Say (Coleoptera, Bruchidae). Ann.
Zo o 1 • Ec o 1 • .A n i m• 6 : 5 6 1- 5 7 4 .
Huignard, J. and J. c. Biemont. 1978. Comparison of four
populations of Acanthoscelides obtectus
(Coleoptera:Bruchidae) from different Colombian ecosystems.
Oecologia 35:307-318.
156
Johnson, C. D. 1978. Ecology of Neltumius texanus
(Coleoptera:Bruchidae) in seeds of Condalia (Rhamnaceae). J.
Kans. Entomol. Soc. 51:432-440.
Johnson, C. D. 1981a.
Seed beetle host specificity and the
systematics of the leguminosae.
pp. 995-1027, In: R. M.
Polhill and P. H. Raven (eds.). Advances in legume
Systematics, Royal Botanic Gardens, Kew.
Johnson, C. D. 1981b. Interactions between bruchid
(Coleoptera) feeding guilds and behavioral patterns of the
pods of the leguminosae. Environ. Entomol. 10:249-253.
Johnson, C.D. and R.A. Kistler. 1985. Nutritional ecology of
bruchid beetles. In: F. Slansky Jr. and J.G. Rodriguez
(eds.). Nutritional ecology of insects, mites and spiders,
John Wiley and Sons, New York, submitted.
Keister, M. and J. Buck. 1974.· Respiration: some exogenous
and endogenous effects and rate of respiration. pp. 469-509.
In:
M. Rockstein (ed. ). Physiology of Insecta, Vol. 6,
Academic Press, New York.
Kingsolver, J. M. 1964. The genus Neltumius
(Coleoptera:Bruchidae.
Coleopt. Bull. 18:105-111.
Kingsolver, J. M. and C. D. Johnson.
1978. Systematics of
the genus Mimosestes (Coleoptera:Bruchidae).
Agric. Tech. Bull. 1590, 106pp.
u.s.
Dept.
157
Kingsolver, J. M., C. D. Johnson, S. R. Swier, and A. Teran.
1977.
Prosopis fruits as a resource of invertebrates. pp.
108-122. In:
B. B. Simpson (ed. ). Mesquite: its biology in
two desert shrub ecosystems. Dowden, Hutchinson and Ross,
Stroudsburg, Pennsylvania.
Kistler, R. A. 1982. Effects of temperature on six species
of seed beetles (Coleoptera:Bruchidae): an ecological
perspective.
Ann. Entomol. Soc. Amer. 75:266-271.
Kunhikannan, K. 1923. The function of the prothoracic plate
in Mylabrid (Bruchid) larvae, (A study in adaptation).
Mysore State Dept. Agr., Ent. Ser. Bull. 7, 47pp.
Lawton, J.H. and D. R. Strong. 1981.
competition in folivorous insects.
Community patterns and
Am. Nat. 118:317-338.
Leroi, B. 1978. Feeding of adults of Acanthoscelides
obtectus Say (Coleoptera:Bruchidae). Influence upon the
longevity and ovarian production of virgin individuals.
Ann. Zool. Ecol. Anim. 10:559-568.
Leroi, B. 1980. Regulation of egg production in
Acanthoscelides obtectus (Coleoptera:Bruchidae): The change
in stimulating effect of grain on females of different ages.
Entomol. Exp. Appl. 28:132-144.
May, M. L. 1979. Insect thermoregulation. Annu. Rev.
Entomol. 24:313-349.
158
Messenger, P. S. 1970. Bioclimatic inputs to biological
control and pest management programs.
pp. 84-99. In: R. L.
Rabb and E. E. Guthrie (eds. ). Concepts of pest management.
North Carolina State University Press, Raleigh, North
Carolina.
Mitchell, R. 1977. Bruchid beetles and seed packaging by
palo verde.
Ecology 58:644-651.
Mutchmor, J. A. 1967. Temperature adaptation in insects. pp
165-176.
In: C.L. Prosser (ed. ). Molecular mechanisms of
temperature adaptation. Pub. No. 84. AAAS, Washington, D. C.
Park, T. 1954.
competition.
Experimental studies of interspecific
II. Temperature, humidity and competition in
two species of Tribolium. Physiol. Zool. 27:177-231.
Pesho, G. R. and R. J. Van Houten. 1982. Pollen and sexual
maturation of the pea weevil.
Ann. Entomol. Soc. Amer.
439-443.
Pfaffenberger, G. S. and C. D. Johnson. 1976. Biosystematics
of the first-stage larvae of some North American Bruchidae
(Coleoptera).
U.S. Dept. Agric. Tech. Bull. 1525. 75 pp.
Pierre, D. 1980. Influence of seeds or ripe pods of
Phaseolus vulgaris on the reproductive activity of Zabrotes
subfasciatus (Coleoptera:
Bruchidae). C. R. Hebd. Seances
Acad. Sci. Ser. D. Sci. Nat. 290:1007-1010.
159
Pimbert, M. P. and D. Pierre. 1983. Ecophysiological aspects
of bruchid reproduction. I. The influence of pod maturity
and seeds of Phaseolus vulgaris and the influence of
insemination on the reproductive activity of Zabrotes
subfasciatus.
Ecol. Entomol. 8:87-94.
Price, P.W. 1974. Strategies for egg production. Evolution
28:76-84.
Rathcke, B. J. 1976.
Competition and coexistence within a
guild of herbivorous insects.
Ecology
57:76-87.
Sandner, H. and M. Pankanin. 1973. Effect of the presence of
food on egg-laying by Acanthoscelides obtectus Say
(Coleoptera,Bruchidae).
Pol. Pismo. Entomol. 43:811-817.
Sharma, S. P., S. Rattan, and G. Sharma. 1979.
Temperature
dependent longevity of Zabrotes subfasciatus (Coleoptera:
Bruchidae).
Camp. Physiol. Ecol. 4:229-231.
Simberloff, D. and E. F. Connor. 1981.
Missing species
combinations. Am. Nat. 118:215-239.
Spence, J. R., D. H. Spence, and G. G. E. Scudder. 1980. The
effects of temperature on growth and development of water
strider species (Heteroptera:Gerridae) of Central British
Columbia and implications for species packing.
Zool. 58:1813-1820.
Can. J.
160
Swier, S. R. 1974. Comparative seed predation strategies of
mesquite bruchids in Arizona, with particular reference to
seed height, direction and density.
Unpublished M.S.
Thesis, Northern Arizona University, Flagstaff, Arizona.
97pp.
Taylor, V. A. 1980. Coexistence of two species of Ptinella
Motschulsky (Coleoptera:Ptiliidae) and the significance of
their adaptation to different temperature ranges.
Ecol.
Entomol 5:397-411.
Utida, S. 1971. Influence of temperature on the number of
eggs, mortality, and development of several species of
bruchid infesting stored beans. Jap. J. Appl. Entomol. Zool.
15:23-30.
Wiens, J. A. 1977. On competition and variable environments.
Amer.Sci. 65:590-597.
Wightman, J. A. 1978a. The ecology of Callosobruchus analis
(Coleoptera:Bruchidae):
morphometries and energetics of the
immature stages. J. Anim. Ecol. 47:117-129.
Wightman, J. A. 1978b. The ecology of Callosobruchus analis
(Coleoptera:Bruchidae): energetics and energy reservers of
the adults. J. Anim. Ecol. 47:131-142.
CHAPTER 5
The Role of the Third Trophic Level in the Mesquite-Bruchid
Ecosystem.
161
162
INTRODUCTION
Most knowledge of ecological communities is limited to
at most two trophic levels, with a striking void of
information on the roles played by predators and parasitoids
in communities, despite the fact that all three major
trophic levels appear to be tightly linked.
Because of this
paucity of knowledge about the uppermost trophic levels,
ecologists have began to examine the role of the third
trophic level in the evolution of both organisms and
communities (Price et al. 1980).
This new emphasis has
shown that communities of herbivorous insects may be more
limited by natural enemies then by other factors, like
competition, that have been thought prominent in the past
(Lawton and Strong 1981).
Thus, selection for enemy free
space (Lawton 1978) may be more prominent than intra-trophic
level interactions (Price 1983).
This study examined the role of parasitoids in a
mesquite-bruchid ecosystem (Leguminosae:Prosopis velutina
Wooten, Coleoptera:Bruchidae) in central Arizona.
In light
of the general lack of knowledge about the significance of
parasitoids in insect communities the major question asked
in this study was if the community of parasitoids is
important enough to exert a selective influence on the seed
predator community.
A secondary question asked whether or
not the parasitoid community exerts a differential influence
163
on the members of the seed-predator community, thus acting
as an organizing factor in this community.
METHODS
The populations of parasitoids were monitored through a
three year series of field collections of mesquite pods and
laboratory rearings as described in chapter 2.
A subsample
of these pods were examined immediately upon collection and
the number of bruchid eggs present on the external surface
of the pods was counted.
The number of these eggs that had
been parasitized by trichogrammatid egg parasitoids was
recorded.
To further examine the parasitoid community, field
experiments were undertaken in which cages (20cm X 10cm X
10cm) made of 1/4 inch (6.4mm) mesh galvanized hardware
cloth were filled with 15 mesquite pods, collected from the
population in 1982.
These were then hung in a tree which
had produced no pods in 1983.
Two sets of experiments were
carried out, with five replicate cages of each set.
The
entire set was then replicated in two distinct populations.
To examine the egg parasite population, a laboratory culture
of Mimosestes amicus (Horn) was allowed to freely oviposit
on a large number of pods for a three-day period.
These
pods were then divided randomly into groups of 15 pods,
placed into the cages and hung in trees during August 1983,
(tree #4 at site 5 and tree #10 at site 4), with five cages
per tree.
After 13 days all eggs were counted and
164
classified as dead, hatched, or parasitized.
These same
cages were used to examine parasitoids of early instar
bruchids.
After this thirteen-day period in the field, the
cages were collected, the pods were placed into jars, and
the bruchids and parasitoids were reared as described in
chapter 2.
The second set of experiments examined the parasitoid
community that attacks older instar bruchids, in the same
manner as described above.
However,
the~·
amicus larvae
were allowed to develop for 21 days prior to placing the
pods in cages and hanging them in the experimental trees in
the field.
These pods were collected 10 days later just
prior to emergence of adult bruchids.
These experiments
thus acted as a bioassay for the parasitoid community
attacking the eggs, early instar, and late instar and pupal
stages of the bruchid community.
The possibility of differential rates of parasitism
within the bruchid community was examined in a set of
laboratory experiments.
Three species of parasitoids were
used; egg parasitoids (Trichogrammatidae), Heterospilus
prosopidis Viereck (Braconidae) and Eupelmus cyaniceps
Ashmead (Eupelmidae).
prosopis,
~·
amicus,
Fifteen pods containing
or~·
la~vae
of A.
arizonensis of the appropriate
stage {eggs or 20 day old larvae) were placed into jars with
20 pairs of parasitoids.
Three replicates were used for
larval parasitoids and 12-were used for the egg parasitoid
tests.
165
RESULTS AND DISCUSSION
The population dynamics of the bruchids and larval
parasitoids varied between years as well as within each year
(Fig. 5-1).
The prominent resuli of these data was that the
parasitoid population closely followed the dynamics of the
host bruchid populations, but with a slight time lag.
This
is typical for parasitoid-host populations in general
(Hassell 1978) and for bruchid-parasitoid populations (Fujii
1983, Kistler 1979).
However, Figure 5-1 underestimates the
importance of the parasitoids.
Once pods were collected
from the field all larvae in the pods were instantaneously
removed from further parasitism which probably would still
occur in the field.
To achieve a more realistic measure of
the importance of parasitism (probably still an
underestimate), parasite populations were examined in
comparison with only the first two weeks of bruchid
emergence in 1983 (Fig. 5-2).
From these data it was
apparent that parasitism ranged up to 50% of the total
number of larvae per 30 pod sample.
It appeared possible
that populations of both egg and larval parasitoids might
strongly influence population dynamics of the bruchid guild.
This possibility was examined further for the egg parasitoid
populations by field counts of actual eggs parasitized in
comparison with the total number of eggs per 30 pod sample
(Fig. 5-3).
Fifty to 100% of all eggs on the external
surface of the pods were parasitized and there was a strong
166
0
I
90
I
I
I
0
I
\
I
I
I
I
0
\ i
60
0
1\
vo
a:
w
CD
:::0
::::>
0
I
I
I
I
0
z 30
\J
0
I
I
.
0
.
I
I
I
0
0
\'
I
0
Q
I
\
~
0
1\
0
'
.0
0
o' ""-.
.
p
I
~•
0
'
I
'
I
I
'
.,
'
o"'~ .?-o
i:J.-0 '"0
,'
! I'
0
''
_o
~
l.J.()oU
;
,'
\_
O~o~-.-~~Jdl~~-o~,o~/4--+o--r-----+~~a+-'~o~~~o-~o~--~+--+~~-r.~
9/1 7/1
1980
9/1
1981
1111
9/1
11/1
1982
8/1
10/1
1983
9/12
1984
DATE
Fig. 5-1. Population dynamics of the larval parasitoids (squares)
and their host bruchids in the mesquite ecosystem (circles) from
1980 to 1984 at site 1. These numbers represent the number of
successful emergences from pods maintained for 35 days in the
laboratory and are thus a measure more of potential than real
population levels. The parasitoid populations closely follow
the pattern in the bruchid populations. The bruchid population
is highly dependent upon the resource seed dynamics (chapter 2).
0 BRUCHIDS
12
o LARVAL P
t::.
EGG P
9
1
0::
w6
CD
~
/ !::.'
:J
z
3
'
~'f
'
..........
'
'~::. .....
""-....._
g/
-~o/~~yo
..... .....
'!::.--
' ' ----7/30
8;13
22
9/1
13
22
10/3
17
19 8 3
DATE
Fig. 5-2. Population dynamics of the bruchids (circles), larval parasitoids
(squares), and egg parasitoids (triangles) in the mesquite ecosystem for the
1983 season at site 1. These data are based upon only the first two weeks of
insect emergence after the pods were collected. This gives a more accurate
estimate of the actual dynamics of these populations in the field than Fig.
5-1. Egg parasitoid populations are high until pods began to fall from the
trees, while the larval parasitoids follow the dynamics of their host population more closely.
......
0'1
'-J
168
linear relationship between the total number of eggs and the
number of eggs parasitized.
The egg parasites possessed a
strong capability to regulate the overall populations of
bruchids in the field.
Because of the dependency of this study upon laboratory
rearing of field samples, it was more difficult to determine
the instantaneous importance of larval parasitoids.
That
larval parasitoids may also strongly limit or regulate
bruchid populations was indicated by three lines of
evidence.
First, the community of parasitoids found in this
study was extremely diverse (Table 5-1, Fig. 1-1),
indicating a relatively stable resource pool to support
these species.
Secondly, two factors point toward a
relatively high probability of competitive interactions
between species of parasitoids, indicating a limiting
resource in the second trophic level.
are very low.
Bruchid populations
An examination of Fig. 5-2 indicates a
maximum density of only one bruchid larva per every three
pods.
There was also a definite division of the resource by
bruchid instar, with Urisigalphus bruchi specializing on
early instars and Heterospilus prosopis specializing on
later instars (Fig. 5-4).
There was also some
circumstantial evidence that some of the smaller species
(especially 3 species of Eulophidae) might also specialize
on larvae in green pods while all other species prefer
bruchids in more mature pods.
169
120
R2 =0. 81
p =.001
•
0
w
80
N
I(/)
<(
a::
~
0
.40
z
40
NO.
80
120
EGGS
Fig. 5-3. There is a significant linear relationship
between the number of bruchid eggs on the external surface
of mesquite pods in the field and the number of these eggs
that have been parasitized by trichogrammatid egg parasitoids.
The regression equation is; Y = 0.619X- 0.9, F(1, 18) = 77.1.
170
Table 5-l.
Parasi toi ds of the mes.qui te seed predator gui 1d.
MOTH PARASITOIDS
Hymenoptera
Braconidae
Agathis tenuiceps
Species A
Species B
Ichneumonidae
Temelucha sp.
Diptera
Tachinidae
Species A
BRUCHID PARASITOIDS
Egg Parasitoids
Hymenoptera
Trichogrammatidae
Trichogramma spp. ?
Larval Parasitoids
Hymenoptera
Braconidae
Bracon therberi phage
Apanteles sp.
Heterospilus prosopidis
Urisigalphus bruchi
Eulophidae
Horismenus productus
Hyssopus evetriae
Tetrastichus dologus
7 misc. species ?
Eupelmidae
Eupelmus cyaniceps
Eurytomi dae
Eurytoma sp.
LARVAL
AGE
(daysl
<13
22-32
CR
BC
Fig. 5-4. The major larval parasitoids in the system appear to have subdivided
their host larval resource by larval size. Urisi al hus bruchi (UB) attacks mainly
young larvae, while Heterospilus prosopidis HP attacks mainly older larvae.
Two other parasitoids also attack mainly late instars (Eupelmus cyaniceps (EC) and
Urytoma sp. (U)). The numbers in the figure refer to the total numbers that were
reared from these caged pods at each of two sites (CR = site 5 and BC = site 4).
.......
-....J
.......
172
100
0
w
N
~
(./)
<t: 60
a::
<t:
Q..
(./)
~
~
w
~
0
20
AP
MA
NA
Fig. 5-5. Differential rates of parasitism of the eggs of three
species of bruchids by trichogrammatid egg parasitoids occurred
in laboratory tests. The eggs of fl. prosopis (AP) were attacked
significantly less often than the eggs of M. amicus (MA) and
N. arizonensis (NA) (ANOVA, F= 13.51; df=2-;- 27; P< .001).
Vertical bars represent 95% confidence intervals.
173
The third factor that indicated the importance of larval
parasitoids was that they appear to be extreme generalists.
In the laboratory tests, neither Heterospilus prosopidis nor
Eupelmus cyaniceps showed any preference for any bruchid
species.
This generalist behavior would tend to equalize
the populations of the four bruchid species in a density
dependent manner.
Thus the low numbers of bruchids, the
generalist nature of the parasitoids, which is unusual in
parasitic Hymenoptera (Price 1980, M. Hetz pers. comm.), and
the subdivision of the larval resource among the parasitoid
species all indicate that bruchid larvae might be a limiting
resource for the parasitoids.
These factors also indicate
that competitive interactions might occur (exploitation
competition) within this very diverse guild of parasitoids
that makes up the third trophic level in the
mesquite-bruchid ecosystem.
Do these parasitoids play any role in the organization
of the bruchid community?
It is clear from the above data
that their impact upon the bruchid populations was quite
extensive during the three years of this study.
They have a
potential to act as regulatory agents upon the bruchid
population as a whole, allowing all four species to coexist
in the same resource with very little or no interspecies
interactions (Chapter 3).
They may also act in a
differential manner, affecting different bruchid species to
different extents.
This was supported by data on egg
parasitism but not that on larval parasitism.
In the
174
laboratory, egg parasitoids were less able to find and
parasitize the eggs of
~·
prosopis, which are hidden in the
mesocarp of the pod or placed in groups in the exit holes of
other insects or in other damaged areas on the pods.
They
are more efficient at parasitizing the eggs of the other
species which are glued to the external surface of the pods
(Chapter 3, Fig. 5-5, Bridwell 1918).
These egg parasitoids
may thus play an important role in the organization of the
bruchid guild in mesquite, by
allowing~·
prosopis to be the
dominant bruchid in the guild because of its secretive
oviposition behavior.
Oviposition behavior has been shown
to be important in other bruchid populations in desert
ecosystems (Mitchell 1977).
In conclusion, parasitoids may play a very major role in
the bruchid-mesquite ecosystem.
These data point toward
both organizational and regulatory roles for the parasitoid
populations and especially for the population of egg
parasitoids.
175
LITERATURE CITED
Bridwell, J.C. 1918. Notes on the Bruchidae and their
parasitoids in the Hawaiian Islands.
Proc. Hawaiian
Entomol. Soc. 3:465-509.
Fujii, K. 1983. Resource dependent stability in an
experimental laboratory resource-herbivore-carnivore system.
Res. Popul. Ecol. Suppl. 3:15-26.
Hassell, M.P. 1978. The dynamics of arthropod predator-prey
systems. Princeton University Press, Princeton.
Kistler, R.A. 1979. A simple host-parasitoid system: An
examination of factors contributing to stability. Unpub.
M.S. Thesis, Purdue University, West Lafayette, Indiana,
108pp.
Lawton, J.H. 1978. Host-plant influences on insect
diversity: the effects of space and time.
Symp. R. Entomol.
Soc. London 9:105-125.
Lawton, J.H. and D.R. Strong. 1981. Community patterns and
competition in folivorous insects. Am. Nat. 118:317-338.
Mitchell, R. 1977. Bruchid beetles and seed packaging by
Palo Verde.
Ecology 58:644-651.
176
Price, P.W. 1983. Hypotheses on organization and evolution
in herbivorous insect communities.
pp. 559-595, In: R.F.
Denno and M.S. McClure (eds.). Variable plants and
hervbivores in natural and managed systems, Academic Press,
New York.
Price, P.W., C.E. Bouton, P. Gross, B.A. McPheron, J.N.
Thompson and A.E. Weis. 1980. Interactions among three
trophic levels:
Influence of plants on interactions between
insect herbivores and natural enemies. Annu. Rev. Ecol.
Syst. 11:41-65.
CHAPTER 6
GENERAL DISCUSSION
177
178
Recent discussion in ecology has re-emphasized that
single factor explanations for patterns in nature are highly
unlikely.
Instead, a multiplicity of factors more than
likely leads to adaptation of organisms to their ecological
and evolutionary settings.
Although such an answer is not
extremely pleasant to ecologists whose goal has been to
search for pattern in natural systems, the current
questioning of long standing ecological paradigms is leading
to new approaches to answering ecological questions.
The
importance of physiological responses to resources and the
environment (Mitchell 1983, Kistler 1982), the organization
and interaction of communities (Lawton and Strong 1981,
Price 1983), the importance of variation within a resource
(Whitham 1981, Thompson and Price 1977), the real meaning of
generalism versus specialism in ecological communities
(Cates 1981), and the role of all three trophic levels in
ecological communities (Price et al. 1980), have all been
examined with a view towards determining their relative
importance in communities of plants and animals and their
importance as general factors explaining the patterns we see
in natural ecosystems.
This research examined a three trophic level desert
ecosystem consisting of the seeds of Prosopis velutina, a
four species guild of seed predators, and a complex guild of
parasitoids of the seed predators.
The study specifically
addressed the importance of environmental variability on
both seed_ production and on the physiology and community
179
organization of the guild of seed predators, the impact that
such variability has on the population dynamics and guild
structure of the seed predators, and the important roles
played by the guild of parasitoids in both limiting the seed
predator guild and structuring species abundances within the
bruchid guild.
This type of intensive study, combining
field observations and experiments as well as laboratory
experiments, and examination of all three trophic levels
should lead ecologists to explanations of natural patterns
of community organization and interaction in insect-plant
communities.
Variability in seed production was very prominent in the
six populations of Prosopis velutina examined.
Alternate
year pod and seed production resulting from an interaction
of energy and nutrient limitations and the cost of
reproduction, accounted-for a large part of the
interpopulation variability.
Varying levels of reproductive
synchrony within the different populations occurred mainly
as a result of the highly variable abiotic environment found
in these desert ecosystems and indicated little selection by
seed predators for such strategies as synchronous predator
satiation.
Instead, the high variability of seed production
within populations and within individual trees points
towards the existence of an energy and nutrient threshold,
which must be exceeded by individual trees or tree parts
every year in order to reproduce successfully.
Above this
threshold, individual plants allocate different amounts of
180
energy or nutrients to production of pods and seeds,
dependent upon abiotic factors and the recent reproductive
history of the individual plant.
Since experiments were not
used to examine limitations on seed production occuring at
the flowering stage, the environmental and energy limitation
hypothesis for seed production in mesquite is only one
possibility which is most strongly supported by these data.
The real reproductive strategy may be a more complex
combination of flowering strategies based on male versus
female fitness, pollinator interactions, dispersal agent
interactions, and environmental and energy limitations.
The high level of variation at the seed population level
did have significant importance for the upper trophic
levels.
High variation between populations means that seeds
are a very unpredictable resource at the local level.
Thus,
bruchids were unable to build up high local populations.
Similarly, the within-tree and within-pod variation made it
difficult for the foraging bruchids to locate an appropriate
resource seed in which their offspring could successfully
develop.
Thus, variability in the plant population may
actually act as a defensive strategy against the guild of
seed predators.
Furthermore, this variability did not seem
to have a large negative impact upon the parasitoid
populations, prpbably because of the extreme generalist
nature of these parasitoids which attack a wide variety of
bruchids in other host plants in the ecosystem.
181
The bruchids within the mesquite seed predator guild
were also differentially limited by abiotic factors, such as
temperature-moisture relations in this harsh, unpredictable,
desert ecosystem.
The distinctly different adaptations to
temperature variation exhibited by the four species of
bruchids were strongly related with species abundance and
success.
Temperatur~
was one important factor in
determining community organization within this guild.
Parasitoids also acted in a differential manner to aid in
structuring the bruchid community and limiting overall
populations of the seed predator guild.
The dominance of
Algarobius prosopis in the guild was mainly a result of
successful adaptation to the variable abiotic factors and to
parasitism by trichogrammatid egg parasitoids.
Vari.abilty
in the seed resource, abiotic factors, and parasitoids all
acted in concert to maintain populations of bruchids below
levels at which they might become important as selec.tive
agents on reproductive strategies of mesquite over
evolutionary time.
The key factor analysis clearly supports
the relative unimportance of this entire guild of seed
predators.
When compared to the other pre-predation ovule
and seed mortality factors which affect plant reproductive
output, the bruchid guild is the least important mortality
factor.
There is a very complex community of parasitoids in the
mesquite-seed predator system.
The complexity of this third
trophic level community indicates the importance of this
trophic level as a potential plant defense through
182
limitation and/or regulation of the seed predator community.
The extreme generality of most of the parasitoids in the
guild (most species attack bruchids in at least two other
host plants in the Verde Valley) .allows more constant
population dynamics at the third trophic level than would be
likely for specialists on rare mesquite bruchids.
Thus
parasitoids may act as a community defense (Attsat and
O'Dowd 1976).
Within the mesquite bruchid guild, egg
parasitoids may act as an organizing factor, allowing A.
prosopis to be the most abundant bruchid as a result of the
failure of the other species to respond to the extremely
high levels of egg parasitism.
These egg parasitoids are a
good defensive mechanism for mesquite seeds and so factors
that select for attack by egg parasitoids, such as pods free
of crevices (Janzen 1969), which forces the bruchids to lay
their eggs on the exposed surface of the pod, or shelter
from desiccation provided by the maintenance of leaves
throughout the summer, might be expected in desert trees
(Mares et al. 1977).
This study was not successful in
addressing this question of whether trees attempt to attract
and maintain populations of parasitoids as a plant defense,
but the possibility remains.
Trees would be less likely to
select for the presence of larval parasitoids since the seed
has been killed by the time the parasitoid has killed the
bruchid larvae, but the tree might still select for these
parasitoids as a general defense, limiting overall seed
destruction by bruchids.
183
This study of a three trophic level ecosystem thus
supports idea that there is no single factor structuring
intertrophic and intratrophic level interactions and
community organization.
Instead a complex suite of factors
ranging from environmental limitation of all trophic levels
to intertrophic level interactions may all be equally
important in structuring this desert ecosystem.
184
LITERATURE CITED
Atsatt, P.R. and D.J. O'Dowd. 1976. Plant defense guilds.
Science 193:24-29.
Cates, R.G. 1981. ·Host plant predictability and the feeding
patterns of monophagous, oligophagous, and polyphagous
insect herbivores.
Oecologia 48:319-326.
Janzen, D.H. 1969. Seed-eaters versus seed size, number,
dispersal and toxicity.
Ecology 23:1-27.
Kistler, R.A. 1982. Effects of temperature on six species of
seed beetles (Coleoptera: Bruchidae: an ecological
perspective. Ann. Entomol. Soc.
Lawton, J.H. and D.R. Strong.
Amer. 75:266-271.
1981. Community patterns and
competition in folivorous insects.
Am. Nat.
118:317-338.
Mitchell, R. 1983. Effects of host-plant variability on the
fitness of sedentary herbivorous insects. pp343-371, In:
R.F. Denno and McClure (eds. ), Variable plants and
herbivores in natural and managed systems, Academic Press,
New York.
Price, P.W., C.E. Bouton, P. Bross, B.A. McPheron, J.W.
Thompson, and A.E. Weis. 1980. Interactions among three
trophic levels: Influence of plants on interactions between
insect herbivores and natural enemies. Annu. Rev. Ecol.
Syst. 11:41-65.
185
Price, P.W. 1983. Hypotheses on organization and evolution
in herbivorous insect communities.
Denno and McClure (eds.)
pp. 559-593, In: R.F.
Variable plants and herbivores in
natural and managed systems.
Academic Press, New York.
Thompson, J.N. and P.W. Price. 1977. Plant plasticity,
phenology, and herbivore dispersion: wild parsnip and the
parsnip webworm. Ecology 58:1112-1119.
Whitham, T.G. and C.N. Slobodchikoff. 1981. Evolution by
individuals, plant-herbivore interaction and mosaics of
genetic variability: the adaptive significance of somatic
mutations in plants.
Oecologia 49:287-292.