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Does the Small White Butterfly (Pieris Rapae L.) Aggregate Eggs on Plants

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Does the Small White Butterfly (Pieris Rapae L.) Aggregate Eggs on Plants P1: VENDOR/GAY P2: GCP/GDW/GGN Journal of Insect Behavior [joib] PP199-341427 June 24, 2001 8:38 Style file version Feb 08, 2000 Journal of Insect Behavior, Vol. 14, No. 4, 2001 Does the Small White Butterfly (Pieris rapae L.) Aggregate Eggs on Plants with Greater Gas Exchange Activity? A. Mark Langan,1,2 C. Philip Wheater,1 and Peter J. Dunleavy1 Accepted January 10, 2001; revised February 22, 2001 Few studies have investigated insect egg-laying preferences in relation to pho- tosynthesis or transpiration of their host plants. It has been suggested that in- travarietal preferences of the small white butterfly (Pieris rapae L.: Pieridae) include larger plants with characteristically higher transpiration rates. Inter- estingly this species, like many other Lepidoptera, may detect biogenic CO2 gradients associated with photosynthesis. We studied egg-laying preferences in working farm environments examining relationships among host choice, plant gas exchange activity, and plant size. Females discriminated between plants in monocultures on the basis of height. A balance of pre- and post–alighting preferences resulted in plants of medium size receiving eggs. Post–alighting preferences led to plants, but not alighted leaves, with higher rates of photo- synthesis supporting eggs. These findings do not support a mechanistic basis for the use of gas exchange activity during host selection but, for the first time, indicate the greater physiological activity of crop plants that ultimately received the eggs of a pest insect. KEY WORDS: host plant selection; Pieris rapae; photosynthesis; transpiration; brassica crops. 1Department of Environmental and Geographical Sciences, Manchester Metropolitan Univer- sity, Manchester M1 5GD, UK. 2To whom correspondence should be addressed. Fax: 0161 2476318. E-mail: m.langan@mmu. ac.uk. 459 0892-7553/01/0700-0459$19.50/0 C 2001 Plenum Publishing Corporation P1: VENDOR/GAY P2: GCP/GDW/GGN Journal of Insect Behavior [joib] PP199-341427 June 24, 2001 8:38 Style file version Feb 08, 2000 460 Langan, Wheater, and Dunleavy INTRODUCTION Despite considerable evidence that herbivory has an impact on plant gas exchange activity (for review see Welter, 1989), very few attempts have been made to investigate the photosynthetic or transpirational activity of plants visited by insects during egg-laying. Gas exchange activity associates strongly with many other important plant characteristics (see Durzan, 1968) which can influence host choice by phytophagous insects. These include nutrient content (Myers, 1985; Oleksyn et al., 1998), plant health (Habeshaw, 1984), and productivity/size (Lambers and Poorter, 1992). Usually, younger leaves have the greatest gas exchange potential (Lurie et al., 1979) and, due to high levels of nitrogen, are most nutritious for many developing lepidopteran larvae (Scriber and Slansky, 1981). Intuitively, there seems to be good reason for some insect species to select plants, or tissues of plants, with superior rates of gas exchange activity.Knowledge of such preferences, resulting from either direct or indirect insect responses to plants, may be particularly useful for studies of insect–plant interactions in which the yield and nutrient content of potential host plants are important. Host plant selection by Pieris rapae (the small white butterfly) is exten- sively documented (e.g., Courtney, 1986; Hern et al., 1996), probably resulting from the ubiquitous nature of this pest species. Egg-laying P. rapae discrimi- nate between potential host plants using visual cues before alighting (Jones, 1977; Ives, 1978; Myers, 1985) and using leaf surface chemicals detected by chemoceptors on the tarsi after alighting (Renwick and Radke, 1988). Manipulated cage and field experiments have demonstrated that P. rapae females distinguish between cabbage varieties and plants of the same va- riety. Intravarietal preferences are for plants that are larger (Ives, 1978), greener [associated with a higher nitrogen and water content (Myers, 1985)], and located at crop edges (Jones, 1977) and for leaves with acceptable bal- ances of attractants and deterrents (Chew and Renwick, 1995). These studies exposed egg-laying females to plants that contrasted in certain characteris- tics, thus discrimination between crop plants on host preferences in working farm environments (i.e., large-scale cabbage monocultures of uniform age) requires further investigation. It has been suggested that studies of host selection will benefit from ap- proaches that consider plant physiological activity (Hern et al., 1996). P. rapae is one of only a few phytophagous invertebrates that have been included in studies that measured gas exchange activity of host plants during oviposition. Myers (1985) found that P. rapae females deposited more eggs on recently watered cabbage plants that had characteristically higher transpiration rates. In contrast, another lepidopteran pest (Ostrinia nubilalis; the corn borer moth) allocated eggs to leaves which contained preferred concentrations of P1: VENDOR/GAY P2: GCP/GDW/GGN Journal of Insect Behavior [joib] PP199-341427 June 24, 2001 8:38 Style file version Feb 08, 2000 Egg-Laying Behavior and Plant Gas Exchange Activity 461 specific mineral nutrients, and not to plants with higher photosynthetic rates (Phelan et al., 1996). In one lepidopteran, a mechanism has been discovered for detection of photosynthetic activity: during egg-laying the nocturnal moth (Cactoblastis cactorum) uses its labial palp organ (LPO) to detect CO2 gradi- ents associated with the photosynthesis of a CAM plant (Stange et al., 1995). In common with many Lepidoptera, P. rapae possess an LPO with high con- centrations of sensillae which may be capable of detecting CO2 gradients (Lee et al., 1985). However, there is little known about the generality of CO2 detection among the Lepidoptera and how it may relate to host plant choice (Stange, 1996). Recent innovations in the development of portable infrared gas analyzers provide a tool for ecologists to make nondestructive measurements of gas exchange activity of specific areas of leaves in the field. When high intensities of light are used to saturate leaf surfaces, this tech- nique provides an indication of the potential of leaf areas for exchange of CO2 (photosynthesis) and H2O (transpiration). This study investigates how photosynthesis, transpiration, size, and injury level of cabbage plants are associated with host plant preferences in cabbage monocultures by P. rapae. MATERIALS AND METHODS Oviposition behavior of P. rapae was recorded between 1100 and 1600 BST from 27 July to 18 August 1995 in a late cabbage crop (var. Slawdena) grown at Barton Moss Farm, Irlam, Manchester (2250N, 53 280W). The first observations were made at an early stage of crop growth, 24 days after transplantation (DAT). Females exhibiting egg-laying behavior were pursued by a single observer and all positions of contact with plants (consid- ered to be investigation by the female) were marked with a numbered peg (following Jones, 1977) and a pole to facilitate relocation. Within 30 min the width (minor axis) of the largest leaves and the presence of butterfly eggs or larvae of marked plants were recorded. The minor axis of the largest leaves of harvested var. Slawdena plants correlated well with their total leaf area (rS = 0.767, P = 0.027, n = 8) but not their height (rS = 0.132, P = 0.863, n = 8). Rates of photosynthesis and transpiration of plants contacted dur- ing egg-laying flights were measured using a portable infrared gas analyzer (LCA3; Analytical Development Company, Hoddesdon, UK) used in the differential mode. Air was dried as it entered the analyzer to reduce error 2 in CO2 measurements. The cuvette (PLC-B; containing an area of 625 mm ) was positioned over the leaf area surrounding the egg or position of contact. A second measurement of gas exchange activity was taken, as representative of the plant, from the apex of the largest leaf that exhibited no evidence of senescence. Using nondestructive hand searches, the numbers of P. rapae P1: VENDOR/GAY P2: GCP/GDW/GGN Journal of Insect Behavior [joib] PP199-341427 June 24, 2001 8:38 Style file version Feb 08, 2000 462 Langan, Wheater, and Dunleavy eggs and larvae on each plant were recorded. For comparison with crop plants that were not visited during egg-laying, 10 randomly located plants in close proximity (<20 m) were inspected to measure the same characteristics as examined during oviposition observations. Many variables measured during the observation of egg-laying runs failed to conform to the assumptions of parametric tests, i.e., were skewed and/or failed to conform to Levene’s test for homogeneity of variances. In addition, sample sizes were unbalanced. Consequently, rank means tests (Meddis, 1984) were used for comparisons between plants that were rejected after alighting and those that received eggs. To account for variation between butterflies (see Papaj and Rausher, 1983), data were blocked by individual. Chi-square tests were used to determine whether egg-laying females avoided plants already supporting conspecific eggs or larvae, a scenario which would reduce the likelihood that plants were selected more than once. Chi-square tests were also used to provide an in- sight into the sequential nature of oviposition runs. To decipher whether pre- vious oviposition events influenced egg-laying decisions (i.e., whether there were differences from a rejected plant to an accepted plant, and vice versa), 2 2 contingency tables were constructed examining plants that were pre- viously accepted and later either accepted or rejected against factor values (e.g., photosynthetic rate) that were higher or lower than at the previous event. To determine whether eggs were aggregated on plants, the distribu- tion of P. rapae eggs on plants during peak densities of the second generation was compared against a random (Poisson) distribution on the basis of equal plant susceptibility. A second approach was implemented to compare plants based on the presence of P. rapae eggs. Surveys of 96 randomly located crop plants were carried out during peak densities of the second and third generations of P.
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