bioecology of oncideres ocularis thomson (coleoptera: cerambycidae) on acacia mangium willd....
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Bioecology of Oncideres ocularis Thomson (Coleoptera:Cerambycidae) on Acacia mangium Willd. (Fabaceae)Author(s): Pedro Guilherme Lemes, Norivaldo dos Anjos, and Isaac R. JorgeSource: Journal of the Kansas Entomological Society, 86(4):307-317. 2013.Published By: Kansas Entomological SocietyDOI: http://dx.doi.org/10.2317/JKES121121.1URL: http://www.bioone.org/doi/full/10.2317/JKES121121.1
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Bioecology of Oncideres ocularis Thomson (Coleoptera: Cerambycidae)on Acacia mangium Willd. (Fabaceae)
PEDRO GUILHERME LEMES,1,2 NORIVALDO DOS ANJOS,1 AND ISAAC R. JORGE3
ABSTRACT: Twig girdlers are beetles that girdle branches and trunks of living trees so that
they can deposit their eggs in incisions made by their mandibles. There are few studies about
the biology and ecology of the girdler Oncideres ocularis Thomson, which is considered a
potential pest of forest plantations that can cause injuries to tree species of the family
Fabaceae. The objective of this study was to increase knowledge related to the biological
phases and the ecological patterns of girdling and oviposition of O. ocularis. Field studies were
conducted at four plantations of Acacia mangium Willd located in the cities of Coimbra and
Vicosa, State of Minas Gerais, Brazil. The incubation period of eggs was 12.1 6 0.2 (SE) days
and viability was 61% (n 5 70). The number of egg incisions per girdled branch was 17.27 6
1.0. The great number of eggs was laid in the mid-basal and middle sections of branch with a
mean of 5.80 6 0.38 and 4.97 6 0.3 eggs on these portions. The base diameter of the girdled
branches was 9.88 mm 6 0.18 and the mean length was 99.21 cm 6 2.23. A girdled branch by
O. ocularis led to an average loss of leaf area of 4233.05 cm2 per tree that corresponds to 0.46%
of total leaf area. Other beetles that emerged from the girdled branches were Engyum
quadrinotatum (Thomson), Orthostema abdominale (Gyllenhal), Nesozineus bucki (Breuning)
and Lepturges sp.
KEY WORDS: Twig girdler, oviposition patterns, foliar loss, branch girdling
The subfamily Lamiinae (Coleoptera: Cerambycidae) contains several members of
economic and ecological importance know as twig girdlers (Linsley, 1959; Calderon-
Cortes et al., 2011). Females girdle branches with their mandibles, and then insert
their eggs between the bark and wood (Rice, 1989; Rice, 1995; Lemes et al., 2011).
One of the beneficial outcomes of this behavior is the enrichment of the wood with
nitrogen. The girdling stops the flow of nutrients from the branch to the tree. All that
is produced by photosynthesis on the leaves becomes trapped in the branch
(Forcella, 1982).
The twig girdler genus Oncideres is found only in the western hemisphere with
species ranging from Argentina to the southern United States (Hovore and Penrose,
1982; Rice, 1989; Di Iorio, 1996). In Brazil, the species of this genus are widely
distributed, having been recorded in all the regions (Peres Filho et al., 1992; Witeck
Neto and Link, 1997; Martins and Galileo, 2009; Cordeiro et al., 2010a; Lemes et al.,
2012).
Oncideres ocularis Thomson, 1868, can be considered a potential threat to forest
plantations, as it damages several tree species of the family Fabaceae, e.g., the black
wattle (Acacia mearnsii De Wild.), Acacia bonariensis Hook. & Arn. and
Pithecolobium sp. Mart. in southern Brazil (Vulcano and Pereira, 1978; Marinoni,
1 Departamento de Entomologia, Universidade Federal de Vicosa, Av. P.H. Rolfs, s/n, Centro, Vicosa,
Minas Gerais, Brazil2 Author for correspondence. E-mail: [email protected] Departamento de Engenharia Florestal, Universidade Federal de Vicosa, Av. P.H. Rolfs, s/n, Centro,
Vicosa, Minas Gerais, Brazil
Accepted 17 May 2013; Revised 22 October 2013
E 2013 Kansas Entomological Society
JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY86(4), 2013, pp. 307–317
1979). This girdler is distributed from Argentina to southern and southeastern Brazil
(Vulcano and Pereira, 1978).
So far few studies have been conducted on O. ocularis with the exception of lists of
host plants and distribution in Brazil (Baucke, 1957; Baucke and Bertels, 1966;
Marinoni, 1979). Vulcano and Pereira (1978) briefly described the caracteristics of
the adults of this insect, as well as their the distribution and the host plants they
inhabit. This species is very similar to O. impluviata (Germar) (Martins, 1981). In
those studies, the difference between the two species was highlitghted, as seen in the
white pubescence on the sides of the metasternum. In the case of O. ocularis it
extends to the sides of the mesosternum. They often occur in the same regions and O.
ocularis is harder to be found (Baucke, 1957). Dillon and Dillon (1946) also
described the adult males and females of O. ocularis, although the other phases (e.g.,
larval stage) were not characterized. Hence, there is limited knowledge regarding the
biological stages of this insect.
The objective of this study was to increase the scientific knowledge on the
biological characterization of the life stages and the ecological patterns of girdling
and oviposition of O. ocularis.
Material and Methods
Study Site
Field studies were conducted from November 2009 to March 2011, in four areas.
The first, a commercial plantation of Acacia mangium Willd. in Coimbra, Minas
Gerais (20u519240S, 42u489100W, altitude 720 m, mean annual temperature of 19uCand mean annual rainfall between 1300 and 1400 mm) with 3000 trees, 65 months
of age, contour planted on a slope and spaced 3 3 2 m apart. Two other planting
areas were nearby, with approximately 300 trees of A. mangium, around 30 months
of age. The fourth planting site included a consortium of hybrid clones of
Eucalyptus urophylla S.T. Blake 3 E. grandis W. Hill ex Maiden, 60 trees of A.
mangium and Brachiaria spp. located at Vicosa, Minas Gerais (20u459S, 46u519W,
altitude 689 m, mean annual temperature of 19uC and mean annual rainfall of
1221 mm).
Between November 2009 and March 2010, and November 2010 and March 2011,
the areas were visited weekly to assess the damage and injuries caused by O. ocularis,
by collecting the freshly fallen or hanging branches due to the girdling action of the
beetle.
Laboratory Study
The laboratory study was conducted in the Universidade Federal de Vicosa,
Minas Gerais, Brazil. The taxonomist Prof. Dr. Ubirajara Martins, from the
Museum of Zoology, Universidade de Sao Paulo (MZUSP), in Sao Paulo, Brazil,
determined the species of the twig girlder. Adult specimens are deposited at that
institution.
Field Study
Oncideres ocularis adults and girdled branches were collected on visits to the four
plantation areas, to characterize the season of occurrence and activity period. The
insects collected were preserved in 70% alcohol.
308 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
Egg
Eggs of this beetle were removed from freshly girdled branches of A. mangium to
determine the color, shape, dimensions and incubation period. Measurements were
obtained using a magnifying glass equipped with an ocular micrometer. These eggs
were kept in petri dishes (10 cm diameter and 2 cm height) with distilled water-
moistened filter paper and marked with the laying date. They were maintained under
controlled conditions (temperature: 25uC, relative humidity: 43.8 6 0.8%, and
photophase/scotophase: 12/12 hr). Verifications and notes were made daily to
determine the incubation period and egg viability. When the branches were openedto remove the eggs, the number of eggs was counted per incision.
First Instar Larvae
The larvae were described with the larvae hatched from these eggs. The color, type
of larvae, length and greatest body width (prothorax) and the greatest width of the
head capsule were determined using the ocular micrometer.
Oviposition Patterns
The number of egg incisions was counted for the freshly girdled twigs. The
preferred position for incision was determined by counting the incisions for each of
the fifth part of the branch length (basal, mid-basal, median, mid-apical and apical).
The mean number of incisions and their distribution in each section weredetermined. The means were subjected to Tukey’s test, a 5 5%, using the software
Statistica 9.0 (Stat Soft. Inc., 2009).
Oncideres ocularis Injuries
The girdling diameter of the branches was measured with digital caliper and the
length with millimeter tape to characterize the injuries done by the O. ocularis adults.
The leaves of the freshly girdled branches were counted and their area measured
with a TMK2 leaf area meter (Delta-T Devices, Burwell, Cambridge, England) to
ascertain the leaf area lost in each girdled branch. The mean leaf area lost per girdledbranch was compared with the mean leaf area of a tree of A. mangium of the same
age to obtain the percentage of leaf loss due to a single girdling.
Insects Co-Inhabitating the Girdled Branches
The branches collected from the plantations in Coimbra-MG were stored in
transparent plastic bags (90 3 60 cm) and sealed with some air inside. The branches
were checked weekly from the plastic bags for the presence of any other insect that
emerged from them. Then they were watered, replaced in the bags and maintained in
a room with temperature and relative humidity equal to 23.1 6 0.4uC and 89.4 6
0.6%, respectively.
Adult Cerambycidae were sacrificed, fixed and sent for determination to taxonomist
Prof. Ubirajara Martins. The other insects were identified up to family level.
Results
Egg
The newly laid O. ocularis eggs are white in color (MunsellH Soil Color Name
Diagram: 2,5 Y 8/1), with a smooth-surfaced chorion, elongated ellipsoid of
VOLUME 86, ISSUE 4 309
revolution shape, and about four-times longer than wide with a slight depression in
the center (Fig. 1A). The eggs became pale yellow due to the color of the larvae
within.
The mean values for the maximum length and width of the eggs were 2.44 6
0.02 mm, ranging from 1.92 to 2.78 mm, and 0.58 6 0.12 mm, with an amplitude of
0.41 to 0.76 mm, respectively. The incubation period of the eggs varied from 10 to
15 days, with a mean of 12.1 6 0.2 days and the egg viability of O. ocularis was
60.78%. It was found that there was only one egg laid per incision.
First Instar Larvae
The newly hatched larvae of O. ocularis are pale yellow (Munsell SoilH Color Name
Diagram: 2.5 Y 8/3), is type cerambyciform, legless, with short, brownish jaws, head
protruding and retracted into the prothorax, rigid calcareous plate in the dorsal
prothorax, body with short hair laterally, although with greater amount on the last
abdominal segments, culminating with most hair on the anal segment (Fig. 1B).
The mean body length of the O. ocularis larvae was 1.90 6 0.03 mm, minimum
and maximum length being 1.50 and 2.59 mm, respectively. The greatest body width
was 0.61 6 0.01 mm with a minimum of 0.50 mm and maximum of 0.71 mm. The
mean head capsule width was 0.35 6 0.01 mm, with a minimum of 0.25 and
maximum of 0.50 mm.
Fig. 1. A) Egg and B) first instar larval stage of Oncideres ocularis Thomson.
310 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
Activity Period
One hundred and thirty nine branches of A. mangium girdled by O. ocularis were
collected in the plantations in Coimbra, MG. The first was found on December 2010
and the last on March 2011. No signs of adult activity of this insect were seen outside
this time period. A similar period was found in the silvopastoral system in Vicosa-
MG, between 2009 and 2010 (author’s observation). The cycle of this insect is thusseen to be univoltine, with the seasonal occurrence of adults in the hot and rainy
season between December and March.
Oviposition Patterns
The number of incisions per girdled branch was 17.27 6 1.0, with minimum of one
and a maximum of 66. A large number of egg incisions were found in the mid-basal
and middle sections of the branch, with means of 5.80 6 0.38 and 4.97 6 0.33
incisions on these parts of the branch, respectively, comprising about 62.3% of the
total of incisions. The mid-apical and apical portions had fewer egg incisions,
possessing only 15.9% of the total number (Fig. 2).
Injuries Related to Reproductive Behavior
The diameter at the base of the girdled branches was 9.88 mm 6 0.18 (n 5 100)
ranging from 6.56 to 15.66 mm. The mean length of the girdled branches was99.21 cm 6 2.23 (n 5 100), ranging from 44.20 to 180.60 cm.
Just a single branch girdled by O. ocularis, led to an average loss of 35.37 leaves,
which corresponds to a leaf area of 4233.05 cm2 per tree. Whereas an A. mangium
tree at 36 months of age has a mean of 913,291.90 6 344,479.90 cm2 of leaf area in
Fig. 2. Branch sectionwise distribution of number of egg incisions of Oncideres ocularis in girdled
branches (n 5 100) of Acacia mangium. Histograms followed by the same letter did not differ by Tukey’s
test (P , 0.05).
VOLUME 86, ISSUE 4 311
the cannopy (Cordeiro, 2008), can be infered that the mean defoliation caused by O.
ocularis corresponds to about 0.5% of the total leaf area.
Insects Co-Inhabitating the Girdled Branches
From the girdled branches of A. mangium stored in plastic bags, emerged the
longhorned beetles Engyum quadrinotatum (Thomson) (n 5 10), Orthostema
abdominale (Gyllenhal) (n 5 19), Nesozineus bucki (Breuning) (n 5 2) and Lepturges
sp. (n 5 1). Also emerged from the girdled branches coleopterians of families
Buprestidae, Scolytidae and Bostrichidae, whose species has not been determined.
Discussion
Egg
This color and format is similar to the egg of O. rhodosticta Bates (Polk and
Ueckert, 1973). Similar dimension values were reported for O. impluviata eggs in
southern Brazil (Amante et al., 1976) probably due to the taxonomic proximity
existing between the two species. Eggs of O. humeralis Thomson and O. rhodosticta
are bigger (Polk and Ueckert, 1973; Paulino Neto et al., 2006), however, all the
dimensions of the eggs of O. ocularis ranged within the variation observed in the
genus Oncideres.
Coutinho (1997) and Cordeiro (2008) recorded incubation periods for O. saga eggs
within this time interval. Incubation period of eggs of O. humeralis was above this
range, although under field conditions and among Melastomataceae trees (Paulino
Neto et al., 2006). The egg viability found here is less than the value for O. impluviata
(Pedrozo, 1980), who maintained the eggs on the branches and indoors. This
viability value however, is higher than that found for O. cingulata (Say) (Rogers,
1977; Cramer, 1998), may be due to the technique used to obtain the viability.
Only one egg per incision was observed in O. cingulata (Rogers, 1977). Paulino
Neto et al. (2006) found up to three O. humeralis eggs laid in the same incision,
and Cordeiro (2008) found up to two eggs per incision of O. saga Dalman. This
difference may be due to the great wood volume of the branches girdled by these
other species, resulting in increased food intake and reduced intraspecific
competition (Rice, 1989).
First Instar Larvae
This description is similar to first instar larvae of O. impluviata (Germar) (Amante
et al., 1976; Pedrozo, 1980), as well as for O. saga (Cordeiro, 2008), indicating that
this description may be a pattern for first instar larvae of this genus.
The length and width values are similar to those found for O. impluviata (Baucke,
1958), although they are less than those recorded for the O. saga larvae (Cordeiro,
2008). Neonate larvae of O. impluviata grown in branches of Mimosa scrabella had
similar head capsule width (Pedrozo, 1980).
Activity Period
Oncideres humeralis and O. saga has a similar activity period in Sao Paulo state
(Paulino Neto et al., 2006) and Rio de Janeiro state (Coutinho, 1997), respectively.
The activity of O. impluviata in Rio Grande do Sul state begins in mid-November
and lasts up to three months (Baucke, 1958). However, it is interesting to note that
312 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
the twig girlders activity generally occurs during the warmer and rainy months of the
year.
Oviposition Patterns
The number of egg incisions found here is very close to that found for O. impluviata
and O. captiosa in the branches of P. rigida (Benth.) and Cinnamomum camphora (L.)
(Link and Costa, 1993). The value is less than those found for O. saga in the branches
of A. mearnsii De Wild. (Magistrali et al., 2008) and for O. pustulata LeConte in Acacia
farnesiana (L.) Willd (Rice, 1989). The difference could be related to the dimensions of
the branches girdled by those species, which would provide a greater volume of wood
available to feed more offspring. Lower number of incisions were obtained for O.
humeralis in Melastomataceae; O. cingulata in Carya ovata (Mill.) K. Koch and
Prosopis glandulosa (Torr.) Cockerell, respectively (Paulino Neto et al., 2006; Cramer,
1998; Rogers, 1977). Although the number of egg incisions for these species is lower
than for O. ocularis, the range is quite similar. The number of incisions that this twig
girdler has made is similar to most species of this genus.
The greatest number of incisions of O. impluviata in the branches of P. rigida Benth.
was between 0 and 20 cm from the base of the branch (Link and Costa, 1993), similar
to the incisions made by O. pustulata (Rice, 1989), where they were concentrated
between 10 and 20 cm from the base of the girdled branch. Oncideres cingulata lays
eggs from 20 to 30 cm from the girdled base (Cramer, 1998) and O. guttulata Thomson
laid their eggs mainly in the 10 to 25 cm section (Diodato et al., 1997).
The concentration of the egg incisions concentrating in the mid-basal and middle
portions of the branch could be due to the female twig girdlers ensuring that the
larvae have adequate food reserves in any direction they bored. Twig girdlers tend to
lay eggs away from the edges (Paulino Neto et al., 2006). This would explain the
lower number of incisions found in the basal portion of the branch near to the
girdling, as the larvae could reach the girdled tip of the branch. Also, in this portion
of the girdled branch, the wood would dry faster, making the development of larvae
harder (Rice, 1989; Diodato et al., 1997). In the branch portions having a lesser
wood volume (mainly the apical section), intraespecific competition for food would
become greater, and therefore, the twig girdlers tend to lay fewer eggs in these
regions (Rice, 1989). The least number of incisions in the terminal portions of the
girdled branches are generally observed for other species of Oncideres (Rice, 1989;
Link and Costa, 1993; Cramer, 1998).
Injuries Related to Reproductive Behavior
The mean diameter of girdled branches found is similar to that found for O.
impluviata (Link et al., 1994a) and for O. guttulata, O. cingulata and O. rhodosticta
(Diodato et al., 1997; Cramer, 1998; Polk and Ueckert, 1973), but is smaller than
reported for O. captiosa Martins, O. dejeanii, O. humeralis, O. pustulata and O.
ulcerosa (Germar) (Link et al., 1994b, 1996; Link and Costa, 1988, 1994; Rice, 1989).
This twig girdler beetle becomes important for the cultivation of A. mangium,
especially during the first year, when the trunks have smaller diameters and the
girdled branch could be the trunk itself (Cordeiro, 2008).
Similar length was found for branches girdled by O. impluviata (Link and Costa,
1993) but greater lengths were found for O. pustulata (Rice, 1989), and lower values
were recorded for O. cingulata (Cramer, 1998).
VOLUME 86, ISSUE 4 313
One of the advantages of girdling larger-diameter branches is that as the diameter
of a branch doubles, its volume becomes almost four times more (Rice, 1989). This is
the reason that certain species of big twig girdlers girdle branches large in both
diameter and length, as their larvae would also be bigger in size.
Girdled branches with more leaves are able to absorb more nitrogen than
branches of similar dimensions with fewer leaves (Forcella, 1982). It is possible
that the twig girdlers choose their host branch based on the number of leaves and
leaf area to ensure better nutritional quality of the food for their offspring. An
attack of O. impluviata caused a loss of 34.1% of the leaves as against the non-
girdled trees of A. mearnsii (Pedrozo, 1980). Oncideres saga causes a leaf loss area
ranging from 14.8% to 50% in trees of A. mangium with 36 months (Cordeiro,
2008). At a density of 13 couples of O. rhodosticta per tree of Prosopis glandulosa
Torr., up to 75% of the canopy of this tree could be damaged (Polk and Ueckert,
1973).
The feeding action of Metaxyonycha angusta (Perty) (Col.: Chrysomelidae) caused
a loss of 0.02% of leaf area in eucalyptus (Fernandes, 2004), whereas Lampetis
nigerrima (Kerremans) (Col.: Buprestidae) feeding on the young plants of Eucalyptus
urophylla 3 E. grandis caused 0.9% leaf loss (De Nadai, 2005).
On comparing the leaf loss caused by O. ocularis with the loss caused by other
twig girdlers, it is found to causes less intense defoliation. It must be noted that in
younger trees, O. ocularis can cause a proportionately greater loss of leaf area.
However, when compared with beetles of other families, such as M. angusta and L.
nigerrima, it causes defoliation on intensity comparable with these beetles.
Considering the larvae of the O. ocularis occupied only branches that are detached
of the tree, it is better to consider this beetle as a defoliator beetle rather than a
borer beetle.
Insects Co-Inhabitating the Girdled Branches
Engyum quadrinotatum was reported on branches of A. mangium girdled by O. saga
(Cordeiro et al., 2010b). It was also found in branches of Lauraceae girdled by O.
captiosa, being one of the most common species emerging from those branches
(Witeck Neto and Link, 1997). This Cerambycidae lays its eggs in the same incision
made by O. saga in branches of A. mearnsii (Marinoni, 1979). This fact indicates that
this insect can be considered as an important natural enemy of O. ocularis, as the
larvae of this insect, when hatched near the twig girdler larvae, will compete with it for
food and space within the girdled branch.
This could probably be the first report of the emergence of Orthostema abdominale
on branches girdled by twig girdlers. The occurrence of this insect is in accordance
with the geographic distribution for the species (Martins and Galileo, 2005).
Nesozineus bucki is associated with girdled branches of A. mearnsii in Rio Grande
do Sul state, southern Brazil (Bertels and Baucke, 1966). This is the first record of the
species on the branches of A. mangium.
Lepturges fischeri Melzer was reported emerging from the branches of black wattle
girdled by the Oncideres beetles (Marinoni, 1979). It was also reported the emergence
of L. angulatus (LeConte) and L. infilatus Bates, from the branches of Leucaena
pulverulenta (Schlecht.) Benth girdled by O. pustulata (Hovore and Penrose, 1982).
Therefore, this is the first record of this genus on the branches girdled by O. ocularis,
as well as using A. mangium as a host.
314 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
It can be inferred that these non-girdlers cerambycids have a close relationship
with the twig girdlers, especially with the genus Oncideres and may even depend
upon these beetles more than the host plant species itself (Paulino Neto et al., 2006).
Species of Buprestidae also emerged from the branches of L. pulverulenta girdled
by O. pustulata (Hovore and Penrose, 1982) and Scolytidae beetles on the branches
of A. mangium girdled by O. saga (Cordeiro et al., 2010c). Beetles of the family
Bostrichidae were found in the branches girdled by O. rhodosticta, O. cingulata and
O. pustulata (Polk and Ueckert, 1973; Rogers, 1977; Hovore and Penrose, 1982). The
Bostrichidae beetle Xylobiops texans (Horn) was claimed to be the main competitor
of O. cingulata within the girdled branches (Rogers, 1977). All the beetles that co-
inhabit the girdled branches probably compete with the twig girdler larvae for food
and space within the branch (Polk and Ueckert, 1973). Cerambycidae beetles that
emerged, as well as those other Coleoptera, are important competitors of O. ocularis
during their larval stage.
Acknowledgments
Authors are thankful to Prof. Ubirajara Martins, from the Museum of Zoology,
of Universidade de Sao Paulo, for identifying the longhorned beetles. To
‘‘Coordenacao de Aperfeicoamento de Pessoal de Nıvel Superior (CAPES)’’ for
financial support. Global Edico Services revised and edited this manuscript.
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