and Euterpe edulis (Arecaceae - Instituto Nacional da Mata Atlântica

Transcrição

BOL. MUS. BIOL. MELLO LEITÃO (N. SÉR.) 19:05-30 MARÇO DE 2006
5
Association of non-herbivore wasps (Hymenoptera)
with leaves of Ctenanthe lanceolata (Marantaceae) and
Euterpe edulis (Arecaceae)
Alexandre P. Aguiar1*, Jéssica S. Freitas1
and Antonio C. C. Macedo1,2
ABSTRACT: A comparative analysis for parasitoid Hymenoptera visiting the
structurally contrasting leaves of Ctenanthe lanceolata (Maranthaceae) and
Euterpe edulis (Arecaceae) is presented. A total of 193 hours of observation
and 199 sampled plants yielded 569 parasitoid specimens, in 18 families,
representing 297 morphospecies. Braconidae, Diapriidae, and Scelionidae were
the most abundant and most speciose families, showing sensible differences in
the way they use each plant species. The number of specimens and
morphospecies per family was significantly different from expected values,
suggesting a particular faunistic structure of parasitoid wasps associated with
leaves of C. lanceolata and E. edulis. The suitability of the leaves as landing
substrate, and their potential in retaining water and hemipteran honeydew
droplets, are suggested as main possible reasons for the associations. Absolut
wasp diversity, in number of species, is similar for each plant species, but the
species are different, and similarity indices pointed to significant faunistic
differences between them, even if all singletons are excluded from the analyses.
Sex-related preferences for leaves of C. lanceolata or E. edulis were detected
to Braconidae, Diapriidae, Scelionidae and Encyrtidae, as a whole or for
particular taxa. Data for morphospecies with aggregation tendencies, particularly
in Braconidae and Diapriidae, also point to a differential utilization of each leaf
type. Evidence ultimately indicate that leaves of C. lanceolata and E. edulis
are not randomly visited or utilized by parasitoid wasps, but by functional species
assemblages.
Key-words: Guild, parasitoid, behavior, Palmae, Neotropical.
Museu de Zoologia da USP. Av. Nazaré, 481, São Paulo, SP, 04263-000
Programa de Pós-Graduação em Entomologia FFCLRP-USP
*Corresponding author: Alexandre Pires Aguiar, Universidade Federal do Espírito Santo,
Departamento de Biologia, Av. Marechal Campos 1468, Vitória, ES, Brasil, CEP 29040-090
1
2
6
AGUIAR ET AL.: ASSOCIATION OF NON-HERBIVORE WASPS WITH LEAVES
RESUMO: Associação de vespas não herbívoras (Hymenoptera) com
folhas de Ctenanthe lanceolata (Marantaceae) e Euterpe edulis
(Arecaceae). O trabalho apresenta uma análise da associação de vespas
parasitóides com as folhas estruturalmente contrastantes de Ctenanthe
lanceolata (Maranthaceae) e Euterpe edulis (Arecaceae). Um total de
199 plantas amostradas em 193 horas de observação resultou em 569
espécimes de parasitóides, em 18 famílias, representando 297
morfoespécies. Braconidae, Diapriidae e Scelionidae foram as famílias mais
abundantes e com maior riqueza de espécies, mostrando sensíveis diferenças
no uso de cada espécie de planta. O número de espécimes e de
morfoespécies por família foi significativamente diferente de valores
conhecidos para a Mata Atlântica, sugerindo uma estrutura faunística
particular para parasitóides associados às folhas de C. lanceolata e E.
edulis. A adequabilidade das folhas como substrato de pouso e para a
retenção de água e secreções açucaradas de homópteros são considerados
possíveis motivos para as associações. Cada espécie de planta foi visitada
por cerca de 180 espécies de vespas, mas os índices de similaridade foram
significativamente diferentes, mesmo se desconsideradas as espécies
representadas por um único indivíduo. Diferenças de preferência entre sexos
por folhas de C. lanceolata e E. edulis foram detectadas para Braconidae,
Diapriidae, Scelionidae e Encyrtidae. Dados sobre tendência de agregação,
particularmente em Braconidade e Diapriidae, também sugerem utilização
diferencial de cada tipo de folha. As evidências indicam que folhas de C.
lanceolata e E. edulis não são visitadas aleatoriamente por vespas
parasitóides, mas sim por conjuntos funcionais de espécies.
Palavras-chave: Guilda, parasitóide, comportamento, Palmae, neotropical.
Introduction
The use of leaves or foliage by Hymenoptera for purposes other than
feeding has received limited attention as an independent research subject. The
most commonly described associations are with ants, which, perhaps in function
of its predominantly apterous condition, are not only abundant in the vegetation,
but also use it in multiple and even sophisticated ways. For example, as material
for constructing nests, by rolling leaves in their branches, and sewing them
with silk (Hölldobler & Wilson, 1983); or even to the point of co-evolving with
the plant, as observed with Cecropia spp., with natural cavities to shelter colonies
of Azteca ants, which, in their turn, confer effective protection against herbivores
(Longino, 1991).
BOL. MUS. BIOL. MELLO LEITÃO (N. SÉR.) 19. 2006
7
The nature of the physical association of other arthropods with the foliage
is less well known, but is commonly observed to occur at least on the level of
its use as substrate. In fact, many predatious or saprophagous species explore
the surface of leaves, hunting for prey or searching for carcasses. This is the
case with numerous species of spiders, e.g., all Salticidae, and many insects,
such as the Reduviidae (Hemiptera), and even certain flies of the family
Dolichopodidae, all active predators. Some Opilionida (Arachnida), in special
the Phalangiidae, use the vegetation as their main substrate, patrolling between
leaves in search of dead invertebrates on which they feed. Finally, the imitation
of a leaf shape, texture, or color could perhaps include camouflage as a particular
way of physically utilizing the vegetation for various purposes, such as
ambushing prey, as in Mantodea or Phymatidae (Hemiptera), or hiding from
predators, as many Phasmatodea, and most of the large and arboreous
Tettigoniidae (Orthoptera).
Parasitic wasps are widely known to use visual or olfactory clues from
the vegetation as an aid to locate potential herbivorous hosts (Hanson &
Gauld, 1995); but physical traits of the leaves might be only indirectly
involved with this process, since host localization starts mostly with the
detection of pheromones from an attacked plant, or from the host itself
(Thorpe & Caudle, 1938; Hanson & Gauld, 1995). On the other hand,
laboratory studies suggest that some physical features of plants can reduce
the effectiveness of some parasitoid species, such as high density of
trichomes (Kauffman & Kennedy, 1989; van Lenteren et al., 1995), waxy
leaves (Kareiva & Sahakian, 1990), leaf surface area (Knipling & McGuire,
1968), and complex plant structure (Andow & Prokrym, 1990; Gingras et
al., 2003). Field records, however, are available mostly on the association
of parasitoid Hymenoptera with flowers (van Emden, 1963; Hirose, 1966;
Hassan, 1967; Kevan, 1973; Jervis et al., 1993; Pascarella et al., 2001). In
this case, the association is normally related to the interest of wasps in
gaining access to nectar; even so, some nectar-producing species can be
ignored by the wasps (Syme, 1975). To Jervis et al. (1993), it is not clear
upon which characteristics of the flowers such selectivity is based.
The available literature is, therefore, mostly focused either on laboratory
tests with one or two parasitoid species, or in sampling many plant species at
once, which is insufficient to allow comparisons on how particular vegetation
traits, e.g., plant spatial structure, leaf shape or orientation, may influence wasp
diversity or abundance.
This study is the first result of an ongoing initiative to test the influence of
leaf shapes in attracting parasitoid Hymenoptera, making a direct comparison
of the wasp fauna visiting two contrasting leaf shapes in the Atlantic Forest.
8
The objective of the present study is to provide novel information and insights
on the nature of the association between non-herbivore Hymenoptera with the
folliage, in particular with the leaf surface of understore vegetation, testing the
hypotheses that such association is not fortuitous, and that different plant species
may support distinct parasitoid wasp assemblages on their leaves.
Material and Methods
Study Site and Plant Species. The study site was the Boracéia Biological
Station (EBB), a 96 ha area within a 16,450 ha watershed reserve of Atlantic
rainforest, situated in southeastern Brazil (23º 38´S, 45º 53´W). Boracéia is inserted
in the Tropical Atlantic morphoclimatic domain (Ab´Saber, 1977) at 900 m above
sea level (see Heyer et al., 1990 for a map). Descriptions of the local vegetation
can be found in Travassos & Camargo (1958), Heyer et al. (1990), and Wilms et
al. (1996). The average annual rainfall between 1973 and 1994 was 2024 mm,
and the mean temperature for the same period was 17.9ºC (DAEE, 1994).
The plants C. lanceolata Petersen (Marantaceae) and E. edulis
(Arecaceae) were selected because of their great abundance in all trails,
their contrasting leaf shape (Fig. 1), which could help maximize eventual
faunistic differences associated to this trait, and the abundant fauna of parasitic
Hymenoptera observed on their leaves during preliminary investigations. All
E. edulis specimens sampled were young individuals which could not develop
an inflorescence; many C. lanceolata were adult plants, but showed no
inflorescence either.
The plants were identified by the botanists S. Vieira (ESALQ, Brazil) and
H. B. Q. Fernandes (Museu de Biologia Mello Leitão, Brazil). Both C. lanceolata
(Maranthaceae) and E. edulis (Arecaceae) are native species widely distributed
in the Brazilian Atlantic forest. Structurally, young E. edulis can be similar to
young Geonoma gamiova and Acrocomia sp., other Arecaceae species found
in the EBB by Wilms et al. (1996). Sampling on these species could, in thesis,
have occurred, but the extraordinary dominance of E. edulis in the EBB makes
this possibility unlikely, and of minor concern for the objectives of this study.
Insect Collecting
Insects were collected in five field excursions (collecting dates: 20, 21 and
24 October/2002; 10-12 and 15 January, 27-28 February, 1-4 and 6 March and
17-21 April/2003), at anytime daylight and weather conditions allowed, totalling
9
Figure 1a
Figure 1b
Figure 1. Contrasting leaf shapes between the two sampled plant species. A: Ctenanthe
lanceolata (Maranthaceae); B: Euterpe edulis (Arecaceae).
10
19 days and 193 hours of collecting effort, in four areas selected along three
main trails in the EBB, each one with 1.5-2.0 Km of extension. Only the adaxial
(dorsal) surface of the leaves was checked, and only plants between 30 cm and
1.60 m were considered. The first step consisted of a quick inspection (5-10
seconds) of each and every C. lanceolata and E. edulis plants found along the
way, in search of wasps. Plants with no wasps were ignored, but when a wasp
was observed on a leaf, all leaves of that plant were examined, up to a maximum
of 8 minutes, monitored by a cronometer. All sampled plants received an
identification label, prepared in situ with waterproof ink on a green nylon tape,
fixed around the base of the plant. The codes CT or ED were used, respectively
for specimens of C. lanceolata or E. edulis, followed by a sequential number
(e.g., CT25, ED103). Labelled plants were eventually sampled more than once.
All insects were individually collected by placing 30 ml plastic jars, uniquely
numbered, directly over each specimen. A different jar was used for each
specimen. This method proved to be more convenient than the use of aspirators,
providing also an accurate control of the collected material.
The number of observation hours dedicated to each plant was closely
monitored, and nearly the same sampling effort was employed to C.
lanceolata and E. edulis. Whenever possible, sampling was also done
alternately, that is, after collecting in a C. lanceolata specimen, the attention
was shifted to E. edulis, and vice-versa. All insect specimens were
associated to the individual plant where they were found, by recording, in
the field, the number of the plant and the numbers of the jars with the
specimens collected in that plant.
Identification and Voucher Specimens
Once in the laboratory, the specimens were fixed in 80% alcohol,
dehydrated in 100% ethanol, transfered to Ethyl Acetate, dried, mounted in
triangle points, and labelled. Labels include the field number from the collecting
jars, and the plant species were the specimen was collected. The material was
identified to family level according to the classification of Goulet & Huber
(1993), sorted to morphospecies, and separated according to sex. The use of
morphospecies as a valid strategy for ecological investigations is in agreement
with Oliver & Beattie (1996) and Derraik et al. (2002). Phytophagous genera
known for Braconidae and Eurytomidae were checked for in the studied material,
to certify that these were not included in the analyses. All specimens are
deposited in the entomological collection of the Museu de Zoologia da
Universidade de São Paulo (Brazil).
11
Data Analyses
Species accumulation curves were calculated by randomizing sample order
(Cowell & Coddington, 1994), for both plant species. The number of collecting
days was used in the x-axis, to demonstrate how the number of species increased
with the collecting effort. Total species richness was estimated through first
and second order Jacknife. These calculations were performed by the program
PC ORD for Windows, v. 3.20 (McCune & Mefford, 1997), which uses a
fixed value of 500 randomizations for species accumulation curves. All other
calculations were performed with the aid of conventional spreadsheets (Corell
QuattroPro v. 8.0). All diversity and comparative indexes, as well as the number
of degrees of freedom and values of t for comparisons between any two values
of the Shannon index, were calculated as explained in Magurran (1988).
Whenever applicable, all analyses were performed in all of the following levels:
whole data; males and females; each plant species; each of the most numerous
or most speciose families; each of the most well represented morphospecies.
Chi-Square (χ2) tests, either for comparing observed and expected values, or
when comparing data in contingency tables, were applied according to Zar
(1996). The observed number of morphospecies per family was compared to
the known number of species per family in the Neotropical region, as informed
by the respective specialists on each group (see Acknowledgements) and
according to Díaz et al. (2002) for the Eucoilidae. The observed number of
specimens per family was compared to results from Atlantic forest surveys of
parasitoid Hymenoptera by Azevedo & Santos (2000) and Azevedo et al. (2002).
The latter authors worked in Atlantic forest areas within the same
morphoclimatic domain of the EBB, doing extensive sweeping of herbaceous
vegetation along trails, thus sampling habitats highly equivalent to those studied
in the EBB. These comparisons helped to test if the wasp fauna visiting C.
lanceolata and E. edulis was different from known or expected proportions
for parasitoid Hymenoptera.
Results
General
A total of 199 plants were sampled, with 569 specimens of parasitic
Hymenoptera collected. From these, 291 wasps were found on 91 plants of C.
lanceolata, and 278 wasps in 108 E. edulis (Table 1). The average number of
specimens per plant is 2.86 (3.20 for C. lanceolata and 2.57 for E. edulis,
12
with a 0.63 difference). Although not sampled, ants, and three other insect
orders, Diptera, Coleoptera, and Hemiptera (including Homoptera), were
frequent on both plant species. Hemiptera, and the families Agromyzidae
(Diptera), Chrysomellidae (Coleoptera) and Coreidae (Hemiptera) are among
the most common herbivores observed on both plants.
Considering all data, males and females were found in nearly identical
numbers. For each plant, however, there is an apparent bias toward females in
C. lanceolata, and a similar tendency for males in E. edulis (Table 1, sr), with
a difference of 0.35 between the sex ratios for each plant. A contingency table
test shows no statistically significant values for this supposed tendency (χ2=
3.58, 0.05<p<0.10), but χ2 was close to the critical value (3.841), which would
be reached with an extra divergence of only 2 specimens. For each plant,
however, chi-square results were lower than the critical value, indicating that
the sex ratio values for the wasps on both C. lanceolata ( χ 2 = 2.00,
0.10<p<0.25) and E. edulis (χ2 = 1.91, 0.10<p<0.25) are not significantly
different from 1:1.
Table 1. Number of parasitoid wasp specimens per sex and plant species, sex ratio, and
proportion of specimens on C. lanceolata and E. edulis (ratio C/E).
Females
Males
Unknown 1
Total
Sex ratio
1
C. lanceolata
E. edulis
Total
C/E
156
132
3
291
1.18
127
150
1
278
0.85
283
282
4
569
1.00
1.23
0.88
1.04
-
damaged specimens
Some significant differences on sex ratio were nonetheless found among
the most abundant families (Table 2), with clearly more males than females
collected for Scelionidae, the males being more frequent on C. lanceolata;
and more males of Diapriidae and females of Encyrtidae on E. edulis.
There are apparently more females of Braconidae in C. lanceolata, but
this result was clearly influenced by the large number of females collected
for one morphospecies, an Alysiinae near Asobara Förster, in this plant; in
fact, if the data for this morphospecies are excluded, the differences become
not significant.
13
Table 2. Number of male and female specimens collected in each plant species, and respective
chi-square values (χ2) for an expected sex ratio of 1:1 (for C. lanceolata and E. edulis)
and for the proportions of males and females between the two plants. Braconidae (b):
numbers obtained excluding data of the Asobara sp. morphospecies, the most abundant.
Significant results at p < 0.05 and 1 degree of freedom are marked with an asterisk (*).
C. lanceolata
Family
Braconidae
Braconidaeb
Diapriidae
Encyrtidae
Scelionidae
F
M
63
35
28
8
8
28
26
44
7
26
E. edulis
χ2
13.46*
1.33
3.56
0.67
9.53*
F
M
35
35
28
21
8
50
45
64
4
14
Both plants
χ2
2.65
1.25
14.09*
11.56*
1.64
χ2
10.59*
0.85
0.31
53.10*
16.85*
Behavioral Notes
Most wasps spent at least a few minutes on the leaves, allowing plenty of
time for notes on their behavior, and for collecting. Ichneumonids showed a
typical cryptine host search pattern, consisting of brief and repeated flights and
walks, covering ample areas. This was almost opposite to the aggregation pattern
observed for some braconids, which was also distinct from the long permanence
of diapriids on the leaves. The Diapriidae were the most rarely disturbed, flying
less frequently than any other group.
A large proportion of the observed wasps walked only rarely on the leaf,
as most of the Braconidae. The Diapriidae, however, were normally found
walking on the leaves, often near or along the margins; many would stop and
stay for some time at the very tip of the leaf. None of the wasps were observed
to move to the abaxial (ventral) surface of the leaves. Leaves covered with
lichens and vegetation fragments were only very rarely used by the wasps.
No conspicuous behavioral differences were noted for the wasps on each
plant species, and no intra- or interspecific behaviors, such as courtship,
territoriality, or host searching, were observed or identified for the wasps on
the leaves of C. lanceolata and E. edulis. Predation of wasps was not observed
either, even though salticid spiders were often present, attacking small flies
and other insects.
Alpha Diversity
The Hymenoptera collected belong to 18 families (Table 3), which are all
known to be primarily parasitoid or hyperparasitoid on other insects. The
14
collected Eurytomidae do not correspond to any of the known Neotropical
genera with phytophagous species.
The four most abundant families, either considering the total number of
specimens or the number of specimens per plant species, were, in descending
order, Braconidae, Diapriidae, Scelionidae and Encyrtidae. The most consistent
differences in abundance were registered for Scelionidae and Ichneumonidae,
both with a considerably superior number of specimens captured in C.
lanceolata. Chi-Square contingency table tests indicate that the proportional
abundances for most abundant families, on Table 3, were significantly different
(p < 0.001) from those in the surveys of Azevedo & Santos (2000) (G = 328)
or Azevedo et al. (2002) (G = 239), who collected in a similar area of Atlantic
Forest by sweep-netting the vegetation.
Table 3. Total number of specimens accumulated for each family on days 2, 6, 12 and at
the final day (19). Az1, number of specimens collected by Azevedo et al. (2002); Az2,
number of specimens collected by Azevedo & Santos (2000); C, total in C. lanceolata;
E, total in E. edulis; C/E, ratio of specimens in C. lanceolata/E. edulis; %, percentage
per family, for day 19. Values for C/E, Az1, and Az2 presented only for families with 10
or more specimens in at least one plant.
No/Family
2
6
12
19
%
C
E
C/E
Az1
Az2
01 Braconidae
02 Diapriidae
03 Scelionidae
04 Encyrtidae
05 Eulophidae
06 Ceraphronidae
07 Ichneumonidae
08 Platygastridae
09 Eucoilidae
10 Mymaridae
11 Pteromalidae
12 Eurytomidae
13 Proctotrupidae
14 Chalcididae
15 Chalcidoidea1
16 Monomachidae
17 Bethylidae
18 Aphelinidae
19 Pelecinidae
3
13
3
1
4
2
1
1
-
14
28
10
2
7
1
2
1
4
2
1
1
1
1
-
88
85
30
31
14
11
8
5
7
8
2
2
1
2
2
1
1
177
166
56
40
27
27
23
11
11
10
7
4
3
1
2
1
1
1
1
31.0
29.1
9.8
7.0
4.7
4.6
4.0
1.9
2.1
1.8
1.2
0.7
0.5
0.4
0.4
0.2
0.2
0.2
0.2
92
74
34
15
15
12
18
5
6
5
4
4
3
1
2
1
-
85
92
22
25
12
15
5
6
5
5
3
1
1
1
1.08
0.80
1.55
0.60
1.25
0.80
3.60
-
1034
264
603
161
658
107
45
-
1207
807
1809
243
471
324
306
-
All families
28
75
298
291 278
1.05
-
-
1
damaged specimens, near Pteromalidae
569 100.0
15
The most abundant families were also the most speciose, although
Encyrtidae ranked higher in number of morphospecies than Scelionidae
(Table 4). The family Diapriidae is notable by having almost half of its
morphospecies registered on both C. lanceolata and E. edulis, while this
ratio ranges between 0-24% for all other families with more than 10 captured
specimens. The number of morphospecies per plant species, however, was
generally similar, either considering each family separately or the total
number of morphospecies registered for each of them (Table 4, column C/
E). The high C/E value for Ichneumonidae departs significantly from the
ratio 1:1, which should be expected if the plants were equally used by the
species of this family.
Table 4. Observed number of morphospecies per family and plant species, and number
of shared morphospecies. C, number of morphospecies on C. lanceolata; C/E and
C&E, ratio C/E and number of morphospecies occurring both in C and E; E, number of
morphospecies in E. edulis; Mspp, total number of morphoespecies; Ntspp, number
of known Neotropical species; %, percentage of C&E in relation to Mspp. Values for C/
E and % shown only for families with 10 or more morphospecies. The asterisk (*) marks
statistically significantly differences for χ2 with p < 0.001.
Family
Braconidae
Diapriidae
Encyrtidae
Scelionidae
Eulophidae
Ceraphronidae
Ichneumonidae
Platygastridae
Eucoilidae
Mymaridae
Pteromalidae
Eurytomidae
Chalcidoidea
Proctotrupidae
Aphelinidae
Bethylidae
Chalcididae
Monomachidae
Pelecinidae
All families
Mspp
Ntspp
C
E
C/E
C&E
%
84
54
29
25
23
19
18
10
8
8
6
4
2
2
1
1
1
1
1
14890
270
472
367
751
16
2896
111
457
286
400
220
95
224
717
438
20
3
48
38
14
17
13
10
14
5
6
4
4
4
2
2
0
0
1
1
0
53
42
19
14
12
12
5
5
4
4
3
0
0
0
1
1
0
0
1
0.91
0.90
0.74
1.21
1.08
0.91
2.80*
1.00
-
17
26
4
6
2
3
1
2
1
-
20
48
14
24
9
16
6
0
-
297
22633
183
176
1.05
62
21
16
A total of 297 morphospecies were recognized, with 183 found only in C.
lanceolata, 176 only in E. edulis, and 62 found on both plant species (Table 5),
with an average 1.9 specimens per morphospecies. Species accumulation curves
indicate the number of morphospecies has not stabilized for either plant (Fig.
2). First and second order Jacknife estimators suggest a total number of wasp
morphospecies between 496-641, with 302-395 for E. edulis, and 318-424 for
C. lanceolata.
Figure 2. Species accumulation curves for wasp morphospecies collected on Ctenanthe
lanceolata and Euterpe edulis in the EBB. Collecting days: 1-3 = 20, 21, 24 October
2002; 4-7 = 10, 11, 12, 15 January 2003; 8-9 = 27, 28 February 2003; 10-14 = 1, 2, 3, 4, 6
March 2003; 15-19 = 17, 18, 19, 20, 21 April 2003.
In spite of this, the observed proportions of morphospecies per family were
significantly different (p < 0.001) from proportions implied by the known number
of species per family, as currently known for the Neotropical region (Table 4),
either as a whole (G = 542) or for the eight families with 10 or more
morphospecies (G = 511). In the latter, the difference remains significant (G =
114) even if the data for Braconidae and Ichneumonidae, the families which
show the most intense differences, are not considered.
A similar number of morphospecies, and similar values for the Shannon
diversity index, were found for both plant species (Table 5). The Simpson
diversity index, however, returned a value two times greater for E. edulis in
relation to C. lanceolata (Table 5). Shannon values were significantly different
at p < 0.001 between C. lanceolata and E. edulis (t = 105.3).
17
Table 5. Number of morphospecies (Total, Exclusive, Shared) per plant, Simpson,
Shannon, and Brillouin diversity indexes, and evenness for the fauna of wasps occurring
in C. lanceolata and E. edulis in the EBB.
Unit
Total
Exclusive
Shared
Simpson
Shannon
C. lanceolata
E. edulis
Both plants
ratio C/E
183
176
297
1.04
121
114
235
1.06
62
-
71.77
149.16
119.22
-
4.85
4.94
5.29
-
Brillouin Evenness
4.16
4.24
4.68
-
0.80
0.82
0.82
-
Particular Cases
Aggregation in Braconidae: For one Alysiinae species, Asobara sp., several
female specimens were collected in groups, which contained few or no males
(Table 6). Females of this species were found together on the same plant in four
collecting events on days 9 (28/February), 10 and 13 (1 and 4/March), on two
different individuals of C. lanceolata, with 2 and 4+2+8 females respectively; one
female and a male were collected together on a C. lanceolata on day 9. Other 10
females (36%) were collected alone. Males were scarce, but also were found
together in the same plant in two collecting events, with 2+3 males on a E. edulis
on day 16 (18/April). In overall, grouped specimens of Asobara sp. were found in
7 of 18 collecting events, or 39%. Females were restricted to C. lanceolata, with
28 specimens captured in 16 collecting events exclusively on this plant; males were
collected from both plants, with 7 specimens obtained in 4 collecting events.
Table 6. Number of specimens for the Asobara sp. (Braconidae), according to individual
plants. CT, C. lanceolata; ED, E. edulis; Nce, number of collecting events.
Plant
Nce
Females
CT16
CT23
CT24
CT25
CT26
CT29
CT33
CT36
CT41
CT42
CT60
CT71
ED73
1
2
1
1
2
3
1
1
1
1
1
1
2
2 (1+1)
1
1
3 (2+1)
14 (4+2+8)
1
1
1
1
2
1
Total
18
28
Males
1
1
5 (2+3)
7
18
Dispersion in Diapriidae
Four morphospecies were represented by two specimens found on the
same individual plant (Table 10), but only a single specimen per plant was
registered for 28 other morphospecies with 2 or more specimens collected.
For one morphospecies, of an unidentified genus of Belytinae, 4 females
and 5 males were found on C. lanceolata, and 6 females and 9 males on
E. edulis. However, except for 2 males on another individual of E. edulis,
all other specimens were collected on a different plant, that is, 24 specimens
in 23 plants.
Table 7. Similarity values between the wasp fauna in C. lanceolata and E. edulis.
Group (a), all mspp. considered; group (b), all mspp. except those with only one
specimen; group (c) all mspp. except singletons and all shared mspp. with only two
specimens. Families listed correspond to the three most abundant. Asterisc (*): numbers
obtained excluding all data relative to Asobara sp.
Wasp taxa
Group (a)
Group (b)
Group (c)
Braconidae
Braconidae*
Diapriidae
Scelionidae
Morisita Horn
0.46
0.50
0.48
0.35
0.39
0.78
0.50
Jaccard
0.22
0.73
0.61
0.20
0.27
0.48
0.24
Sorensen
n
0.36
0.84
0.76
0.34
0.43
0.65
0.39
569
369
327
144
142
166
56
Table 8. Number of exclusive and shared morphospecies per plant, according to
frequency of morphospecies (spms/mspp).
spms/
number of cases in
both
mspp
C. lanc.
E. edulis
plants
01
02
03
04
05
06
07
08
09
10+
104
15
1
1
0
0
0
0
0
0
96
17
2
0
1
1
0
0
0
0
26
6
7
9
7
1
3
1
2
19
Beta Diversity
Considering all data, both plant species harboured a very similar number
of morphospecies, but shared about than 21% of them (Table 5). Most
species were collected only once, with about 100 morphospecies represented
by singletons for each plant species (Table 8); however, 38 morphospecies
were collected two or more times exclusively in each plant species (17 for
C. lanceolata, and 21 for E. edulis), while 62 morphospecies were sampled
once or more on both plants (Table 8). For 16 morphospecies there was a
difference of 3 or more specimens collected in each plant species, 6 of
them with more specimens for C. lanceolata (Table 9, last six mspp.) and
10 with more specimens in E. edulis (Table 9, first ten mspp.); for E. edulis,
most of these morphospecies belong to Braconidae and Diapriidae; for C.
lanceolata, 3 of 6 morphospecies were Scelionidae. Chi-Square values
indicate that frequencies were significantly different from a 1:1 proportion
for four morphospecies, three braconids and one scelionid.
Table 9. Number of specimens for morphospecies with difference of 3 or more specimens
collected per plant species, and corresponding χ2 considering an expected proporton
of 1:1. BR, Braconidae; EN, Encyrtidae; DI, Diapriidae; SC, Scelionidae; IC,
Ichneumonidae. Morphospecies BR19 corresponds to Asobara sp. The asterisk (*)
marks significantly different values for p < 0.05.
Mspp.
C. lanceolata
E. edulis
BR8
BR80
BR58
EN2
DI4
DI53
DI35
DI51
DI55
SC25
SC17
SC11
SC1
IC16
BR19
DI30
1
9
1
1
1
1
1
4
7
5
3
30
4
6
5
5
3
15
5
4
4
4
3
2
1
5
1
χ2
6.0*
5.0*
2.7
3.0
1.5
2.7
1.8
1.8
1.8
1.0
4.0*
2.8
2.7
3.0
17.9*
1.8
20
The faunistic similarity between C. lanceolata and E. edulis, as
measured by three similarity indexes, was generally low or very low, even
when excluding morphospecies represented by singletons, and those with
only one specimen for each plant species (Table 7). Similar results were
obtained with the three most abundant families, although with comparatively
high values for Diapriidae, and consistently low values for Braconidae, even
if disconsidering the data for the supposed Asobara sp. (Table 7), the most
abundant morphospecies, and the one more characteristically associated
with only one plant.
For 13 morphospecies two or more specimens were found in the same
individual plant, once or more times, to a maximum of 5 male specimens of
Asobara sp. on one E. edulis individual, and three occurrences of 2 or more
Asobara sp. in C. lanceolata (Table 10). Groups of two or more males without
females were found nine times; groups of females without males, five times;
males and females were found together in the same plant four times (Table
11). When considered as a whole, this group of taxa also seem to show some
sex-related differences, with more males on E. edulis and more male/female
groups on C. lanceolata (Table 11).
Table 10. Morphospecies found more than once on the same individual plant or in
contiguous plants. CoD, collecting day number(s); mspp, morphospecies; spms,
number of specimens. CE, Ceraphronidae; MY, Mymaridae.
Mspp
spms
BR19

BR80

BR70
BR7
DI41

DI43
DI13
DI51
DI55
CE11
IC16
MY5
SC25
5
3
3
2
3
2
2
2
2
2
2
2
2
2
2
2
2
2
5
1
2
2
2
1
2
2
2
2
1
2
2
Total
42
26
Plant
CoD
2
3
2
1
2
1
2
2
1
-
ED73
CT23
CT26
CT60
ED13
ED92
ED7
CT18
CT77
ED18/19
ED30
CT16
ED55
ED101/102
ED22
CT72
CT11
ED103
12/13
9/13
9/1
13
15/19
19
5
8/9
2
8
9
13
12
17
17
16
7
1
16
-
-
21
Table 11. Sex-related selection of plant species for aggregation. Summary of data from
Table 10. CT, C. lanceolata; ED, E. edulis; C&E, occurrences or number of specimens
both in CT and ED. Superscript letters mark significantly different values for ChiSquare tests considering an expected proportion of 1:1 (p < 0.01).
Wasp
Occurrences
Specimens
sex
CT
ED
C&E
CT
&
3
2
3
6
3
1
8
10
Total
ED
C&E
9
5
4
a
6
5
7
15
6b
3c
21e
11
10e
18
18
24
42
a,b,c
Discussion
Data Representativeness
The present work is not a species inventory, but a comparative assessment
of the wasp fauna on the leaves of C. lanceolata and E. edulis, and as such,
this is the first work to associate a large number of non-herbivore wasps
specifically with plant leaves, with all records representing original information.
The results from analyses with the collector´s curve and Jacknife estimators
can therefore be interpreted as satisfactory for the purposes of this study,
since they indicate that a large proportion of the species visiting C. lanceolata
and E. edulis have been collected. Similar numbers were also obtained by
Jervis et al. (1993), who collected 936 individuals of parasitoid Hymenoptera,
representing 249 species, in flowers of 33 plant species. Such results seem in
fact typical for parasitoid Hymenoptera, particularly in tropical systems. In
Borneo, for example, Stork (1988) collected 1,455 individuals of Chalcidoidea,
representing 739 species; of these, 437 were singletons, only eight had more
than ten individuals, and the commonest species was represented by only 19
individuals. The group is so diverse that even a monoculture field can harbour
a large number of species, e.g., as shown by Jensen & Pewlong (1998), who
recognized 326 species of parasitoid Hymenoptera for 7,159 individuals collected
exclusively in rice paddies, or by Perioto et al. (2002), who collected specimens
of 26 families of parasitoid Hymenoptera in a cotton field.
Structure and Specificity of the Associated Wasp Fauna
Alpha diversity and community profile: Whichever way the results are
22
evaluated, it is clear that numerous species of non-herbivorous wasps visit
leaves of C. lanceolata and E. edulis. Surprisingly, however, no large wasps
(greater than 4 mm) were collected, and groups such as Vespoidea, Sphecoidea,
and Apoidea were entirely absent on all samples. Apparently, this could be
related to the fact these insects see well, and can efficiently detect
approximation, and flee. However, it must be stressed that throughout the nearly
200 hours of observations, none of these wasps were observed, either on C.
lanceolata or E. edulis, suggesting that they in fact may not be associated
with these plants the same way parasitoid wasps seem to be. Large wasps
may also not benefit from the small quantities of water and honeydew that can
be found on leaf surfaces (see below), further helping to explain their absence.
The reasonably constant proportions of morphospecies collected for each
family along the study (e.g., Braconidae and Diapriidae always dominant,
followed by Scelionidae, Encyrtidae and Eulophidae, etc) (Table 3), also suggest
that this frequency structure is well established for the studied plants and area,
and would probably remain the same with further sampling. In other words, the
dominance of Braconidae and Diapriidae does not seem to be an artefact of
collecting biases or undersampling.
The significant differences between the known and observed faunistic
proportions for the families (Tables 3, 4) help to support the hypothesis that the
wasps were not randomly visiting the leaves of C. lanceolata and E. edulis.
Possible faunistic differences between the compared areas are mitigated by
the fact that the numerous species in each family represent multiple biologies,
and that these areas belong to a same morphoclimatic domain, all this making
the family rank highly equivalent in ecological terms. In addition, all compared
families are well established as monophyletic taxa, ensuring their comparative
power.
Also, if the the leaves were used by the wasps entirely at random, then
groups such as Pteromalidae, Eulophidae, and Ichneumonidae, usually dominant
families both in number of species and specimens, would be much better
represented in the samples, instead of appearing only in isolated occasions.
Although Jacknife estimators suggest many more species should occur, it must
be noted that virtually all the wasps seen on the plants were captured, indicating
that all accessible records for this study were actually retrieved and analysed.
Nature of the parasitoid-plant associations: Host searching on the plant
seems unlikely, since the sampled plants were virtually intact, showing no signs
of immediate or past attack by larval herbivores, the most likely hosts. The
observed behaviors also do not fit known host-searching patterns for most
wasps, e.g., as summarized by Hanson & Gauld (1995) and Quicke (1997).
Insect eggs, pupae, or insect products were not observed on the plants either.
23
Insects of several orders were common, but only as adults, stage only rarely
attacked by parasitoid Hymenoptera. Vos et al. (2001), however, demonstrated
that parasitoids may be attracted by infochemicals from leaves containing nonhost herbivores, and then spend considerable amounts of time on such leaves.
It seems therefore difficult to reject that the several herbivores observed on C.
lanceolata and E. edulis could have played some role in attracting and
maintaining the parasitoids on the leaves, independently of representing suitable
hosts or not.
It is also quite evident that the leaves of C. lanceolata and E. edulis
represent suitable substrate for the wasps, a fact which asks for an underlying
reason. Leaf structure has an obvious role: these plants have features which
are locally unique or uncommon, as large size and area, an exposed, smooth,
uniform surface, and high integrity of form, showing little or no damage inflicted
by herbivores. This is very different from the much more frequent but small
leaves of shrubs and trees, often damaged or protected by trichomes. Correlation
between leaf structure with density of herbivorous insects has been registered
for some groups, and Peeters (2002) noted a significant influence of features
such as leaf surface area, leaf shape, and distance between lignified tissues.
For the present work, possible structural influences are further suggested by
the notable preference of the wasps for leaves of both plant species which
were clean, i.e., unobstructed by dirt or lichens.
Feeding might seem, at first, an unlikely reason why non-herbivore wasps
would visit leaves, especially considering that the examined plants had no
flowers or fruits at the time. However, it has long been known that adult insect
parasitoids exploit plants to drink from water droplets or to consume honeydew
deposited by Hemiptera that feed on plants (e.g., Illingworth, 1921; Townes,
1958; Downes & Dahlem, 1987; Idoine & Ferro, 1988), even after the
honeydew dries out on the leaf surface. Although only a few Hemiptera have
been observed on C. lanceolata and E. edulis, their large leaves could easily
receive droplets of honeydew from Hemiptera feeding on the plants above.
The few behavioral observations also concur to the idea that some wasps
could have been drinking or feeding: they would stay and move on the leaves
basically searching for water or honeydew patches.
Finally, parasitoid Hymenoptera may also offer some protection for plants
against herbivores in natural situations (Washburn & Cornell, 1981; Hassell
& Waage, 1984; Hassell, 1985; Weis & Abrahamson,1985; Price & Clancy,
1986). However, while the nearly perfect physical integrity of all C.
lanceolata and E. edulis indicate absence of attack by herbivores,
observations for this work provided no direct evidence that parasitoids actually
had something to do with this.
24
Behavioral clues
Ichneumonids, braconids and diapriids showed distinct behaviors on the
leaves. Although such differences are derived mostly from their distinct
biologies, they nonetheless clearly indicate that the leaves were differently
used by each taxon; in this case, being occasionally visited by cryptines, while
used in specific but prolonged periods by braconids, and continuously explored
by diapriids, indicating that the leaves are differently important for each of
these non-herbivorous groups.
Faunistic Differences Between C. lanceolata and E. edulis
Sex ratio: In spite of the differences between the overall sex ratios for
wasps found on the two plant species (Table 1), it is probably not surprising
that these values were, ultimately, not statistically significant, since this can
result from family-level or species-level differences counterbalancing one
another. In fact, family and morphospecies-level analyses indicated some
consistent or statistically significant differences between the two plant species
(see Table 2, and item Particular Cases), which make good auxiliary evidences
to the hypothesis that the leaves of C. lanceolata and E. edulis are differentially
utilized by parasitic Hymenoptera. Jervis et al. (1993), based on 249 species of
parasitoid Hymenoptera collected on flowers of 33 plant species, also found
sex-related preferences, with females visiting about 75% of the plant species,
while males were more specific, visiting only around 50% of them.
Morphospecies composition: The intense differences between the fauna
of wasps collected on each plant, either as compared in terms of absolute
diversity (Table 5) or similarity indexes (Tables 7, 8), seem, at first, to reflect
the extreme diversity of the parasitic Hymenoptera. This suggests that further
sampling could reveal more mosphospecies occurring on both plant species,
with few of them restricted to one plant or another. However, although a
possible scenario, it is, strictly, only speculation, and therefore cannot discard
the veracity of the observed differences. At the same time, it must be noted
that the detected differences remained significant even when all
morphospecies with only one or two records were entirely disconsidered
(e.g., Table 7). The Morisita-Horn index, in particular, which is among the
most precise quantitative index available (Wolda, 1981), in fact returned
consistently low and similar values in all situations (Table 7), suggesting that
the dissimilarity between the two wasp faunas is real.
When applied only to the most diverse families, morphospecies comparisons
25
between plants show even stronger differences than the previous analysis,
with values for similarity indexes falling within a slightly lower range than those
calculated for the entire data set (Tables 7). Additionally, the notable differences
between similarity values obtained for each family provide also indirect evidence
about plant choice by the wasps: low values for Braconidae suggest that its
species might show a different degree of preference for one plant or another,
while Diapriidae, which yielded the highest similarity value (Table 7), might be
naturally more widely distributed on C. lanceolata and E. edulis than other
families.
Statistically significant differences on the frequency of morphospecies of
Ichneumonidae on each plant (Table 4), and differences observed on the number
of specimens of some morphospecies on C. lanceolata vs. E. edulis, some of
which are also statistically significant (Table 9), strongly suggest that some
wasps do prefer one plant over another. The case of Asobara sp. is also notable.
In addition, the following facts indicate that the detected differences cannot be
attributed to a circumstantial event, such as a group of plants of a same species
visited by a local population of a given wasp species, or numerous individuals
of a same species emerging from its host, etc: (1) all sampled plants of C.
lanceolata and E. edulis where nearly always very close to one another, and
mixed together; and (2) the Ichneumonidae and most morphospecies on Table
9 were collected in several different plants and in several distinct collecting
events (see also Table 6 for Asobara sp.).
The influence of the drastically different leaf shapes and structure between
the studied plants may also have played a role in attracting different groups of
wasps. The influence of plant structural traits in the attraction of parasitoid
wasps has also been proposed by Jervis et al. (1993). Studying parasitoid
Hymenoptera on flowers, these authors found that 67% of over 579 wasp
species were uniquely associated to a distinct plant species, and suggested that
floral morphology would be a key factor. In that study, all Ichneumonidae were
obtained exclusively on Apiaceae, whose exposed nectaries offer easier access
to these large wasps than the narrow tubular corollas of other plants, but all
Braconidae, represented in that study by small species with specialized
mouthparts, showed a clear preference for plants with narrow and tubular
corollas. The intense structural differences on the leaves of C. lanceolata and
E. edulis can, analogously, offer different mechanical limitations or advantages
for different wasp taxa. Peeters (2002) showed that it can happen even with
herbivorous insects, demonstrating that entire species assemblages are
sometimes more strongly related with leaf structure than with leaf constituents.
Aggregation and dispersion: As discussed, parasitoid Hymenoptera in the
tropics are typically found as singletons (see item Data Representativeness),
26
and only very rarely 2 or more individuals are collected together. Because of
this, all cases with 2 or more individuals of a same morphospecies collected on
the same leaf were considered significant, that is, the result of a non-randomic
event.
Data for morphospecies found in groups of 2 or more suggest that some of
them, either as a whole (Table 10), or their males or females (Table 11), may
also show some degree of preference for one plant or another. Data for
Diapriidae (see item Particular Cases, and Table 10), on the other hand, suggest
that both males and females are solitary, and are found highly dispersed on the
plants, that is, they also do not seem to have a preferential plant. Such differences
once more suggest that C. lanceolata and E. edulis are not randomly used by
the wasps, but rather differently selected by distinct wasp taxa.
In conclusion, the analyses show that an extremely rich fauna of parasitoid
Hymenoptera, consisting of at least 300 species, visit and often stay on the
leaves of C. lanceolata and E. edulis. Absolute wasp diversity for each plant
species is equivalent, but the faunistic composition is different for each plant.
The taxonomic structure of the parasitoid wasp fauna visiting C. lanceolata
and E. edulis, in number of species or specimens per family, is significantly
different from published results for the Atlantic Forest as a whole; at the same
time, the Diapriidae and Braconidae were much more closely associated to the
studied plants than any other wasp family. Such preferences seem to have
their origins in the nature of the parasitoid-leaf association, which, in its turn, is
clearly related to the fact that the leaves of C. lanceolata and E. edulis
represent highly suitable substrates for the wasps.
While some parasitoid taxa seem to visit both plants with equal frequency,
part of the associated fauna of wasps clearly show some degree of sex- or
taxon-related preferences, both at family and morphospecies level, for the leaves
of either C. lanceolata or E. edulis. The consideration of all evidences
ultimately indicate that the leaves of C. lanceolata and E. edulis are definitely
not randomly visited or used by parasitoid wasps, which form functional species
assemblages particular to each plant.
Acknowledgments
The botanists Silvana Vieira (ESALQ, Brazil) and Helio de Queiroz Boudet
Fernandes (Museu de Biologia Mello Leitão, Brazil) helped with the
identification of C. lanceolata and E. edulis. Rogério R. Silva helped with
statistical questions; Helen A. Ferreira mounted and labelled part of the collected
specimens; Ana Carolina Arlindo do Rosário and Flávia de Moraes Rodrigues
27
participated in one collecting excursion each. Two anonymous reviewers
contributed with suggestions. Celso O. Azevedo, Norman F. Johnson, Luciana
Musetti, John S. Noyes, Fredrik Ronquist and Michael Sharkey kindly contributed
with updated information on the number of known neotropical species for some
families of Hymenoptera. This work benefited from scholarships provided by
FAPESP (Brazil) directly to the authors (processes 00/05704-6, 02/12173-2,
03/00738-8 and 03/08585-6), and from funds allocated to this work from the
project of C. Roberto F. Brandão (FAPESP process 98/05083-0).
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