Source: COLORADO STATE UNIVERSITY submitted to NRP
CAUSES AND CONSEQUENCES OF COMPETITIVE DISPLACEMENT IN COTESIA PARASITOIDS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1000988
Grant No.
2014-67013-21727
Cumulative Award Amt.
$453,177.00
Proposal No.
2013-02527
Multistate No.
(N/A)
Project Start Date
Mar 1, 2014
Project End Date
Feb 28, 2018
Grant Year
2014
Program Code
[A1111]- Plant Health and Production and Plant Products: Insects and Nematodes
Recipient Organization
COLORADO STATE UNIVERSITY
(N/A)
FORT COLLINS,CO 80523
Performing Department
Bioagricultural Sciences
Non Technical Summary
This project focuses on the ecological interactions involved in the competitive displacement of Cotesia glomerata by C. rubecula, two imported biological control agents of the imported cabbageworm Pieris rapae, a serious pest of cruciferous crops worldwide. Careful studies of competitive displacement provide an extraordinary opportunity to explore the mechanisms behind successful invasions and establishment of introduced biological control agents. We make the case that because much is known about interspecific larval interactions, host use patterns, and sex determination involving these two species that we are in an excellent position to examine the process of competitive displacement, a widespread but poorly understood phenomenon that can provide important insight into understanding why some biological control introductions succeed whereas others fail. We take advantage of the fact that C. rubecula has not yet invaded the western Great Plains and propose to study how different mechanisms involved in competitive displacement interact. Our specific objectives are to 1) Explore the mechanisms (intra- and inter-host competition, host range, and sex determination) allowing C. rubecula to displace C. glomerata using a series of laboratory and field studies; 2) Model the joint effects of differences in life-history traits, host range, and sex determination mechanisms on the competitive displacement of C. glomerata and C. rubecula; 3) Conduct field releases of C. rubecula in Colorado to test the importance of these three mechanisms as C. rubecula displaces C. glomerata.
Animal Health Component
0%
Research Effort Categories
Basic
100%
Applied
0%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
21514401130100%
Goals / Objectives
We will investigate how displacement of C. glomerata by C. rubecula affects biological control of Pieris rapae - one of the most important pests of crucifers in the U.S. and throughout the world. This investigation features the following objectives: Objective 1. Explore the mechanisms allowing C. rubecula to displace C. glomerata using a series of laboratory and field studies. Specifically, we will a) explore whether C. glomerata avoids P. rapae hosts already parasitized by C. rubecula, b) compare the functional responses of C. rubecula and C. glomerata across a range of P. rapae densities in the presence and in the absence of an interspecific competitor as well as the presence or absence of alternative hosts, and c) measure diploid male production in field populations and estimate whether C. rubecula populations still have 2-locus CSD or whether they have effectively collapsed to sl-CSD. Objective 2. Model the joint effects of differences in life-history traits, host specificity, and sex determination mechanisms on the competitive displacement of C. glomerata by C. rubecula. We will use a continuous-time modeling framework that incorporates the main life-histories that are relevant to the P. rapae/Cotesia rubecula/C. glomerata system. The model will be parameterized according to the results of Objective 1 and produce predictions for Objective 3. Objective 3. Conduct field releases of C. rubecula in CO to test the importance of these three mechanisms as C. rubecula displaces C. glomerata. While C. glomerata is a common parasitoid of P. rapae in cruciferous crops in CO, C. rubecula has never been recorded in the state. This provides an excellent opportunity to explore the role of life-history traits, host range, and sex determination as competitive displacement is potentially occurring. We propose experimental releases of C. rubecula at various field sites in CO that will allow field-scale, population level evaluation of the hypotheses from Objective 1 and predictions from the models developed in Objective 2.
Project Methods
Objective 1. Explore the mechanisms allowing C. rubecula to displace C. glomerata. Objective 1a) does C. glomerata avoid multiparasitism? To examine whether C. glomerata or C. rubecula avoid multiparasitism, we will conduct the following experiments. Experimental arenas will consist of a 0.5 by 0.5 by 0.5 m cage containing a cabbage plant and two third instar P. rapae larvae. Two types of experiments will be conducted: choice tests and no-choice tests. In the choice tests, one of the two P. rapae larvae will be parasitized by a C. rubecula female; in the no-choice tests both of the P. rapae larvae will be parasitized by a C. rubecula female. Immediately after one (choice tests) or both (no-choice tests) P. rapae larvae are parasitized (determined by observation), the C. rubecula female will be removed. A C. glomerata female will be introduced into the arena and her foraging and oviposition decisions will be recorded. A single female C. glomerata will be introduced into either a choice or a no-choice cage at 0-2 hours, 1 day, 2 days, or 3 days after oviposition by C. rubecula. C. rubecula's avoidance of multiparasitism will be tested under choice and no-choice conditions. Hosts will be dissected 4 days after the 2nd attack to determine whether multiparasitism occurred and to assess the outcome of any competitive interactions. Objective 1b: compare the functional responses of C. rubecula and C. glomerata to changes in P. rapae densities. We will examine differences in the low-density functional responses of C. rubecula and C. glomerata in the absence and presence of interspecific competitors with the use of large (8m long by 4m wide by 2.5m tall) field cages. For each trial we will place 50 potted cabbage plants inside the field tent arranged in a 5 by 10 array. In each trial, we will place 1, 2, 4, 8, or 16 third instar P. rapae larvae randomly across the 50 plants. One mated C. rubecula female, one mated C. glomerata female, or two mated females (one of each species) will be released into the cage and allowed to forage and oviposit for 24 hours. Host P. rapae will be allowed to establish for 24 hours to allow them to begin feeding and release any plant and host-associated volatiles known to be attractive to these parasitoids. Three days later, the P. rapae larvae will be collected and brought into the lab where they will be dissected to determined whether they were attacked and, if so, which species (in the combination treatment) laid eggs. Objective 1c: does C. rubecula have a 2-locus CSD system or effectively a sl-CSD? Using methods developed in previous work by our group (de Boer et al. 2007a,b, 2008, 2012) we will assess the CSD locus and allele diversity in multiple populations of C. rubecula in MN. Collections will be made at experiment stations in MN from cabbage and other crucifer fields that regularly harbor P. rapae and C. rubecula populations. P. rapae will be collected as 3rd instar larvae and reared in the laboratory to obtain C. rubecula pupae, and pupal C. rubecula will be collected directly from the field as well. Two methods will be used to assess sex locus and allele diversity. First, a minimum of 50 C. rubecula males from these collections will be assessed for ploidy level using flow cytometry as described in de Boer et al. (2007b, 2008, 2012). High proportions of diploid males are consistent with a single sex locus and relatively few sex alleles, but a low proportion of diploid males could be consistent with either a single sex locus with many sex alleles or more than one sex locus (Heimpel & de Boer 2008, de Boer et al. 2008, 2012). We will conduct mother-son inbreeding studies to distinguish between sl-CSD and 2-locus CSD within C. rubecula populations. Crosses will be done using methods previously developed by de Boer et al. for C. rubecula (2012) and a minimum of 10 control outcrosses will be done as well, in which males are paired with females from different populations (collection sites). Data from these crosses will be used to estimate the number of loci and the number of alleles per locus for each populations sampled using a statistical simulation modeling approach developed by De Boer et al. (2012) in which the maximum likelihood for scenarios involving 1 and 2 loci (or more if this is deemed possible) is compared with each collection site. To compare across populations, the cross-population matings will be used to determine whether there is evidence for shared loci or alleles across these populations. Objective 2. Model the joint effects of differences in life-history traits, host range, and sex determination mechanisms on the competitive displacement of C. glomerata by C. rubecula. Here, we develop a modeling framework to investigate the population dynamics of the Pieris rapae/Cotesia rubecula/C. glomerata system. The purpose of the model will be to investigate the effect of the two parasitoid species on each other's population levels as well as that of the host. The most appropriate framework is a continuous-time model with host and parasitoid stage structure that allows for time lags in both parasitoid and host development and overlapping windows of vulnerability for the parasitoid. We will construct the model in two ways: first, we will model multiparasitism, in which C. glomerata oviposit into hosts that had been previously parasitized by C. rubecula but the larvae are killed by C. rubecula larvae. Second, we will model avoidance of multiparasitism in which C. glomerata detects the presence of C. rubecula in previously parasitized hosts and do not oviposit into these. This latter formulation is functionally equivalent to a model explored by Briggs (1993) but the former formulation will be a novel contribution. Objective 3. Conduct field releases of C. rubecula in CO to test the importance of these three mechanisms. We will conduct releases at three field sites in CO. At each of the three sites, we will plant two 100 m2 (0.01 hectare) plots with cabbage, each embedded in larger crucifer fields (typically, cabbage or canola). At each research center, the two 100 m2 plots will be separated by at least 4 km. At one of the plots at each of the three sites, we will release 500 mated C. rubecula females in the center of the plot. No C. rubecula will be released at the other plot (located at least 4 km away to reduce the likelihood that C. rubecula will move between plots), which will serve as a control plot with only C. glomerata present. We will monitor each of the 6 plots (paired plots at each center) monthly from June through September during each of the three field seasons covered by this proposal. During each visit we will sample 100 randomly selected plants within each plot. Each plant will be carefully examined and all P. rapae larvae as well as all Pontia spp. larvae will be collected. Half of the larvae will be examined for the presence of C. rubecula and C. glomerata eggs and larvae. As we dissect each host, we will record any occurrences of multiparasitism as well as any evidence of fighting (dead larvae). The proportion of larvae that were parasitized by each of the Cotesia species will be recorded. The other half of the P. rapae larvae will be placed in insect diet cups containing an artificial diet for P. rapae and allowed to complete development until either an adult moth or adult parasitoids emerge. AAdult parasitoids will be frozen for flow cytometric analysis to determine the ploidy level of males. We expect that the frequency of diploid male production will increase for C. glomerata and that this will be partially explained by reduced population sizes of C. glomerata and increased likelihood of inbreeding. Finally, we will use a repeated measures analysis of variance to explore whether C. rubecula releases result in a decrease in the parasitism rate of the two native Pontia species.

Progress 03/01/14 to 02/28/18

Outputs
Target Audience:The target audience for this project includes biological control researchers, both academic and government (federal, state, and local), as well as practitioners and land managers. The target audience also includes ecologists and evolutionary biologists focused on invasive species ecology and management. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project provides field, greenhouse, and laboratory research experience for two graduate students and four undergraduate students. This project also provided opportunities for graduate students to present at national and international professional meetings How have the results been disseminated to communities of interest?Our findings have been dessiminated in two publications and four oral presenations at professional meetings during the past year. What do you plan to do during the next reporting period to accomplish the goals?This is the final year of the project.

Impacts
What was accomplished under these goals? Objective 1) We continued to conduct weeking sampling at six field sites (four organic, commerical farms; two CSU field sites) to determine population size estimates of Pieris rapae, parasitism rates by Cotesia glomerata, and hyperparasitism rates. Ongoing laboratory and greenhouse experiments examined foraging behavior in the face of competition in the presence of conspecifics and heterospecific. This past year, we expanded our comparative studies to include C. glomerata from other source popualtions that experience different types of competition (e.g., Maryland, where C. glomerata and C. rubecula cooccur). Objective 2) work on this objective was completed in the previous year. Objective 3) We continued to monitor the establishment success and spread of our introduced C. rubecula colonies that showed evidence of establishment the previous year. This was the fourth and final year of this project.

Publications

  • Type: Journal Articles Status: Accepted Year Published: 2018 Citation: Pearse IS, Paul R, Ode PJ. in press. Variation in plant defense suppresses herbivore performance. Current Biology.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Ode PJ, Keasar T, Segoli M. 2018. Lessons from the multitudes: insights from polyembryonic wasps for behavioral ecology. Current Opinion in Insect Science 27: 32-37.


Progress 03/01/16 to 02/28/17

Outputs
Target Audience:The target audience for this project includes biological control researchers, both academic and government (federal, state, and local), as well as practitioners and land managers. The target audience also includes ecologists and evolutionary biologists focused on invasive species ecology and management. Changes/Problems:We have made substantial progress in reducing problems with the Pieris rapae granulosis virus that had previously devastated our butterfly and parasitoid colonies. By increasing the rate of fertilizer application, we were able to produce higher quality plants that resulted in butterflies that were better able to withstand infection by the granulosis virus. This will enable us to make significant progress in the last year of this project. What opportunities for training and professional development has the project provided?This project provides field, greenhouse, and laboratory research experience for two graduate students, three undergraduate students, and one postdoctoral associate. This project has also provided opportunities for the graduate students to present their findings at national (Entomological Society of America Annual Meeting, Denver, CO) and international (5th International Entomophagous Insects Conference, in Kyoto, Japan) meetings. How have the results been disseminated to communities of interest?Our findings have been desseminated in four publications as well as three oral presentations at professional meetings. What do you plan to do during the next reporting period to accomplish the goals?We plan to continue our field monitoring and experiments for one more summer to monitor the establishment success and spread of C. rubecula under field conditions. We also plan to finish laboratory and greenhouse experiments.

Impacts
What was accomplished under these goals? Objective 1) 2016 was the third field season of this project. We continued weekly sampling at six field sites (organic farms that grow a variety of brassicacious crops) from June through October 2016. Weekly samples generated population size estimates of Pieris rapae and parasitism rates by Cotesia glomerata. We also estimated rates of parasitism of C. glomerata by native hyperparasitoids. We are continuing laboratory and greenhouse experiments documenting the functional responses (responses to changes in host density) of both Cotesia glomerata and C. rubecula. We are also exploring how foraging behaviors change in the presence of conspecifics and heterospecifics. This information provides baseline data against which we can assess the impact of C. rubecula releases. Finally, we are beginning to explore how these foraging behaviors differ across populations of C. glomerata that exhibit different host species availability and competitive environments. Objective 2) We finished our exploration of sex determination mechanisms and modeling efforts - this is published in Evolution (Weis et al. 2017). Objective 3) We successfully recovered C. rubecula from two field sites where this species was released in 2015 - despite no evidence of establishment in 2016. Field studies described in Objective 1 are being used to analyze mechanisms responsible for the establishment and spread of C. rubecula.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Cockrell DM, Griffin-Nolan RJ, Rand TA, Altilmisani N, Ode PJ, Peairs F. 2017. Host plants of the wheat stem sawfly (Hymenoptera: Cephidae). Environmental Entomology 46: 847-854. https://doi.org/10.1093/ee/nvx104
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Weis JJ, Ode PJ, Heimpel GE. 2017. Balancing selection maintains sex determining alleles in multiple-locus complementary sex determination. Evolution 71: 1246-1257. http://dx.doi.org/10.1111/evo.13204
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Peterson JA, Ode PJ, Oliveira-Hofman C, Harwood JD. 2016. Integration of plant defense traits with biological control of arthropod pests: challenges and opportunities. Frontiers in Plant Science 7, Article 1794. http://dx.doi:10.3389/fpls.2016.01794
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Ode PJ, Harvey JA, Reichelt M, Gershenzon J, Gols R. 2016. Differential induction of plant chemical defenses by parasitized and unparasitized herbivores: consequences for reciprocal, multitrophic interactions. Oikos 125: 1398-1407. http://dx.doi.org/doi:10.1111/oik.03076
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Harvey JA, Ode PJ, Malcicka M, Gols R. 2016. Short-term seasonal habitat facilitation by an insect herbivore. Basic and Applied Ecology 17: 447-454. http://dx.doi.org/doi:10.1016/j.baae.2016.03.005
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Kaiser L, Ode P, van Nouhuys S, Calatayud P-A, Colazza S, Cortesero A-M, Thiel A, van Baaren J. 2017. The plant as a habitat for entomophagous insects. Advances in Botanical Research 81: 179-223. http://dx.doi.org/10.1016/bs.abr.2016.09.006
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Lestina J , Cook M , Kumar S, Morisette J, Ode PJ, Peairs F. 2016. MODIS imagery improves pest risk assessment: a case study of wheat stem sawfly (Hymenoptera: Cephus cinctus) in Colorado, USA. Environmental Entomology 45: 1343-1351.


Progress 03/01/15 to 02/29/16

Outputs
Target Audience:The target audience for this project includes biological control researchers, both academic and governmental (federal, state, and local), as well as practitioners and land managers. The target audience also includes ecologists and evolutionary biologists focused on invasive species ecology and management. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has provided field and greenhouse research for three undergraduate students, two graduate students, and one postdoctoral student. In addition, this project has provided evolutionary ecology modeling experience for the postdoctoral student. How have the results been disseminated to communities of interest?Preliminary results have been disseminated in three publications as well as four oral presentations at professional meetings. What do you plan to do during the next reporting period to accomplish the goals?We will continue our weekly sampling protocols at each of the six field sites. We will likely have to conduct additional releases of C. rubecula in the event that establishment from last year's release efforts were unsuccessful or inadequate. This spring (2016) we aim to begin our laboratory and greenhouse experiments in earnest now that our rearing efforts appear to be working.

Impacts
What was accomplished under these goals? The summer of 2015 was the second full field season of this project. We continued to conduct weekly samples at six field sites beginning May 2015 through early November 2015. All six field sites are commercial organically grown cabbage and related cultivars with no control measures taken for lepidopteran control. We obtained population estimates of Pieris rapae (imported cabbage worm) as well as parasitism rates by Cotesia glomerata. This information provided further baseline data with which we will assess the impact of releasing C. rubecula. At three of the field sites, we released approximately 50 C. rubecula individuals in support of Objective 2. Successful reproduction in the field was confirmed at one of the field sites; establishment success at the other two sites will be assessed in summer of 2016. In support of Objective 1, we continued to collect C. glomerata males for flow cytometry analysis of their ploidy levels.

Publications

  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Ode PJ, Harvey JA, Riechelt M, Gershenzon J, Gols R. in press. Differential induction of plant chemical defenses by parasitized and unparasitized herbivores: consequences for reciprocal, multitrophic interactions. Oikos DOI: 10.1111/oik.03076
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Kaser JM, Ode PJ. 2016. Hidden risks and benefits of natural enemy-mediated indirect effects. Current Opinion in Insect Science 14:105-111. http://dx.doi.org/10.1016/j.cois.2016.02.004
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Kaplan I, Carrillo J, Garvey M, Ode PJ. 2016. Indirect plant-parasitoid interactions mediated by changes in herbivore physiology. Current Opinion in Insect Science 14: 112-119. http://dx.doi.org/doi:10.1016/j.cois.2016.03.004


Progress 03/01/14 to 02/28/15

Outputs
Target Audience:The target audience for this project includes biological control researchers, both academic and governmental (federal, state, and local), as well as practitioners and land managers. The target audience also includes ecologists and evolutionary biologists focused on invasive species ecology and management. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has provided field and greenhouse research for two undergraduate students, two graduate students, and one postdoctoral student. In addition, this project has provided evolutionary ecology modeling experience for the postdoctoral student. How have the results been disseminated to communities of interest?Preliminary results have been disseminated in one publication as well as three oral presentations at professional meetings. What do you plan to do during the next reporting period to accomplish the goals?We plan to continue weekly sampling at each of our field sites throughout the summer of 2015. We plan releases of Cotesia rubecula in half of our field sites mid-summer of 2015. In addiiton we will conduct laboratory and greenhouse studies of competitive displacement between foraging adults as well as between larvae of the two parasitoid species within individual hosts in our exploration of the mechanisms responsible for the competitive displacement of Cotesia glomerata by Cotesia rubecula.

Impacts
What was accomplished under these goals? The summer of 2014 was the first full field season of this project. In support of both objectives, weekly samples were conducted at six field sites beginning late May 2014 through the end of October 2014. Population levels of Pieris rapae were estimated from these weekly samples at each of the six field sites. Parasitism rates by Cotesia glomerata were also estimated for each of the weekly samples at each of the field sites. This data will provide the necessary baseline data to assess the effects of releasing Cotesia rubecula in the summer of 2015 (Objective 2). Furthermore, Cotesia glomerata samples have been frozen at -80C for shipment to the University of Minnesota where their ploidy levels will be determined with flow cytometry in support of Objective 1. Laboratory/greenhouse colonies of Pieris rapae, Cotesia glomerata, and Cotesia rubecula have been established during this time period in support of the laboratory/greenhouse experiments - also in support of Objective 1.

Publications

  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Ode PJ, Johnson SN, Moore BD. 2014. Atmospheric change and induced plant secondary metabolites - are we reshaping the building blocks of multi-trophic interactions? Current Opinion in Insect Science 5:57-65.