Acceptability of native and exotic potential host species for the growth and development of Oxyops vitiosa
G. S. Wheeler
Abstract. As predicted from quarantine host testing, O. vitiosa neonates did not complete development when fed the native M. cerifera. When fed M. quinquenervia leaves until the third instar however, they could complete development when fed M. cerifera, though their survival was significantly reduced (20%). Additionally, those few larvae that survived on M. cerifera leaves had significantly reduced biomass; less than half that of the control larvae. Survival of larvae fed the Australian ornamental species C. rigidus, C. viminalis, and M. quinquenervia generally exceeded 65%, also confirming quarantine host testing results. Although the leaves of M. cerifera were nutritious (soft tissues and low dilution of nutrients) they may contain metabolic toxicants that protect this species from herbivory by O. vitiosa larvae. The lack of damage to field populations of M. cerifera at O. vitiosa release site where this native species is intermixed with M. quinquenervia confirms these results.
Australian field collections of Oxyops vitiosa indicated that this species
restricts its feeding to its primary host Melaleuca
quinquenervia and a few Melaleuca relatives
(Balciunas et al. 1994). In no-choice laboratory trials feeding and oviposition by this
species occurred on other members of the Myrtaceae but the larvae only completed
development on M. quinquenervia (Balciunas et
al. 1994). Quarantine host testing of O. vitiosa suggested that suitable laboratory hosts
included several species of Australian ornamental myrtaceous plants in the Callistemon genus, namely C. viminalis (Sol. Ex Gaertner) G.Don ex Loudon and
C. rigidus R.Br. Additionally, O. vitiosa larval feeding and development occurred
when neonates that had previously been fed M.
quinquenervia leaves until the third instar were transferred to the distantly related Myrica cerifera L. (Myricaceae). Confirmation of
these results is essential to continue promoting this insect as a biological control agent
of M. quinquenervia. Furthermore, understanding the mechanisms by which
this apparently highly specific biological control agent utilizes alternate hosts in the
laboratory will assist in our understanding of future agent specificity and allow
practitioners to better predict host range.
Within the family Myrtaceae the two
genera Callistemon and the Melaleuca have numerous similarities including
components of their terpenoid chemistry (Brophy et al., 1985; Brophy et al., 1989;
Ramanoelina et al., 1994; Brophy et al., 1997). This,
together with morphological similarities have, suggested that members of these two genera
are closely related resulting in the reclassification of C. viminalis as Melaleuca viminalis (Sol. Ex Gaertner) Byrnes
(Byrnes 1984; 1986). Even though this
biological control species is highly selective in its feeding and development it is not
surprising, considering their similar secondary chemistry, to find laboratory-host
acceptance of members of similar genera or the same plant genus. However, it was more surprising to find that in
laboratory host testing O. vitiosa third instars
completed development on an unrelated North American plant M. cerifera.
However, as first instars do not survive and no oviposition was found on this
species the only potential damage to this native plant in natural conditions would occur
as ‘spill-over’ from larvae feeding on neighboring M. quinquenervia (Balciunas and Buckingham, 1986).
Thus any threat M. cerifera is limited to the
range of M. quinquenervia that is restricted to
south Florida (Turner et al. 1998) whereas that of M.
cerifera extends north to New Jersey and west to Texas (Small, 1972).
Specialized herbivores are well adapted
to the chemical defenses of their host plant. However, under artificial conditions such as
laboratory environments specialists will feed on less preferred hosts. As a consequence
this ‘host broadening’ may result in decreased survival, and differences in
consumption, food digestibility and feeding efficiency and weight gain. The objectives of this study were to determine the
larval survival, growth, development, food digestibility and feeding efficiency of O. vitiosa when fed these laboratory hosts. This information will determine the safety of this
agent for continued field release and examine the mechanisms of host utilization by this
specialist herbivore.
Plants. Leaves of all
four species M. cerifera, C. rigidus, C.
viminalis, and M. quinquenervia were
collected from local ornamental trees in Ft Lauderdale.
Three times weekly, leaves were clipped from trees and brought back to the
laboratory for use in the test. As O. vitiosa is a known tip feeder (Purcell and
Balciunas 1994; Wheeler unpublished data), only the silky terminal 10 cm tip leaves of
each tree species were collected and fed to the larvae.
Plant Quality. Leaves were
tested for toughness using a modified gram gauge (Wheeler and Center 1996 and 1997) that
estimates the pressure required to puncture leaf tissues.
Nearly 100% mortality of O. vitiosa
larvae was found on older leaves of M. quinquenervia
with toughness values greater than 500 g/mm2 (Wheeler unpublished data). Leaf toughness was measured on leaves 1 - 15
(counting from the tip leaves toward the branch base).
Replicates consisted of 20 leaves of each position.
Leaf percent dry weight (dw) was determined gravimetrically by weighing each leaf
(positions 1 – 10) fresh and after drying (60 °C for 48 h).
Larval
survival, growth and development. Neonate O.
vitiosa larvae were transferred to individual reared through to pupation on tips of
each of the species. Additionally, neonates
were reared to the third instar on leaves of M.
quinquenervia and transferred to leaves of each species. The larvae were reared in plastic petri dishes
lined with moistened filter paper and sealed with Parafilm.
All rearing was conducted at 28 °C 50% RH and under a 14:10 h photoperiod. Data were collected on larval survival and
developmental performance. The final dw
(dried at 60 °C for 48 h) of each pupa (± 0.1 mg) and the time (days) required to reach
pupation was recorded. Leaf consumption was
estimated gravimetrically according to the following method. Each leaf was cut was paired with an adjacent leaf
on the same branch and each was weighed fresh. One
leaf served as the control leaf and was dried (60 °C for 48 h) directly to determine the
initial percent dry weight of the companion leaf. The
half was fed to a larva until at least 60% of the leaf area was consumed. The uneaten portion of this leaf half was dried
and weighed. With the estimate of initial dry
weight and the final dry weight of the leaf material not consumed, we estimated dry weight
consumption by subtracting the final dry weight from the initial dry weight.
Data analysis. All analyses were conducted with SAS/PC (PROC
GLM) unless otherwise noted (SAS Institute, Inc., 1990).
The leaf dry weight, toughness and nitrogen results were analyzed on different
leaves and comparisons of regression coefficients of the different species were performed
by ANCOVA. The nutritional parameters (e.g.,
survival, consumption, development time, weight gain) were analyzed by ANOVA and means
were compared with the Ryan’s Q test (p =
0.05).
Plant Quality. Leaf percent dry weight differed according to leaf
position on the stem and plant species where the highest percent dry weight was found on
leaves from M. cerifera and the values for this
species increased gradually toward the base of the stem (Fig. 1). This is in contrast to the leaves from the other
three species whose dry weight decreased toward the base.
A comparison of regression slopes of these lines (ANCOVA) indicated that the slope
of the M. cerifera leaf dry weight was
significantly greater that those of the other species (t = 7.83; P < 0.0001).
Leaf toughness
also differed according to leaf position and plant species where the greatest leaf
toughness was found with M. quinquenervia leaves
toward the base of the branch tip (Fig. 2). Again this was in contrast to the leaves from M. cerifera whose leaves were significantly less
tough compared with the other species.
Larval
survival, growth and development
Neonate performance. Recently emerged larvae (< 12 h old) were
transferred to fresh tip leaves and monitored for survival and development time. None of the neonate larvae transferred to M. cerifera survived to the prepupal stage, whereas
survival of those transferred to C. rigidus, C. viminalis, and M. quinquenervia were 75 (± 9.6 %), 65 (± 12.6
%), and 85 (± 5.0 %), respectively (Fig. 3). Larval development was greatest for larvae fed the
C. rigidus leaves, whereas less time was
required to complete development for larvae fed C.
viminalis and M. cerifera.
Third instar performance.
Neonate larvae were reared on M. quinquenervia
leaves during the first two instars and then transferred to their respective test plants
until pupation. Survival of these larvae to
the adult stage was significantly reduced for those fed the M. cerifera leaves (20% ± 11.6%) compared with
those fed leaves of C. rigidus (75.0 ± 9.6
%), C. viminalis (67.5 ± 7.5 %), and M. quinquenervia (81.7 ± 6.9 %) (Fig. 4). Larval food
consumption was reduced significantly only in those larvae fed leaves from C. viminalis, where these larvae consumed 70.9 mg
(dry mass; Fig. 4). Larval
development time to the prepupal stage was greater in the larvae fed M. cerifera (11.4 ± 0.9 d) and C. rigidus (10.8 ± 0.2 d)¸ compared with those
fed the other two plant species (Fig. 4). Weight gain was reduced
only for those larvae fed the M. cerifera leaves
where the larvae gained 14.2 (± 3.0 mg) (Fig. 4). The sex of the prepupae (F 1,43 = 23.0;
P < 0.0001), pupae (F 1,43 = 31.7; P < 0.0001) and adults (F 1,43
= 39.7; P < 0.0001) significantly influenced their weights (excluding those fed M. cerifera), regardless of larval diet. Female
prepupal (62.6 ± 1.2 mg), pupal (54.3 ± 1.1 mg), and adult (47.2 ± 1.2 mg) weights were
all greater than those of males (54.0 ± 1.2 mg; 45.0 ± 1.2 mg; 37.3 ± 0.8 mg,
respectively).
These results confirm the studies
conducted in quarantine that indicated that O.
vitiosa neonate larvae could not complete development on M. cerifera. Furthermore,
when larvae were reared on M. quinquenervia
leaves until the third instar, they could complete development on M. cerifera, though survival of these larvae was
significantly reduced (20%). Additionally, those few larvae that survived on M. cerifera leaves had significantly reduced
biomass; less than half that of the control larvae. Survival
of larvae fed the Australian ornamental species C.
rigidus, C. viminalis, and M. quinquenervia generally exceeded 65%, also
confirming quarantine host testing results. Although
larval consumption was reduced in those fed C.
viminalis leaves and development time was increased in larvae fed M. cerifera and C. rigidus, larval performance was similar among
those fed the Australian ornamentals.
The relatively high consumption of the M. cerifera leaves found here suggests that the proper stimulants to initiate and continue feeding by third instar O. vitiosa larvae were present. The nutritional quality of the leaves of M. cerifera may be higher than the other species tested as demonstrated by the leaf toughness values which were lower (therefore softer tissues) and percent dry weights (therefore less nutrient dilution) which were higher than those of the other species. However, the relatively high larval mortality and reduced weight gain suggests the presence of metabolic toxicants that were not successfully detoxified. Additional research indicates that the leaves of all four species contain numerous terpenoids, compounds known to be highly active anti-herbivore defensive compounds (Gershenzon and Croteau, 1991). Although these species have several compounds in common (e.g., a-pinene, 1-8 cineole, a-terpineol, nerolidol, viridiflorol), M. cerifera is most unlike the others containing principally the terpenoid limonene. Possibly this compound is unacceptable to O. vitiosa larvae at the concentrations present in the leaves of M. cerifera. However, additional research will be needed to address this factor directly.
References