The diamondback moth (DBM), Plutella xylostella (L.), is the primary pest of cabbage and related crops in the family Brassicaceae. Insecticide resistance in diamondback moth populations is a major factor limiting cabbage production worldwide. Biological control offers an alternative to insecticides, but little is known of whether multiple natural enemies have additive, antagonistic, or synergistic effects on DBM populations.
Therefore, we evaluated interactions between Cotesia plutellae (Kurdj.), an important specialist parasitioid of the diamond back moth, and Podisus maculiventris (Say), an important generalist predator of numerous agricultural pests, and their effect on DBM populations.
First, we evaluated the seasonal activity of the predator P. maculiventris in North Florida to determine its potential in influencing DBM populations and alternate natural enemies. The seasonal activity of P. maculiventris overlaps with that of DBM, suggesting that P. maculiventris could have a significant effect on DBM populations.
To determine how P. maculiventris and C. plutellae interact, we studied their combined effect on DBM populations and consequent plant damage. Often when a predator and parasitoid are present together the predator prefers to feed on parasitized pest larvae rather than unparasitized ones, which interfere with the parasitoid’s ability to control a pest species and can release the pest from an acceptable level of control. In lab trials, we found that P. maculiventris does preferentially attack parasitized larvae. In field cage trials, we found that C. plutellae reduce DBM populations and plant damage, but this control is not enhanced by the addition of P. maculiventris. These results indicate the importance of evaluating interspecific interactions to optimize biological control.
Temporal Occurrence of Natural Enemies
Determining the seasonal activity or temporal occurrence of a pest and a potential predator or parasitoid is an important factor to quantify for optimizing biological control. The proportion of seasonal overlap between a pest and potential natural enemy may be indicative of the influence that predator or parasitoid has on pest populations.
Prey preference is a situation in which a predator selects one type of prey more frequently than another type of prey. Research has shown that behavior, locality, morphology, density, ontogeny, environmental temperatures, and/or physiology of the prey or natural enemy influence prey preference and prey selection. The beneficial impact of a parasitoid on a pest may be reduced if predators prey more on parasitized prey than on unparasitized prey. This preference could release the pest from an economically acceptable level of control by a parasitoid, especially when the predator’s attack rate on parasitized hosts is high.
Multi-species Assemblages in Biological Control
Competition, resource partitioning, niche overlap, interguild or intraguild predation, and/or emergent properties (e.g. antagonism) can influence pest populations when multiple species of predators and/or parasitoids are present together in an agricultural system. The resulting level of pest suppression as a consequence of these interactions is extremely variable. Multiple natural enemy assemblages can function additively, antagonistically, or synergistically on pest populations. Additive mortality is a situation where two or more natural enemies do not influence each other’s population structure. The resulting mortality on pest populations is equivalent to the sum of mortality induced by the natural enemies independently. Historically, ecologists have considered multiple natural enemies to act additively upon pest populations. However, multiple natural enemy assemblages often display emergent properties (i.e. antagonism or synergism). Antagonism occurs when mortality of a pest population induced by two or more species of natural enemies is less than the additive mortality. Synergism occurs when the combined mortality of a pest population induced by two or more species of natural enemies exceeds the additive mortality from those natural enemies. The level of pest suppression may not be optimized when antagonism among natural enemies occurs. However, synergism can be highly desirable in pest suppression. These associations can significantly influence biological control when multiple species of natural enemies are present.
- To determine the temporal occurrence of P. maculiventris in Northern Florida.
To determine if the occurrence of P. maculiventris overlaps the occurrence of the DBM.
To determine preference of P. maculiventris for unparasitized DBM larvae or larvae parasitized by C. plutellae.
To determine how P. maculiventris and C. plutellae influence P. xylostella populations and plant damage in cabbage.
Temporal Occurrence of Podisus maculiventris (Heteroptera: Pentatomidae) In North Florida
Our study was conducted at the Florida Agricultural and Mechanical University, Viticulture and Small Fruit Research Center, Tallahassee, Florida. Six pheromone-baited traps were used to collect adults of P. maculiventris. Traps were baited every two weeks with a male produced sex pheromone formulation that is attractive to males and females. Collections of adults began three days after trap placement and were inspected twice a week.
Predation by Podisus maculiventris (Heteroptera: Pentatomidae) on Larvae Parasitized by Cotesia plutellae (Hymenoptera: Braconidae) and its Influence on Plutella xylostella (Lepidoptera: Plutellidae) Populations in Cabbage
Laboratory Study of Prey Preference
Experiments were conducted in arenas with cabbage leaves used as host plant. No-choice and choice tests were conducted. Parasitized larvae were exposed to parasitism as third instars. No-choice tests were conducted at 24 hours after larvae molted into third instars and 72 hours after larvae molted into third instars and consisted of unparasitized larvae or parasitized larvae. Choice tests were conducted with unparasitized larvae and parasitized larvae at the same time intervals after parasitism as no-choice tests. Newly emerged third instar P. maculiventris were given water and starved 48 hours. An individual P. maculiventris was placed on the center of each leaf to expose larvae to the predator. Larvae were exposed to predation for 24 hours.
Field Study of Multi-species Interaction
Two field studies were conducted at the Florida Agricultural and Mechanical University, Viticulture and Small Fruit Research Center, Tallahassee, Florida. Twenty field cages with mesh screen and a zippered door were set up. In the 2002 growing season,‘Bonnie’s Hybrid’ cabbage was used as the host plant. ‘Constanza’ cabbage was used in the 2003 growing season. Six cabbage transplants were planted in two rows in each cage. Four treatments and one control were randomly assigned to individual cages: 1) a cabbage only control, 2) DBM, 3) DBM with P. maculiventris, 4) DBM with C. plutellae and 5) DBM with P. maculiventris and C. plutellae. Twenty-two DBM larvae were released per plant and 30 pupae were released per cage. The predator and parasitoid also were released one week after the final DBM release. Five third instar P. maculiventris were released per plant, and 30 C. plutellae pupae were released per cage. To estimate DBM populations, larvae and pupae were counted weekly on each plant.
Plant Damage Estimates
At the end of each growing season the plants were removed and 3 leaves were sampled from the base (old growth), the center (intermediate growth), and the head (new growth) of each plant. Plant damage was estimated by using image analysis software to determine the amount (area) of feeding on four randomly selected leaf discs from each sampled leaf.
In our trapping study, we found that P. maculiventris has two population peaks, one in May and one in June. P. maculiventris is active from March through October and its activity overlaps DBM activity throughout most of the cabbage growing season.
In our lad study developmental duration of parasitized DBM larvae was not quantified. However, ad hoc visual comparisons of unparasitized larvae and parasitized larvae suggest increased developmental duration of parasitized individuals. Parasitized larvae, after 72 hours of exposure to parasitism, remained third instars and unparasitized larvae developed into fourth instars. Our laboratory studied shows that P. maculiventris preferentially preys on parasitized DBM larvae after the larvae have been parasitized for 72 hours. Parasitism by C. plutellae indirectly influences P. maculiventris preference for parasitized larvae because the developmental duration of parasitized individuals increases. Increased developmental duration of parasitized individuals requires P. maculiventris to consume greater numbers of third instar DBM before becoming full. Our results also show that the presence of a C. plutellae egg in its host 24 hours after exposure to parasitism does not induce a predatory preference in P. maculiventris. In addition to increased developmental duration of parasitized individuals, a behavioral and/or physiological response in parasitized larvae may contribute to its vulnerability to predation. Parasitized DBM larvae also may become more lethargic and/or less capable of avoiding predation after 72 hours. Greater consumption of 72 hour parasitized DBM larvae also could be because they are a lower quality prey than unparasitized individuals.
When evaluating our field data total larval and pupal counts in 2002 the data show that neither natural enemy had an impact on DBM populations. When both natural enemies are combined they display an additive association because their impact on DBM populations is equivalent to either natural enemy acting independently. An additive association is also suggested by the 2003 plant damage estimates were no treatments differed. Conversely, in 2003 when C. plutellae was present alone DBM populations were reduced. Moreover, when analyzing the data by date the data in 2002 and 2003 shows that when C. plutellae is present alone, DBM populations are suppressed late in the growing season until harvest. The late season suppression of DBM populations when C. plutellae is alone shows that an early season antagonistic effect is occurring when C. plutellae and P. maculiventris are together. Preference of P. maculiventris for parasitized DBM larvae early in the season induces enough mortality on parasitoid populations to produce a noticeable antagonistic effect later in the season. Also, the 2002 plant damage estimates show that C. plutellae had the greatest impact in reducing plant damage showing that the antagonistic interaction is strong enough to increase plant damage when both natural enemies are present together.
An additional phenomenon revealed in our investigations suggests that DBM larvae prefer feeding on the intermediate growth of cabbage. In nearly all treatments there are greater amounts of damage on the intermediate growth stage of the cabbage plants. This suggests larvae of the DBM prefer feeding in this region of the plant because it is greater in nutrients for development, increases protection from natural enemies and/or the female chooses to lay her eggs on the intermediate region of the plant. Alternatively, the natural enemies may prefer searching the new growth or old growth of the plant.
Educational & Outreach Activities
Two Presentations were given at two meetings of the Entomological Society of America.
Herrick, N. J. and S. R. Reitz. 2002. Synthetic guild analysis of Podisus maculiventris and Cotesia plutellae: Their effects on Plutella xylostella populations in cabbage. Entomological Society of America, 50th Annual Meeting, Ft. Lauderdale, Florida.
Herrick, N. J. and S. R. Reitz. 2003. Prey Preference of Podisus maculiventris for larvae parasitized by Cotesia plutellae and unparasitized Plutella xylostella larvae. Entomological Society of America, 51st Annual Meeting, Cincinnati, Ohio.
One presentation was given at the Florida Agricultural and Mechanical University.
Herrick, N. J. and S. R. Reitz. 2001. Synthetic guild analysis of Podisus maculiventris and Cotesia plutellae: Their effects on Plutella xylostella populations in cabbage. Florida Agricultural and Mechanical University, 1st annual Research Forum, Tallahassee, Florida.
One scientific note has been published.
Herrick, N. J. and S. R. Reitz. 2004. Temporal occurrence of Podisus maculiventris (Hemiptera: Heteroptera: Pentatomidae) in North Florida. Florida Entomologist 87: 587-590.
One manuscript has been prepared and is being reviewed by the authors to be submitted to Environmental Entomology.
Herrick, N. J., S. R. Reitz, J. E. Carpenter and C. W. O’Brien. Predation by Podisus maculiventris (Heteroptera: Pentatomidae) on Larvae Parasitized by Cotesia plutellae (Hymenoptera: Braconidae) and its Influence on Plutella xylostella (Lepidoptera: Plutellidae) Populations in Cabbage.
The antagonistic association between the predator and parasitoid in our study and other natural enemy combinations likely contributes to the pest status of the DBM. Furthermore, when testing for interactions between natural enemies it is vital to make observations over time to fully understand any interaction or lack thereof. Furthermore, plant damage estimates are essential for assessing the strength and practical implication of any interaction.
Areas needing additional study
Similar tests over longer durations would provide valuable information to understand the consistency and frequency of multiple natural enemy interactions. Studies involving behavioral modifications of parasitized DBM larvae would be useful to help understand what contributes to the preference or non-preference in predators like P. maculiventris.
Understanding these phenomena could reveal an important predator of the DBM and lead to more efficacious management of this pest. In addition, these investigations raise questions concerning the influence, biology, and interactions of other predator and parasitoid species that attack DBM in agricultural and natural habitats. Emphasis on measuring interactions over longer periods of time, varying release times and monitoring populations of the natural enemies would reveal information important towards practical applications of desirable natural enemy interactions in brassica systems. Investigations involved with these phenomena may permit biological control to be viewed as more favorable management tactic for controlling the DBM in brassica crops and other annual crops.