Effects of leaf nitrogen content on oviposition site selection, offspring performance, and intraspecific interactions in an omnivorous bug

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1 Ecological Entomology (2006) 31, Effects of leaf nitrogen content on oviposition site selection, offspring performance, and intraspecific interactions in an omnivorous bug RONNY GROENTEMAN 1, MOSHE GUERSHON 2 and M O S H E COLL Department of Entomology, The Hebrew University of Jerusalem, Israel Abstract. 1. Oviposition site preference and its relation to offspring performance have received much attention in studies of herbivorous insects. Although this relationship is of great ecological significance, its presence in predacious and omnivorous insects has hardly been explored. When selecting an oviposition site, omnivores are expected to respond to both prey availability and, even more strongly, to plant traits that affect both females and their offspring. 2. In this study, females of Orius albidipennis (Heteroptera: Anthocoridae) showed a strong preference for oviposition at the vein origin site of cotton leaves. It appears that this site is a limited resource for ovipositing females, because they defend it against conspecific intruders. This defensive behaviour was significantly more pronounced on nitrogen-rich than nitrogen-poor plants. 3. The females defensive behaviour on nitrogen-rich leaves corresponds with offspring performance; the nymphs developed faster and enjoyed higher survival on nitrogen-rich than on nitrogen-poor leaves. At the between-plant level, oviposition preference was not significantly correlated with offspring performance, and egg hatching rate did not differ significantly between nitrogen treatments. 4. Oviposition site selection by this omnivorous bug appears, however, to be correlated positively with offspring performance at the within-leaf level. This is supported by the significantly higher hatching success of eggs deposited at the preferred vein origin site as compared with those deposited on other parts of the leaf. Key words. Omnivore plant interactions, omnivory, Orius albidipennis, oviposition preference offspring performance, resource guarding. Introduction The relationship between oviposition site selection by adults and the performance of their offspring has received much attention in the ecological literature (Craig et al., Correspondence: Ronny Groenteman, School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand. rgr51@student.canterbury.ac.nz 1 Present address: School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand. 2 Present address: Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, Tel Aviv, 69987, Israel. 1989; Thompson & Pellmyr, 1991). It has been argued that eggs should be deposited where optimal conditions exist for the offspring (Jaenike, 1978). This linkage between oviposition preference and offspring performance is expected particularly when parental care is absent and offspring mobility is low. Under such conditions, offspring fitness should be correlated strongly with characteristics of the egg deposition site. Indeed, a positive correlation between female preference for oviposition sites and offspring performance was detected in many studies, primarily for herbivorous insects (Craig et al., 1989; Stein & Price, 1995; Craig & Ohgushi, 2002). In some cases, however, no such correlation was detected (some recent examples include Berdegue et al., 1998; Lamb et al., 2003; Scheirs et al., 2003, and references therein). One possible Journal compilation # 2006 The Royal Entomological Society 155

2 156 Ronny Groenteman, Moshe Guershon and Moshe Coll explanation for this lack of correlation was offered by Scheirs et al. (2000), who pointed out that females act to maximise their fitness not only through offspring performance, but through their own performance as well. Whitham (1978, 1980) found that females of the gall aphid Pemphigus betae indeed maximise their overall fitness; stem mothers prefer to establish galls at sites on the leaves that support more offspring. Adult females should therefore preferentially inhabit host plants that will increase their own longevity and fecundity rather than those that improve offspring performance (Evans, 1976; Coll & Ridgeway, 1995; Nakashima & Hirose, 1999). A conflict could result when, for example, the nutritional needs of ovipositing females and their offspring are not the same (Evans, 1976). While much is known about the relationship between oviposition preference and offspring performance in herbivorous insects (Jaenike, 1978; Thompson, 1988; Craig et al., 2000; Scheirs et al., 2000; Kanno & Harris, 2002), relatively little is known about this relationship in predators. Some predators deposit their eggs where prey is concentrated (Hagen et al., 1999). Others oviposit away from prey (Schellhorn & Andow, 1999), possibly relying on the high mobility of the hatching young. However, a rigorous exploration of the relationship between offspring mobility and oviposition strategy in predators has not yet been attempted. Even less is known about the oviposition preference offspring performance relationship in omnivorous insects that feed on both prey and plant food sources (but see Coll, 1996). Omnivory is widespread in nature, and may be exhibited by most consumers during at least one of their life stages (Pimm & Lawton, 1978; Whitman et al., 1994; Coll & Guershon, 2002). These consumers are therefore expected to respond to both plant characteristics and prey availability when choosing an oviposition site. Nitrogen content of host plants often limits the development and fecundity of herbivorous insects (McNeill & Southwood, 1978; Denno & Roderick, 1990) and there is much evidence to indicate the preference of insects for nitrogen-rich plants (e.g. Valladares & Lawton, 1991; Kyto et al., 1996; Jauset et al., 1998; Barros & Zucoloto, 1999). Little is known, however, about the effect of nitrogen content on oviposition site selection in omnivorous insects. It is not clear, for example, whether omnivorous consumers that feed on nitrogen-rich prey are responsive to variations in nitrogen content of their food plants. Plant chemical composition influences omnivore performance through nutritional and allelochemical effects (see examples in Naranjo & Gibson, 1996; Coll, 1998; Coll & Guershon, 2002). Additionally, plant tissue structure affects the ability of omnivores to feed on and oviposit in plant materials. Unlike strict predators, omnivorous females are able to evaluate the nutritional and structural properties of the oviposition substrate, the plant. Plant characteristics are especially important to the performance of omnivore offspring, because many of them feed exclusively on plant material during the first nymphal stages (Parker, 1981). It was therefore hypothesised that omnivorous females strongly prefer to deposit their eggs on plants of high nutritional value for their offspring. This prediction was tested by manipulating the quality of cotton plants using different nitrogen fertilisation regimes, and quantifying its effect on female oviposition and offspring performance in the omnivorous bug Orius albidipennis Reuter (Heteroptera: Anthocoridae). The relation between omnivore oviposition preference and offspring performance was tested on two spatial scales, between plants of different nutritional value, and between areas within a leaf. Whether preferred oviposition sites are limited was inferred in this study from intraspecific interactions among gravid females at these sites. Materials and methods Plants and insects Cotton plants, Gossypium hirsutum (cv. Acala SJ2), were grown individually from seeds in an inert rooting mixture (Vermiculite 2 Ò ) in 200-ml pots in the greenhouse. An O. albidipennis culture was established from about 50 females that were collected in the spring of 2000 from sunflower heads in the Arava valley in southern Israel, and maintained at 25 1 C, 70 10% RH, and LD 16:8 h following the protocol of Schmidt et al. (1995). In the culture, the omnivores were fed Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs. Bean pods were provided for moisture, to supplement the bugs diet, and to serve as an oviposition substrate. Female behaviour To assess the significance of different leaf areas for O. albidipennis females, their behaviour on leaves was observed. To that end, we randomly collected seven 6 1-day-old mated females from the colony and placed them individually on intact cotton leaves, in ventilated Petri dishes. Four Helicoverpa armigera eggs were offered to the females as prey on the underside of each leaf and the bugs were then observed continuously for 8 h. Time allocated by the females for walking, standing, feeding, and other behaviours (mainly preening) was recorded. The location of the females, whether on the upper or lower leaf surface, at the vein origin site, on the leaf lamina, or on the dish, was also noted. w 2 tests (SAS, 2001) were used to compare event frequencies. Leaf nitrogen content Cotton plants were irrigated with tap water until the threenode stage, and then assigned randomly to either rich or poor nitrogen fertilisation regime. The composition of the watering solutions is provided in Table 1 (following Epstein, 1972). Leaf nitrogen content was determined for eight randomly selected leaves from each treatment, following methods described by Smith (1980).

3 Oviposition site selection by an omnivore 157 Table 1. Composition of irrigation solutions used to manipulate nitrogen content of cotton leaves. Component (concentration in M) Oviposition site selection To evaluate the effect of leaf nitrogen content on the within-leaf oviposition site selection, we randomly collected 20, 6 1-day-old mated O. albidipennis females from the culture and placed them individually in Petri dishes containing an intact nitrogen-rich cotton leaf or a nitrogenpoor leaf. The females were supplied with E. kuehniella eggs ad libitum and were allowed to oviposit for 6 days. To prevent cannibalism on newly hatched nymphs by adult females, the leaves were replaced on the third day of the experiment. At the end of the experiment, the number of eggs and their location on the leaves were recorded. Two zones were recognised on each leaf: the vein origin within a 0.5 cm radius from the petiole, and the rest of the leaf lamina. The area of each leaf zone was measured and used to calculate egg density per cm 2 per day per female. Cumulative number of eggs deposited per female per day at the two leaf zones was also calculated. Data were analysed using ANOVA with a split-plot model (SAS, 2001), with nitrogen treatment as the whole plot effect, and leaf zone as the subplot level. Egg-bearing leaves were observed for an additional 5 days to determine hatching rate. These results were then analysed together with results of the egg hatching experiment below. Egg hatching success Nitrogen rich (ml l 1 distilled water) 2.0 KNO Ca(NO 3 ) MgSO (NH 4 )H 2 PO KCl CaCl NaH 2 PO Koratine Òa Nitrogen poor (ml l 1 distilled water) a Contains the following microelements (g l 1 ): Fe, 5.5; Mn, 2.7; Zn, 1.35; Cu, 0.2 and Mo, 0.5. To determine differences in hatching rate between eggs deposited at the two leaf zones, single O. albidipennis females were placed together with intact leaves from either one of the two nitrogen treatments (seven nitrogen-rich and nine nitrogen-poor leaves) in Petri dishes. The females were allowed to oviposit for 3 days. The number of eggs deposited in the two leaf areas (vein origin and leaf lamina) was determined for each female. The eggs were allowed to hatch for five additional days, after which the hatching success (proportion of hatched eggs) in different zones of nitrogenrich and nitrogen-poor leaves was determined. To assess the effects of nitrogen fertilisation regime and oviposition site on hatching success, data were arcsine of square root transformed to homogenise variances and then subjected to ANOVA with a split-plot model (nitrogen treatment as the whole plot and leaf zone as the subplot) (SAS, 2001). Nymph performance In this experiment, the effect of leaf nitrogen content on offspring performance was evaluated. Nymph performance at the vein origin site and the leaf lamina were not compared, because this comparison is not likely to be of biological importance in view of the high mobility of the nymphs. Bean pods bearing 2 1-day-old eggs were collected from the O. albidipennis culture and held at 25 1 C until nymphs emerged. The pods were inspected every 2 h, and newly hatched nymphs were used in the experiment. Intact nitrogen-rich and nitrogen-poor leaves were enclosed singly in Petri dishes at 25 1 C. On each leaf, four first-instar nymphs were enclosed individually in plastic tubes (0.12 cm diameter 0.7 cm height) attached to the underside of the leaf with modelling clay. This way, the nymphs were held individually to prevent cannibalism. The nymphs were inspected every 4 10 h over the course of 2 days. At each inspection, survival (alive or dead) and developmental stage (first or second stadium) were recorded for each nymph. The observations were terminated when a nymph reached the second stage, which was recognised by a change in body shape and transparency, and the presence of exuvium. The experiment was replicated three times for a total of 12 nymphs for each nitrogen fertilisation treatment. Per cent mortality on nitrogen-rich and nitrogen-poor leaves was analysed using ANOVA with nymphs nested within leaves. Duration in hours of the first instar on the two nitrogen treatments were compared with a Student t-test (SAS, 2001). Female survival Female survival on nitrogen-rich and nitrogen-poor leaves was recorded daily during the oviposition site selection experiment above. As stated, the 20, 6 1-day-old females were provided with E. kuehniella eggs ad libitum and were held individually for 6 days on either nitrogenrich or nitrogen-poor cotton leaves. The females had no opportunity to cannibalise nymphs because leaves were replaced before egg hatching. Female Orius do not feed on conspecific eggs that are imbedded in leaf tissue (Collyer, 1953; Askari & Stern, 1972; R. Groenteman, pers. obs.). Female survival on nitrogen-rich and nitrogen-poor leaves were compared using a Student t-test (SAS, 2001). Intraspecific interactions Interactions between O. albidipennis females were recorded to assess whether preferred leaf settling sites constitute a

4 158 Ronny Groenteman, Moshe Guershon and Moshe Coll limited resource for the females. Mated, 6 1-day-old female bugs (n ¼ 20) were randomly collected from the culture and placed individually in Petri dishes (9 cm in diameter) containing an intact either nitrogen-rich or nitrogen-poor cotton leaf. After a 20-min acclimation period, during which most females settled on the leaves, a second female, labelled as the intruder, was introduced into each dish. Interactions between the two females were observed and the outcome was recorded. The female that remained at the interaction site was declared the winner, while the one that left the site was designated the loser. When both females remained or both left the site, a draw was declared. The proportion of spontaneous settling at the vein origin site and the proportion of victories achieved by owners and intruders on nitrogen-rich and nitrogen-poor leaves were analysed using w 2 tests (SAS, 2001). Relative size of the interacting females, expressed as head and prothoracic widths and the length of the fore tibia, was recorded, and the correlation of these parameters with interaction outcome was w 2 tested (SAS, 2001) for the effect of size on the likelihood of winning the interaction. Results Female behaviour Standing on the underside of the leaf was the most frequent behaviour exhibited by the females; it occurred in 73% of the events (w 2 3 ¼ 42.97, P < 0.001). In 40% of the cases where females stood on the underside of the leaves, they did so at the vein origin. These results indicate that females occupy the vein origin site over 30 times more frequently than would be expected based on the differences in size between the vein origin and leaf lamina sites. Leaf nitrogen content Fertilisation regime had a significant effect on leaf nitrogen content (t 14 ¼ 11.31, P < 0.001). Leaves of plants grown under a poor regime had a significantly lower nitrogen level than those that received nitrogen-rich fertilisation (mean SE: % and % nitrogen of dry weight respectively). Oviposition site selection Females deposited significantly more eggs per leaf area at the vein origin site than on the lamina (F 1,18 ¼ 45.19, P < 0.001, Table 2). Nitrogen fertilisation regime did not significantly affect the overall number of eggs deposited per female per day ( and on nitrogenrich and nitrogen-poor leaves respectively; F 1,18 ¼ 0.501, P ¼ 0.488), and no significant interaction was detected in the effects of nitrogen level and leaf site on oviposition rate (F 1,18 ¼ 0.33, P ¼ 0.575). Egg hatching success Hatching success was significantly higher at the vein origin site than on the leaf lamina in both nitrogen regimes. Whereas % and % of the eggs in the vein origin site hatched on nitrogen-rich and on nitrogenpoor leaves respectively, only % and % of the eggs hatched on the leaf lamina of nitrogen-rich and nitrogen-poor leaves respectively (F 1,36 ¼ 15.83, P < 0.001). Nitrogen fertilisation regime did not affect hatching success significantly (F 1,32 ¼ 1.88, P ¼ 0.18) and there was no significant interactive effect between nitrogen regime and leaf site (F 1,36 ¼ 0.159, P ¼ 0.69). Nymph performance Duration of the first instar was significantly shorter on nitrogen-rich than on nitrogen-poor leaves ( and h respectively; t 5 ¼ 3.59, P ¼ 0.016). Although nymphs survived longer on nitrogen-rich than on nitrogen-poor leaves ( and h respectively), this difference was not statistically significant (F 1,20 ¼ 2.57, P ¼ 0.137). Female survival and behaviour Female survival time did not differ significantly on leaves from the two nitrogen regimes ( and days on nitrogen-rich and nitrogen-poor leaves respectively; t 39 ¼ 1.59, P ¼ 0.12). Intraspecific interactions Mated O. albidipennis females displayed a tendency to settle spontaneously at the vein origin site. This tendency (measured as frequency of settling events) was stronger on nitrogen-rich leaves than it was on nitrogen-poor ones (w 2 19 ¼ 3.2, P ¼ 0.07 and w 2 19 ¼ 1.8, P ¼ 0.18 Table 2. Density (means 1 SE) of Orius albidipennis eggs deposited in two areas of cotton leaves grown under two nitrogen fertilisation regimes. Eggs (no. cm 2 ) a Site on leaf Area (cm 2 ) Nitrogen rich Nitrogen poor Vein origin b a a Leaf lamina c b b a Values within columns followed by the same letter do not differ significantly (Student t-test, P < 0.001). Values within rows do not differ significantly. b An area of 0.5 cm diameter tangent to the petiole. c An area 4 cm diameter tangent to the petiole, excluding the vein origin site.

5 Oviposition site selection by an omnivore 159 respectively). Moreover, females that settled at the vein origin site on nitrogen-rich leaves prevailed in conspecific contests significantly more often than did the invading females. This, however, was not the case on nitrogen-poor leaves; on these leaves, settled and invading females had a similar chance of winning conflicts (w 2 19 ¼ 6.25, P ¼ 0.01 and w 2 19 ¼ 2.57, P ¼ 0.1 on nitrogen-rich and nitrogenpoor leaves respectively). The relative size of the interacting females did not correlate with their chance of winning. Larger females were not more likely to win the interaction on both nitrogen-rich and nitrogen-poor leaves. w 2 values for differences in prothoracic size are given; head and fore tibia sizes act in the same manner (w 2 1 ¼ 2.2, P ¼ 0.14 and w 2 1 ¼ 0.03, P ¼ 0.88, on nitrogen-rich and nitrogen-poor leaves respectively). Discussion In this study, O. albidipennis females showed a strong preference for oviposition at the vein origin sites of cotton leaves. Results indicate that oviposition site selection by this omnivorous bug is correlated positively with offspring performance at the within-leaf level. Nitrogen content of cotton leaves did not affect oviposition rate by O. albidipennis; a similar number of eggs were deposited per female on nitrogen-poor and nitrogen-rich plants. In another omnivorous anthocorid, Anthocoris confusus, however, young bean pods were preferred over old pods for oviposition (Evans, 1976), perhaps in response to a difference in nitrogen content in old vs. young plant tissues (Mattson, 1980). Although no significant effect of leaf nitrogen content on egg deposition was detected in the present study, first-instar O. albidipennis nymphs developed more rapidly and survived longer on nitrogen-rich leaves than on nitrogen-deficient ones. Several studies on omnivorous Heteroptera have shown that the quality of the food plant greatly affects the performance of young nymphs. For example, Naranjo and Stimac (1985) showed that low quality food plants (foliage) enabled Geocoris punctipes to develop only to the second instar, while higher quality plants (bean pods) allowed the development up to the third instar. Contrary to its effect on the young nymphs, leaf nitrogen content did not have a significant effect on female longevity or egg deposition. This result may be attributed to the free access the females had before the experiment to prey, a high nitrogen food source. Evans (1976) suggested that A. confusus females insert their rostrum into plant tissue to determine the suitability of the plant for oviposition. In Orius insidiosus, which feeds mostly in the xylem with some evidence of mesophyll feeding (Armer et al., 1998), both moisture and nutrient levels could be detected by the females. Data show that significantly more eggs were deposited per cm 2 at the vein origin site than on the leaf lamina. The ability of O. albidipennis females to distinguish between structures within the leaf and preferentially deposit their eggs at particular sites appears to be correlated with egg hatching success. It seems that the eggs are inserted into the most succulent part of the leaf to reduce risk of desiccation (Richards & Schmidt, 1996). A similar preference for petioles and main leaf veins as oviposition sites has been reported for other Orius species (Askari & Stern, 1972; Tawfik & Ata, 1973a, b; Richards & Schmidt, 1996). These results suggest therefore that oviposition site selection is influenced primarily by water balance rather than nutritional requirements, because leaf nitrogen level did not have a significant influence on the number of deposited eggs or on their hatch rate. That the females select oviposition sites that maximise the hatch rate of deposited eggs rather than to optimise nymph performance may be related to the high mobility of the neonates and their ability to search for food away from the egg hatching site. Nymphal food may include not only prey items but also plant material, such as pollen (Kiman & Yeargan, 1985; Cocuzza et al., 1997; Vacante et al., 1997). In the gall aphid Pemphigus betae, in contrast, nymphs are totally restricted to their gall and cannot alter their feeding site until adulthood. In a classic study, Whitham (1978, 1980) demonstrated that females show strong preference for oviposition (gall forming) sites on the leaf most suitable for the nymphs. Aggregated aphid nymphs often exhibit mutual facilitation to increase the quality of their food source (Freese & Zwo lfer, 1996). In strict predators and in omnivores, however, preference for optimal oviposition sites may be counteracted by potential aggressive and cannibalistic behaviours. The preference of O. albidipennis for the vein origin site of the leaf was also apparent from the behaviour of females. Mated females were frequently observed standing at the vein origin site on the lower surface of cotton leaves. Orius tristicolor has also been reported to prefer this resting site (Shields & Watson, 1980). The bugs actively seek the vein origin site, and once it is found they remain there, inactive, for extended periods. Furthermore, mated O. albidipennis females that spontaneously settled at the vein origin site of cotton leaves actively defended it against other females. These antagonistic interactions were significantly stronger on the nitrogen-rich leaves. That the females primarily defend the vein origin site as an oviposition site rather than a resting site is strongly suggested by preliminary data that indicate that males and unmated females do not settle spontaneously at this site and are not likely to defend it successfully (R. Groenteman and M. Guershon, unpublished data). Aggressive interactions for preferred reproduction sites on the leaves were also recorded for the gall aphid P. betae (Whitham, 1980). Unlike the current study, however, female size mediated contest outcome, with larger stem mothers usually taking over the preferred site on the leaf. In the current study, variation in size between gravid females appears to be less important for contest outcome, maybe because of their predatory habits. The insertion of the eggs in plant tissue may protect them not only from desiccation, but from predation as well. In Anthocoris confuses, another family member with a similar

6 160 Ronny Groenteman, Moshe Guershon and Moshe Coll oviposition strategy, eggs that were deposited loosely on the plant surface were preyed upon by the ovipositing females themselves (Evans, 1976). In this species, which is apparently more prey-dependent than Orius sp., more loose eggs are deposited and higher egg predation occurs when prey is scarce. In a companion study, it was observed that female O. albidipennis deposit more loose eggs on the leaf surface when more females compete for the preferred oviposition site, the vein origin (R. Groenteman, pers. obs.). These eggs may then be more vulnerable to predation. The guarding behaviour exhibited by females at the vein origin site is likely to reduce the number of loose eggs and result in clustered deposition of sibling eggs. It would be interesting to investigate the impact of egg clustering, either sibling or conspecific, on female reproductive success. Strict predators rely on a nitrogen-rich prey diet, and ovipositing females may therefore respond to prey availability. In many cases, however, prey availability varies greatly in space and time, making it difficult for ovipositing females to predict prey availability for their offspring. Omnivores, however, feeding on both plants and prey, may capitalise on their ability to assess the quality of plant resources, as these often change more slowly than does prey availability. Omnivores may therefore respond primarily to variations in host-plant quality, which may be a better predictor of nymph performance. Further, omnivores and their herbivorous prey may respond in similar ways to variations in plant quality, resulting in a spatial or temporal overlap in their distributions. A similar oviposition strategy is probably exhibited by at least some of the strict predators and the omnivores that were found to oviposit near prey aggregations; they may actually be responding to variations in plant quality, be it by taste (in omnivores) or smell, in a way similar to that of their herbivorous prey. Oviposition site selection that enhances offspring performance in omnivores and strict predators is likely to greatly influence their ability to suppress prey populations on various host plants. Acknowledgements We thank T. Yuval and A. Yigael for technical assistance, R. Yonah for help with manuscript preparation, and R. Yonah, B. Yuval and two anonymous reviewers for valuable comments on its drafts. References Armer, C.A., Wiedenmann, R.N. & Bush, D.R. (1998) Plant feeding site selection on soybean by the facultatively phytophagous predator Orius insidiosus. Entomologia experimentalis et applicata, 86, Askari, A. & Stern, V.M. 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