Download Food web relationships involving Anadiplosis sp. galls

Revta brasil. Bot. 10:117-123 (1987)
Food web relationships involving Anadiplosis sp. galls (Diptera: Cecidomyiidae) on
Machaerium aculeatum (Legum~nosae)
O. WILSON
FERNANDES'.
ROGÉRIO
P. MARTINSl
and E. TAMEIRÃO
NETOl
ABSTRACT(Food web relationships involving Anadiplosis sp. gal/s (Diptera: Cecidomyiidae) on Machaerium aculeatum
(Leguminosae». The characterization and occurrence of Anadiplosis sp. , new species, (Diptera: Cecidomyiidae) leaf galls on
Machaerium aculeatum (Leguminosae) were studied. The food web centered upon the leaf galls was composed of six species
of hymenopterans (two species of Platygasteridae, two species of Eurytomidae,one
species of Tanaostjgmatidae, and one
species of Vespidae), three species of Berytidae (Hemiptera), one species of Geometridae (Lepidoptera), and three species of
Salticidae (Aranae). The existence of herbivores utilizing galls and causing death to Anadiplosis sp. indicated asymmetrical
competition, a "new" aspect to be explored in gall studies. The intensity of parasitism on Anadiplosis sp. larva was 64,0070
(SD:t 1.4). Galls possess hairs with sticky secretions which trapped and killed insects of several orders, including parasitoids
attacking the gall maker larvat...
RESUMO -(Relações
tróficas envolvendo as galhas de Anadiplosis sp. (Diptera: Cecidomyiidae) ern Machaerium aculeatum (Leguminosae». Foram estudadas a caracterização e ocorrência das galhas foliares de Anadiplosis sp., nova espécie
(Diptera: Cecidomyiidae) em Machaerium aculeatum (Leguminosae). Seis espécies de himenópteros associados (duas espécies d~ Platygasteridae, duas espécies de Eurytomidae, uma espécie de Tanaostigmatidae e uma espécie de Vespidae), três espécies de Berytidae (Hemiptera), uma espécie de Geometridae (Lepidóptera) e três espécies de aranhas Salticidae, compuseram
a teia alimentar baseada nas galhas foliares. A existência de herbivoros utilizando as galhas e causando a morte do cecidógeno sugere competição assimétrica, um "novo" aspecto a ser explorado em estudos envolvendo galhas. A taxa de parasitismo
em larvas de Anadiplosis sp. foi de 64,0070 (D. P. :t 1,4). Pêlos com secreção pegajosa, presentes nas paredes externas das
galhas, foram responsáveis por aprisionar e matar insetos de diversas ordens, dentre eles, parasitóides do cecidógeno.
Key words -Anadiplosis,
herbivory,
insect galls, Machaerium
Introduction
The interest in studies on insect galls, besides
their importance in ethnobotany (Berlin &
Prance 1978, Fernandes & Martins 1985) and
biological control of weeds (Berube 1978, Hartnett & Abrahamson
1979, Peschken 1979,
Peschken et al. 1982), can provide important
contributions to theoretical and evolutionary
ecology. The knowledge of galling insects has
contributed to understanding patterns of community structure, in aspects of three trophic level interactions (host plant -herbivore -enemies
(Price et al. 1980», and in applied ecology
(agriculture, management and conservation of
forest areas). Studies on insect galls are rare for
the neotropical region, notwithstanding the apparent abundance and diversity of these organisms (Fernandes & Martins 1985).
I. Northem Arizona University, Department of Biological
Sciences, P.O. Box 564G, Flagstaff, Arizona 86011,
U.S.A.
2. Departamento de Biologia Geral, Instituto de Ciências
.Biológicas, Universidade Federal de Minas Gerais, Caixa Postal 2486. 30000 Belo Horizonte. MO. Brasil.
aculeatum.
Machaerium aculeatum Raddi (Leguminosae), "jacarandá de espinho", is a tree species
of widespread occurrence in the Brazilian "cerrados" (Hoehne 1941) whose leaf galls have
been described morphologically by Fernandes
et al. (1982, 1987). These galls are caused by a
new species of Anadiplosis sp. (Diptera: Cecidomyiidae, nearA. venustaTavares, R.J. Gagné, personal communication). The description
of this species is currently in preparation. Tavares (1916) described the genus Anadiplosis and
the species A.pulchra and A. venusta. Anadiplosis pulchra were obtained from spherical
leaf ga"s on an unidentified species of Mimo.S'a
(Leguminosae), while A. venusta was also obtained from sphericalleaf ga"s on an unidentified species of Machaerium. Besides these, two
other species, A. caetensis and A. procera, were
described by Tavares (1920): the former in ga"s
of an unidentified legume and the latter in ga"s
of another unidentified species of Mimosa (Leguminosae).
The aim of this study was to describe the
food web centered on Anadiplosis sp. ga"s on
leaves of M. aculeatum and the intensity of
parasitism on the ga" maker by hymenopteran
parasi.toids.
o. w .Fernandes. R.P. Martins & E. Tameirão Neto
118
Material and methods
Galls were observed from August 1980 to December
1982. The great majority of observations occurred between
August and November 1981, when ga11swere most abundant.
In the field. nine host plants bearing galls were labelled .
with flagging tape and samples of 50 to 400 galls were collected from them weekly for the evaluation of attack frequency by gall maker and parasitoids. and for biometric
characterization of the galls. We collected 3.500 galls between August to November. 1981. Due to the low abundance of galls. samples were not taken frequently in 1980 and
1982.
Galls were measured. to the nearest millimete!:. along
their longest axis using calipers. Adults and larvae were
fixed in 70C7/o
ethanol and mounted on slides. Insect specimens were kept in the authors. collection. and at the United
States Department of Agriculture (USDA). Samples of the
plants were deposited in the Herbarium of the Departamento de Botânica of the Universidade Federal de Minas Gerais.
Results and Discussion
Galls were mainly located along the leaf
rachis, and only very rarely occurred on new
stems or leaflets. The number of galls per leaf
was extremely variable (figure 1). When numerous,
galls were aggregated
and displayed
smaller dimensions without the spherical shape
which i§ a characteristic
of single occurence.
200~
~
>
~
IAI
-1
1501
100
~
m:
IAI
G)
2
~
z
50
o
9
~
17
~
2S
33
41
4'
ST
as
7!
NUMBE" OF GALLS
Figure I. Oistribution
Ieaves.
of Anadip/osis
galIs among infected
Anadip/osis
sp. began oviposition
in leaf
buds at the end of August, soon after the emergence and mating of the adults. At this time, M.
acu/eatum was producing new stems and leaves
where the females oviposit. Eggs were laid into
the plant tissues. Eggs hatched a few days later
and the first instar larva entered diapause from
November to early July. After oviposition,
leaf-
lets
were
abscised
and
rachises
became
apparently
dried
and hypertrophied.
Gall
development
begins the following
year before
vegetative development of the host plant (figure
2). Later in the season, we oberved new galls
being developed
on new stems and leaflets.
These galls were morphologically
similar to the
ones developed by the diapausing larvae.
Anadip/osis
galls were found
on host
plants between the months of August and November, coinciding
with the period of vegetative development
of M. acu/eatum.
Due to the
annual periodicity
of growth and leaf initiation
in M. acu/eatum and the fact that galls are induced in undifferentiated
tissues, Anadip/osis
galls are phenologically
restricted and synchronized to the growing season of the host plant.
Insect-host plant phenological
synchronization
may be an important
factor in regulating insect
and plant populations.
The Anadip/osis
life history is completely
synchronized
with the life
history of its host plant. Brewer & Skuravy
( 1980) studied the phenological
synchronization
of a gall former and its host plant and showed
that plants and plant organs avoided massive
attack by the gall former by growing at different rates at any given time. Larval diapause occurs from November to August in leaf rachises
which are apparently
dry and hypertrophied.
We suggest that maintenance
cif diapause, besides occurring in cold and dry conditions, allows
synchronization
of Anadip/osis
adults with vegetative growth of the host plant.
We suggest that the leaflets are selectively
abscised because galled leaves shed their leaflets
much earlier than do ungalled leaves. The apparently dry and hypertrophied
shapes of the leaf
rachises may be related
to the protection
against enemies, but more work is called for to
elucidate the mechanisms and processes involved.
The oviposition carried out in young leaves
is probably related to the ability of these still
differentiating structures to react in a specific
manner to the influences of the galls maker, as
well as to nutrient availability in these growing
organs (Mani 1964, Rohfritsh & Shorthouse
1982). According to Mani (1964), this ability to
react specifically seems to vary with the age and
the stage of development to the affected structure. The ocasional development of galls on
new branches and leaflets may be due to ovipositional mistakes, or to competition for oviposition mistakes, or to competition for ovipositio-
Food web relationships in galls
nal sites with displacement of the less competitive females. Shifts in the host organ attacked
and in the time of attack could eventually lead
to the formation of a new population or race of
Anadip/osis isolated from the prime population
by developmental time and/or behavior. To
answer this question, experimental studies on
the relative abundance of ovipositional sites,
and studies of the behavior and fitness of the
two "populations"
of Anadip/osis should be
performed.
Anadip/osis galls are greenish in color ,
with short hairs' which are distributed alI over
the spherical surface. Hairs are the first structures that appear at the oviposition site. During
119
the early developmental
stages of the gall, small
droplets
of a sticky secretion (from
0.2 to
0.6mm in diameter) are produced at the apices
of the hairs. This secretion ends as the gall maker ends feeding activity.
Once gall development is complete, a small circular area (about
2mm diameter),
which is lighter in color than
the rest of the gall, appears. From this circular ,
portal-area
the adult gall maker later emerges.
Generally, after emergence of adults, the puparium remains in the emergence hole (figure 2).
Subsequently,
the galls dry up and the affected
leaves are abscised.
An average of 10.81 (SD :t 10.24) galls per
leaf were found (range of 1 to 73 galls per leaf,
Figure 2. Life cycle of Anadiplosis, new species, (Diptera: Cecidomyiidae) on its host plant Machaerium aculeatum (Leguminosae). (A) After mating, females oviposit in leaf buds of the host plant. (B) First larval instar enter in diapause from November to August in the apparently dry and hypertrophied leaf rachis. Leaflets are selectively abscised during gall development. .(C) Anadiplosis larva initiate gall formation before vegetative growth begins in the host plant. (D) Cross-section showing larva inside a gall; arrows in D show direction expansion of galls. (E) The adults emerge from a small, circular portal,
area leaving their puparia in the emergence hole.
o. w .Fernandes, R.P. Martins & E. Tameirão Neto
120
n = 308). Figure
I shows the frequency
and/ or consumed by the inquiline larvae which
takes over the gall. Of 1,107 observed gal1s, 706
were parasitized
corresponding
to a total of
64.0OJo (SD :t 1.4) parasitism
in 6 host plants
(table 1). Platygasteridae
species " A" produced
distri~
butiôn of the number of galls per leaf. The same
distributional
pattern of galls among infested
leaves was observed by Washburn
& Cornell
(1979) in Acraspis harta galls on Quercus prinus. The mean diameter of gall size was 5.lmm
(SD ::!: 0.7, n = 1,522, figure 3). Each gall contained a single cavity.with
only one larva in it.
multiple
larvae in each gall parasitized.
An
average of 13.70 (SD :t 5.37, n = 201) Platygasteridae species ' , A' , were reared per A nadiplosis larva. The frequency distribution
of the
number of the Platygasteridae
species " A" per
.00 1/1
:1
.,
...
O
8:
larva of the gall maker is shown in figure 4. For
the remaining
parasitoids,
only one larva per
host was found.
The high percentage of parasitism (table 1)
indicates that parasitism is probably important
in population
regulation of the gall former. The
almost normal distribution
of the number of
Platygasteridae
sp. " A" per larva of Anadiplo-
500
400
300
"'
~
2
j
Z
200
100
o
3,0
3,~
4,0
4,5
~p
5,5
sp
6,5
sis (figure 4) suggests a behavioral variability
in
the pattern of oviposition
'of this parasitoid.
Variation
may be due to positively graded egg
number increasing with host-gall size, effects of
egg depletion over several oviposition
bouts, or
polyembryony.
These possibilities cannot be separated at present.
1,0
DIAMETER(mm)
Figure 3. Oistribution
of leaf gall diameter of Anadiplosis.
Larvae of Anadip/osis are parasitized by
two unidentified platygasterids, and two unidentified eurytomids (Hymenoptera). In addition, at1acks by one species of Tanaostigmatidae have been observed. Most of the New
World tanaostigmatids are gall makers, with
some records of seed infesters (Gomes 1942),
and a few species whose biology is unknown
(LaSalle,
personal communication).
Galls
which are parasitized by tanaostigmatid wasps
are recognizable by their tougher consistency,
larger size and different shape. It has been
shown that some inquilines modify the normal
pattern of gall development (Shorthouse 1973,
1980). No gall maker larva was found in galls
which contained the tanaostigmatid wasp. The
cecidomyiid
larvae are presumably killed
NUMBER
Figure 4. Oistribution
...w
OF
PLATYGASTERIDAE
.w
.w
sp
A
of Platygasteridae sp. " A.. on Ana-
dip/osis larvae.
Table 1. Overall gal1 number and percentage o! parasitized Anadiplosis
PLANT
gal1s.
INDIVIDUALS
OBSERVED*
A
B
c
D
E
F
TOTAL
No. of larvae or galls
examined per plant.
471
168
36
124
38
270
1107
No. and (percentage)
of parasitized
larvae.
274 (58)
115 (68)
18(50)
35 (28)
16 (42}
248 (92)
706 (64)
.Ali
measurements
were taken
during
November
1981
Food web relationships in galls
The phytophagous
hemipterans Jalysus SObrinus, Parajalysus
pal/idus,
and P. spinosus
(Berytidae)
feed on the galls. Previously,
only
adults of P. pal/idus were described, however
without any records of host plant and life cycle
(T. Henry, personal communication).
For J.
sobrinus, only the host Nicotiana
tabacum (Solanaceae) has been described (Wheeler & Schaefer 1982). Females probably
lay their eggs on
the galls of M. aculeatum and the nymphs and
adults feed on gall tissues. The berytids extend
their proboscis and penetrate the gall with the
stylets in order to obtain the fluids contained
therein. This renders the attacked galls softer
than unattacked
ones, and results in the death
of the Anadiplosis
larva. The death of the larva
occurs indirectly through the feeding activity of
these phytophages .
A geometrid
(Lepidoptera:
Geometridae)
larva chews through the gall walls, opening the
larval chamber and causing the larva to fall
from the gall. Larvae which fall from galls presumably die from exposure and/or predation.
Gall tissues are a modified
product of the
host plant which are induced by the gallmaker .
Most of the gall maker life is spent inside these
niodified
tissues. There, the gall maker finds
rich and abundant food, protection
against climatic factors,
and in some cases protection
from natural enemies. However,
galls are not
free from being eaten by other organisms,
or
predators. The gall "predators"
should be considered competitors
of the gall makers, as they
compete with the gall former for the gall resource. The existence of a geometrid
species
and three berytid species utilizing the galls and
causing death to Anadiplosis
indicates a possibility
of
strong
asymmetrical
competition
(Lawton
& Hassel 1981) by these herbivores
against the gall maker. Since the gall maker is
killed by the feeding activity of the competitors,
'Ye believe 1Jlat the dominant species are the ift~~~~hile
the gall former is the subordinate species in the system. The mechanism: by
which the gall maker is excluded from the food
source by the geometrid
is probably
exploitation of resources and habitat modification.
The
interaction
between the berytids and the gall
maker is more difficult
since the Anadiplosis
larva may be killed by habitat modification,
resource exploitation
or by direct aggression and
death. unfortunately,
these interactions
cannot
be cla!ified without extensive additional
work.
Studies of gall communities
may offer num-
121
erous examples of competition
between gall makers, inquilines
and other associated arthropods. This contrasts with the view of Lawton &
Strong (1981), who state that although ants and
bees provide many good examples of competition, competition
for food between phytophagous species is unusual.
One species of Vespidae (Hymenoptera)
preys on the pupae of Anadiplosis
and Platygasteridae sp. ' , A' , .These wasps cut through
the gall walls to reach the pupae of Anadiplosis
and they make multiple cuts in order to obtain
ali the pupae of the Platygasteridae
sp. "A".
After opening the galls and locating the pupae
of Anadiplosis,
these are held with the mandibules and masticated before being ingested. AIternatively,
the wasp might withdraw the pupae
of the Platygasteridae
sp. "A"
from their puparia, before mashing and ingesting them.
Besides this predator, three species of Salticidae (Aranae) (here named Salticidae species
A, B, and C) have been observed which prey
upon both the adults of Anadiplosis
and of Tanaostigmatidae.
A food web based on Anadiplosis galls is shown in figure 5.
The hairs of the galls display sticky secretions that trap insects of several orders, including Diptera,
Hymenoptera,
Homoptera,
Coleoptera and Thysanoptera,
that have an average body size less than 2mm. The most frequent
insects trapped were dipterans, hymenopterans
and homopterans.
Platygasterid
parasitoids of
the gall forming
larvae were frequently
seen
trapped and killed by the hair secretions.
The secretions present in the hairs of most
Anadiplosis
galls may act in the deterrence or
destruction
of parasitoids on Anadiplosis.
Hair
secretions may, by trapping potentially
phytophagous insects of the gall and/or plant, confer
protection
to the gall former as well as to the
host plant. There are examples of galls secreting
substances that can trap small insects (Bequaert
1924, Cornell
1983, Darlington
1975, Mani
1964). The ecological significance of these hair
secretions
to plant and/ or insect protection
may be important
to studies on interactions
among three trophic levels, as proposed by Price
et al. (1980), though little work has been done on this aspect to date (but see Washburn
1984).
Galls are associated with a broad spectrum
of plant taxa, in. ali plant organs, and with
many different
habitats. In addition, they present astonishing variations in morphology,
ana-~
G. w .Fernandes.
122
R.P.
Martins
SALTICIDAE
SAL TICIDAE
sp.
& E. Tameirào
Neto
SD. A
B
SAL TICIDAE
""'I"-_/
ANADIPLOSIS
sp.
C
sp.
(adult)
MACHAERIUM
ACULEA
TUM
(host plant)
PARAJALYSUS
PALLIDUS
-
GEOMETRIDAE
VSUS
VESPIDAE
SPINOSUS
~,
JALYSUS
1:;
1:.::;:;:;:;:.:;;;:;:
ANADIPLOSIS
~
:!i!!!i!iJii[
/00
~
SOBRINUS
sp.
? (larva)
::;;;:;;:'
':;:;:;:;;;;;;:
/~
EURYTOMIDAE
sp.
A
EURYTOMIDAE
sp. B
\
PLATYGASTERIDAE
sp.
A
T ANAOSTIGMA
Fjgure 5. Food web based upon
and platygasterjds
are Anadiplosis
Anadiplosis
predator
\
\
PLA TYGASTERIDAE
sp.
B
TIDAE
sp. leaf galls on Machaerium
and parasjtojds.
respectively.
aculeatum.
Observe that the vespids. eurytomids
while1he berjtids and geometrjd
larvae are actually
feeding on gall tjssue. hence bejng here calledcompetitors
of the gall forming
{)n thp a"ll ti"",IP 1."n1icl linp) "ncl n{)""ihlv
c{)n",lmp"
thp a,,1I f{)rmina
in"pct
cecidomyjjd.
I"rv" (rl""hpci
The tanaostigmatjd
linp)
species feeds
Food web relationships in galls
tomy,
chemistry,
seasonality
and ecology,
which makes the study of the gall maker/gall
complex
and their associated
organisms
of
great interest in the developmen.t of evolutionary and applied ecology.
Acknowledgements -The
authors wish to thank J.M. Ferrari (Botany Department -U.F.M.G.)
and L. Kinoshita
(Herbarium of the University of Campinas), for the determination of M. aculeatum; R.J. Gagné(U.S.D.A.)
for the
determination of Anadiplosis sp.; A.A.P. Fidalgo (Fundanción Miguel Lillo, Tucumán -Argentina) for the family
determinations of the hymenopteran parasitoids; T. Henry
(U.S.D.A.) for the determination of Berytidae; J. LaSalle
(University of California -Riverside) for helpful information on the Tanaostigmatidae; J .H. Kirkbride and v. Rudd
for information on M. aculeatum; to draughtsmen J. Bittencourt Neto and T. Dougi, for the drawings. In addition,
we wish to thank R. Bronner, T. Craig, P .W .Price. C. Sacchi. R. Woodman. and to an annonymous reviewer for their
criticisms and assistance with the English language during
the preparation of this manuscript. Also, we thank the Departamento de Biologia Geral, ICB-U.F.M.G.,
for general
support, and the Ralph M. Bilby Research Center, N.A.U.
for providing the facilities.
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