Evolutionary Ecology, 1994, 8, 188-195

Pollen availability, seed production and seed predator clutch size in a tephritid-thistle system

R. G. LALONDE* and B. D. ROITBERG Behavioural Ecology Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada V5A 1S6

Summary

We develop a simple model explaining clutch size behaviour of Orellia ruficauda on its principle host in North America, Cirsium arvense. Offspring of flies feed solely on thistle seeds and seed production is pollen- limited. Thus, female flies risk reduced offspring fitness when committing large clutches to hosts (female flower heads) occurring in localities where male plants are locally absent. We therefore predict that attacked hosts will contain fewer eggs in such localities, a prediction that is consistent with data obtained in the field: large clutches are never laid in flower heads in low-pollination localities. However, larvae reared from such low-quality hosts are significantly smaller on average and will therefore carry smaller egg loads as adults. Small clutches in poor-quality hosts may thus be an expression of lower per-adult fecundity. Nevertheless, sufficient numbers of large, fecund flies are produced in low-pollination localities to make this last explanation less convincing. Keywords: Canada thistle; pollen limitation; tephritid

Introduction

The success of parasitic insect larvae depends upon choices made by adults at the time of oviposition. As accurate an assessment of a host's quality as is possible should be made to obviate the consequences of an overly optimistic or pessimistic assessment. An overestimate of a host's quality may result in a large clutch of eggs and reduced availability of food for offspring. Conversely, an underestimate, while ensuring a higher probability of offspring survival, will presumably lead to spending too much time searching to be able to locate hosts for all of her eggs (Roitberg, 1990). In fact, many parasites that exploit insect and plant hosts do facultatively adjust dutch size and apparently base this decision on simple host assessment rules. For example, parasitic insects frequently exploit the often close relationship between a host's size and its capacity to support a parasite's offspring and will allocate more eggs to larger hosts (Zw61fer and Preiss, 1983; Schmidt and Smith, 1985; Zw61fer, 1985; Papaj, 1990). Similarly, easily assessed indicators of host plant vigour such as colour may provide accurate information to a parasite (Myers, 1985). Proximate cues to host quality are not always so reliable or obvious, however. Seed predatory insects may assess host quality in different ways, depending upon what limits seed production in the host. If the host is typically resource-limited, general cues indicating an individual host's relative vigour can reliably indicate higher seed production and elicit a higher attack rate from seed predators (Zimmerman, 1980; Brody, 1992a,b). However, individuals in a population of pollen-limited hosts may be vigorous and yet set few seeds if pollen sources are

*To whom correspondence should be addressed at: Department of Biology, Okanagan Univ. Coll., Kelowna, B.C. Canada V1V 1V7. 0269-7653 © 1994 Chapman & Hall Seed predator clutch size in a tephritid-thistle system 189 distant (Bierzychudek, 1981; Hainsworth et al., 1985; Lalonde and Roitberg, 1993). In this situation the local presence of a pollen source may be the most reliable indicator of a host's quality. In some systems of this sort, seed predators have reduced the effect of pollen limitation on host quality by becoming pollinators (Janzen, 1979; Wiebes, 1979). In this paper we examine how infestation of the seed predatory tephritid, Orellia ruficauda in its host, Canada thistle (Cirsium arvense) may be affected by the availability of pollen. In Europe, O. ruficauda attacks flower heads of several non-dioecious species of thistles (Anger- mann, 1986) and their host exploitation behaviour is apparently different from that expressed by North American flies (H. Zw61fer, personal communication), but in North America these flies only attack the female flower heads of C. arvense (McFadden and Foote, 1960). Reproductive success of O. ruficauda flies depends upon the quantity of fertilized seeds available in the host flower head (Lalonde and Roitberg, 1992a). Heads vary strongly in their ability to support larval development, in an apparently unassessable way: flies oviposit early in flower head development (Lalonde and Roitberg, 1992b) and, whereas a flower head's size is a partial predictor of its quality as a host, much more of the variation in host quality is explained by seed mass, pollination success and abortion rate (Lalonde and Roitberg, 1989, 1992a). Flies do not allocate more eggs to large hosts (Lalonde and Roitberg, 1992a). We suggest that from the flies' perspective, the amount of resources that will eventually be present in a host of any size is probably an expectation. An intuitive prediction is that O. ruficauda females can maximize the probability that each of their offspring will have sufficient food for development by limiting clutch size. However, given some estimate of how host quality varies, we can quantify offspring success with respect to clutch size. From this, it is possible to make more specific predictions of how host variation will affect parental behaviour.

Offspring success with uncertain resources The per-offspring fitness returns from a clutch of c eggs, laid into a head that has R resources (i.e. f(c,R)) will be maximal as long as R represents a resource level that is greater than or equal to the amount necessary to support c larvae up to a maximum size. Larval densities in excess of food availability will presumably make all individuals undersized, since contest competition does not apparently occur in O. ruficauda (Lalonde and Roitberg, 1992a,b). Per-offspring fitness levels will thus decline when R is less than c. Given some estimate of the frequency distribution of host quality in a locality, we can solve the expected per-offspring fitness returns from a clutch, c, laid into a randomly encountered seed head by summing offspring success for all possible resource states. The expected success of a larva in a clutch of c eggs (%(c)) is thus the summation for all R, of the product of the probability that R resources will be present, p(R) and the fitness expected from a clutch of c eggs sharing R resources, f(c,R) (Yoshimura and Shields, 1987; Lalonde, 1991a). Thus,

= 0p(R) f(c,R) (1) Canada thistle is dioecious and pollen-limited (Amor and Harris, 1974). Because of this, the mean amount of seed that can be expected in a host head will be predictably smaller in localities where male thistles are locally absent (Amor and Harris, 1974; Lalonde and Roitberg, 1993). Flies recognize male thistle heads as non-hosts (Lalonde and Roitberg, 1992a). Therefore, female flies can potentially establish whether male plants are locally present or absent. In this paper, we employ data obtained in the field and Equation (1) to numerically calculate the returns expected from parasitizing hosts in localities where pollen donors are either locally present or absent. From this we predict that O. ruficauda should be much less prone to allocating large clutches to flower 190 Lalonde and Roitberg heads of female plants when male thistles are locally absent. We then present data obtained from field samples that are consistent with this hypothesis.

Materials and methods

Twenty-three sites containing female thistle shoots infested by O. ruficauda were sampled at several locations on the lower mainland of British Columbia near the city of Vancouver. Sixteen of these sites also had male thistles interspersed with female thistles and at the remaining seven, male thistles were locally absent (no male shoots were nearer than 50 m to the point of sampling). At each site a cohort of at least 50 female flower heads (all heads which had just begun to flower and were therefore in the same phenological stage and subject to fly attack at the same time) were tagged. To ensure that no fertile seeds would be released prior to sampling, sites were visited approximately 1 week after tagging to ensure complete pappus growth and all tagged heads were bound shut with plastic twist ties. Tagged flower heads were sampled when the bracts enclosing all heads had opened, indicating that seed release would normally have taken place. Sampled heads were dissected and all fertilized, healthy seeds were counted and weighed collectively to the nearest 0.1 mg. Any insect-damaged seeds were counted and their mass was estimated from the mean mass of unattacked seeds in that head. Total seed mass was estimated as the sum of healthy and insect-attacked seeds. All third instar maggots were counted and weighed to the nearest 0.1 mg. Even if all had died prior to attaining third instar, the number of larvae present in the head was measurable because each first instar larva elicits hypertrophied growth in one immature ovule, the remains of which are always present in the mature head (Lalonde, 1991b). We show elsewhere (Lalonde and Roitberg, 1992a), that the number of larvae present in the head measured in this manner is not significantly different from the number of eggs present. Thus, we are confident that our counts of larvae per head are an accurate measure of eggs laid per head.

Results and discussion

We used a regression model (larval mass = seed mass consumed x 0.554 - 0.024) (Lalonde and Roitberg, 1992a) to calculate the number of larvae that each seed head could support to modal mass (5.7 mg) in each sampled seed head. The distribution of resources in flower heads within the two types of locality (high- (male thistles present) and low-quality (males absent)) showed strong differences (Fig. 1). We then used these estimates, the relationship between mature mass and fecundity (Lalonde and Roitberg, 1992b) and Equation (1) to calculate the fitness expected from laying a given clutch of eggs into a randomly encountered flower head in one of the two types of locality. Figure 2 illustrates each egg's expected fitness resulting from a parent's decision to lay a given dutch of eggs into a randomly encountered flower head. The upper curve represents the returns expected when a fly forages for hosts in a high-quality locality and the lower curve represents the returns expected in a low-quality locality. Note that eggs laid into flower heads in high-quality localities experience diminishing returns with increasing clutch size, but that this effect is not strong at clutch sizes of less than four eggs (a larva that shares a high-quality host with three others can expect over 90% of the resources that a solitary larva can garner). In contrast, eggs laid in flower heads in low-quality localities immediately experience strong diminishing returns with increased clutch size (a larva in a two-egg clutch can expect less than 80% of the resources Seed predator clutch size in a tephritid-thistle system 191

40 ,° t • High Pollination ] [] Low Pollination O 30

O 20

0 0 2 4 6 8 10 12 14 # of Larvae Able to Mature Figure 1. Distribution of female flower heads expressed in terms of available food for larval development. Units are in terms of number of larvae that can attain a mature mass of 5.7 mg (the population mode). Heavily shaded bars represent this distribution in high-quality localities (pollen donors present) and light bars represent individual quality distribution in low-quality localities (pollen donors absent).

(/1 ,. I .0, U ~>~0)o(~)= ~ p (R) tic ,R) (J " 0.8' C ~c~ High Pollination •Q.r- 0.6 ~ ~es present) u,..c/) q,. o 0.4

-'i "o 0.2. Low Pollination L; (males absent) --= 0.0 5 10 15 Clutch Size Figure 2. An individual offspring's expected fitness, relative to one attaining modal mass, with respect to the number of other larvae sharing the host's resources. Open circles: in high-pollination localities; closed circles: in low-pollination localities. obtained by a single larva). The costs associated with committing many eggs to each clutch are clearly greater in low-quality localities than they are in high-quality localities. Infestation patterns apparently reflect this. Flies commit significantly fewer eggs to individual host heads in low-pollination environments than to heads located where male thistles are locally present (Mann-Whitney U-test, p = 0.0002). One factor that might well cause individual female flies to commit more eggs to each host is the rarity of unattacked hosts in localities where fly population densities are high. These flies deposit a liquid after oviposition in a manner similar to host marking performed by fruit-infesting 192 Lalonde and Roitberg 3 ~ p = 0.0002 2

g Males Absent [ Males Present ]

ill 0 0.0 0.2 0.4 0.6 0.8 Proportion Infested Figure 3. Mean number of eggs laid per infested flower head at each sampling location, by the proportion of available heads that were infested. Open circles: in localities where male thistles are present; closed circles: in localities where male thistles are absent. Bars represent 1 SE. Number of eggs per infested flower head is significantly greater in sites where male thistles are also present (Mann-Whitney U test, p = 0.0002), whereas there is no significant relationship between infestation and proportion infested (Spearman's rho, p = 0.1822). tephritids (Angerman, 1986). Flies can recognize and will avoid using hosts that have been previously attacked by a conspecific (Lalonde and Roitberg, 1992b). Search time costs increase if many encountered hosts are rejected due to prior infestations. Parasites may compensate for such costs by either increasing clutch size when unexploited hosts are located (Charnov and Skinner, 1985; Rosenheim and Rosen, 1992) or by allocating extra eggs to previously attacked hosts (Roitberg and Prokopy, 1983; Roitberg and Mangel, 1988). In either circumstance, we would expect to find a positive correlation between eggs laid per host and the proportion of hosts in the population that is attacked. No such correlation exists (Spearman's rho, p = 0.1822). In a similar way, flies in localities where males are present may spend a larger proportion of their available time searching and may encounter fewer suitable female flower heads on average. More time-limited flies will tend to allocate more eggs when suitable hosts are encountered (Mangel, 1987; Mangel and Clark, 1988). While we cannot discard this interpretation of our results, we have observed that flies in the field are very quick to recognize male plants and probably pay a relatively small increased search cost in localities where males are present. A greater proportion of a fly's time in the field is spent assessing heads on female plants (our observation). Finally, it is possible that the observed pattern may be a passive expression of the generally lower quantity of seed produced in localities where pollen availability is low. An egg-limited fly such as Orellia ruficauda, which experiences diminishing returns from increasing clutch size, can be expected to lay as few eggs as time permits in each host head (Mangel, 1987; Mangel and Clark, 1988; Rosenheim and Rosen, 1991; Minkenberg et al., 1992). In fact, the strongest predictor of clutch size in O. ruficauda is the number of eggs present in the abdomen (Lalonde and Roitberg, 1992a). Presumably flies with large egg loads have relatively less time available to find hosts for each clutch of eggs and compensate by committing more eggs to each clutch (Lalonde and Roitberg, 1992a). Mass of mature larvae is significantly smaller in low-quality localities than it is in high-quality localities (Fig. 4) and small larvae produce significantly fewer eggs as adults (Lalonde and Roitberg, 1992b). Assuming that flies forage for most of their hosts close to where they emerge, one might well expect to find smaller clutches on average in low- Seed predator clutch size in a tephritid-thistle system 193 30

4J Pollination 0 F- 20 Pollination ql-- 0 10

0

I l a I I I Ii a

Larval Mass (rag) Figure 4. Frequency distribution of larval masses in high- and low-quality localities. Masses are significantly greater in localities where male thistles are available (ANOVA, p < 0.01). quality localities, simply because of egg load limitation. While we do not have sufficient data to eliminate this alternative explanation for our field data, we feel that it is less likely. Large individuals, while rarer in low-quality localities, do comprise a significant fraction of the local population (nearly 30% are larger than the modal mass). If flies were not using the local presence', of male thistles as a factor in host assessment, we might reasonably expect to find some larger clutches in our low-quality localities. However out of 74 heads infested in low-quality localities, we found only a single three-egg clutch; all others were of one or two eggs. In contrast, 58 of the 403 heads infested in high-quality localities contained three eggs or more. This difference in the distribution of eggs among heads in the two locality types is significant (X2 = 14.97, p = 0.0105). In conclusion, we predicted that the availability of male thistles in a locality may provide information to female flies as to the general quality of their hosts (female thistle flower heads). As predicted, per head infestation was significantly greater in localities where male thistles were available, suggesting that adult clutch size decisions may be influenced by this factor. What we feel to be the less likely explanation, that the small-sized flies resulting from low-quality hosts may passively produce the observed host-exploitation pattern without any use of information such as pollen availability, cannot be rejected completely. Direct observation of adult host selection behaviour in both high- and low-quality localities is required before this question can be finally settled.

Acknowledgements

The authors would like to acknowledge the assistance of Baldev Sehra, Brent Zaharia, Robert Lunde and Monica Mather in the field. We thank the Reifel Bird Refuge for allowing us to conduct our research on their land and John Hatfield for acting as our liaison with that organization. We also thank Larry Dill, Judy Myers, Rolf Mathewes, Ron Ydenberg, Graham Pyke and Michael Zimmerman for commenting on this material in an earlier form. Ralf Cartar, Marc Mangel and Peter Nonacs provided helpful comments on the present effort. Finally, we 194 Lalonde and Roitberg thank the Natural Sciences and Engineering Research Council of Canada for an operating grant awarded to B. D. Roitberg and a postgraduate scholarship awarded to R. G. Lalonde.

References

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