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. The population dynamics of the gall 2 3 wasp Andricus quercuscalicis ROSEMARY S. HAILS Imperial College at Silwood Park, Ascot, Berkshire, UK Abstract The gall wasp Andricus quercuscalicis invaded Britain from the continent in the early 1960s. The life cycle involves both alternation of generations and alternation of host plants. This study draws on 8 years of population data and considers the factors that limit and regulate the distribution and abundance of A. quercuscalicis. This gall wasp, now abundant, appears to be resource-limited in the agamic generation due to competition for acorns in the ‘low years’ of the acorn cycle. Factors influencing the survivorship of the sexual generation are considered in detail. Although the sexual generation does not appear to be resource-limited, there is evidence of density-dependent mortality during gall establishment. This arises partly as a consequence of the oviposition pattern of the agamic females, because the distribution of eggs is highly aggregated between and within trees. As a result of density-dependent mortality, the distribution of mature galls is less highly clumped. Although the agamic knopper gall suffers only low rates of parasitism from a few species, several native parasitoids attack the sexual gall. The total percentage of parasitism is remarkably consistent from year to year even though the contribution from any one species fluctuates considerably. Introduction 1. The population dynamics of invasion Many species of plants, insects, and other taxa have successfully invaded Britain, for example, garden escapes, some agricultural pests, and bio logical control agents imported to control those pests. Some of these invasions have been natural and some intentionally assisted by man. Data on the success and failure of establishment of biocontrol agents Plant Galls (ed. Michèle A. J. Williams), Systematics Association Special Volume No. 49, pp. 391-403. Clarendon Press, Oxford, 1994. © The Systematics Association, 1994. 392 Rosemary S. Hails suggest that there is a large number of failures (Crawley 1989). Unfor tunately, the very nature of the process means that we have few data on the failure of natural invasions. However, the cynipid gall wasp Andricus quercuscalicis (Burgsdorf 1783) provides a particularly fine example of a successful invader, which has been allowed to reach high population densities due to its lack of economic importance. This species not only allows the process of invasion to be studied, but also the potential impact upon a close-knit native cynipid community (Schönrogge et al. Chapter 22, this volume). There has been an increasing awareness of the importance of spatial processes in the dynamics of populations (for example, Taylor 1988; Walde and Murdoch 1988). This is likely to be particularly true for populations which display patchy, aggregated distributions. Cynipid gall distributions are known to vary considerably in their occurrence from tree to tree, trees being characteristic in favouring particular gall species (Askew 1962; Hails and Crawley 1991). Trees are, therefore, acting as natural and distinctive patches for cynipids. Trees may also be broken down into finer natural units (for example, buds or shoots). Such a naturally patchy environment may well be important in structuring the dynamics of gall-forming species. This chapter presents the dynamics of a successful invader and examines the spatial processes that limit and regulate its distribution and abundance. 2. Invasion of A. quercuscalicis into Britain Andricus quercuscalicis was first recorded in Britain by Claridge (1962), although anecdotal records date back 10 years earlier than this (the late Ted Ellis, personal communication). One reason for its recent arrival in this country is that it is an obligate host alternator, attacking the Turkey oak, Quercus cerris L., as well as the English oak, Q. robur L. The Turkey oak was only introduced into Britain approximately 200 years ago as an ornamental tree. It has since escaped and become established over much of southern and midland Britain. This ‘assisted’ invasion of one of the host trees paved the way for the ‘natural’ invasion of the insect. The biogeographical patterns of invasion by A. quercuscalicis across Europe and into Britain are currently being investigated by Sunnucks et al. (Chapter 21, this volume). Since its arrival in Britain, the wasp has spread to occupy those regions in which the Turkey oak, Q. cerris, is common (McGavin 1981) and it has reached high population densities. One generation attacks the acorns of the English oak, Q. robur, forming large and conspicuous galls. The proportion of acorns attacked can be very high and this caused con siderable comment in the early 1980s when the wasp came to public Population dynamics of gall wasp Andricus quercuscalicis 393 attention (Crawley 1984). Our study started after the gall wasp had already become established in its current range and had reached high densities. 3. Life cycle of A. quercuscalicis The life cycle of A. quercuscalicis is described in full by Schönrogge et al. (Chapter 22, this volume) and is summarized in Fig. 23.1. The sexual galls develop on the male buds during bud burst in April. These galls are much smaller and simpler in form than those of the agamic generation, one flask-shaped gall replacing two of the four anthers in a whorl. One catkin may carry up to 20 galls, but attack rates vary considerably both within and between trees (Hails and Crawley 1992). Each gall contains a sexual male or female. The males emerge first and battle for position over the female galls. The females are mated as soon as they break free from their galls and then disperse to Q. robur. The female flowers of Q. robur are freshly pollinated at this stage (late May) and the sexual females lay their eggs between what will become the acorn and its cup. The large knopper galls develop over the summer. There is one additional feature: a proportion of agamic females Quercus robur Quercus cerris Fig. 23.1. The life cycle of Andricus quercuscalicis. 394 Rosematy S. Hails (approximately 30 per cent in Britain) delay emergence for 1 year, remaining inside the acorn gall in the litter layer. Recent data illustrate that there is geographic variation in this delayed emergence, with up to 80 per cent emerging after the first year (Schönrogge et al. Chapter 22, this volume). The dynamics of a bivoltine, host-alternating insect This system presents a challenging problem for the quantitative ecologist. Most theoretical models of insect populations deal with univoltine systems. This species is not only bivoltine, but also host-alternating. The first approach to modelling such a population is to attempt to predict the abundance of one generation from the abundance of the previous stage. A coupled set of non-linear difference equations is presented below, encapsulating the key features of the life cycle of this insect: St+1 Sexual generation in agamies in year t agamies in year I + 1 mortality year t+ 1 A, (23.2) agamic parasitism other sexual resource migration generation in generation function mortality year t mortalities The first equation predicts the sexual generation in year t + 1 from the abundance of the agamic generations of the previous 2 years (to simplify, the small proportion of agamies that delay their emergence for 2 years or more are ignored). The proportion of agamies emerging in the first year is p, and, therefore, the proportion emerging in the second year is 1 — pe. The parameter A„ and the function f(A,) refer to the intrinsic rate of increase and to any density-dependent mortalities for the agamic generation in the specified year. The additional overwintering mortality that is incurred by those agamies which delay emergence for 1 year is denoted by d. The final term involves ma, the mortality of agamies suffered during migration as they disperse from Q. robur to (I cerris. The second equation predicts the agamic generation in year t from the abundance of the sexual generation earlier in the same year. As the sexual generation does not display delayed emergence, there is no time delay in this equation. The parameter A, and the function g(St) refer to the intrinsic rate of increase and density-dependent mortalities in the sexual generation. Parasitism appears as separate, density-independent term. There is some evidence that the agamic generation is resource- limited and so a resource function, h(Rt), has been included. This will be Population dynamics of gall wasp Andricus quercuscalicis 395 discussed in some detail later. Finally, ms is the migration mortality for the sexuals as they migrate from Q. cerris to Q. robur. Four key features of these equations will now be examined in greater detail. 1. Gall establishment in the sexual generation: a component of g(St) The first mortality to be considered involves the establishment of the small catkin galls on Q. cerris in the spring. Dissection of the male flower buds of Q. cerris early in the year allows us to census the egg population as it is laid by the agamic females. Because this monitoring is necessarily destructive, we only obtain snapshots of the population through time. Egg densities increase over a period of a few weeks, reaching a maximum shortly before bud burst. At the time of peak egg densities, the distribution of eggs across buds is highly clumped, with most eggs being found in relatively few buds. The degree of clumping was quantified by fitting a negative binomial distribution to the frequency distribution of eggs per bud in each tree. This provides us with k, a parameter of this distribution, which describes the degree of clumping for the eggs in a given tree. A relatively high k would result from a distribution that is less clumped (that is, eggs would be more evenly distributed across buds), whereas a relatively low k would describe a highly clumped distribution. In this way, changes in the shape of the distribution can be monitored through time. As bud burst occurs, the eggs hatch and the sexual galls become established. The distribution of galls can be described in the same way as the egg populations for each tree. If the rate of egg mortality had been the same in each bud, then k, the measure of aggregation (or clumpedness), would not change. In other words, random deaths would result in no change in k (Pielou 1977). However, if egg mortality were greater in buds with higher egg densities, aggregation would decrease (so that k would increase). A comparison of the egg and gall population distributions will, therefore, provide an insight into the pattern of mortalities that have occurred in the intervening period. Collection of such data requires a sufficient range of egg densities to fit a negative binomial probability density function. Figure 23.2 illustrates the results for those trees and years in which this was possible. In seven out of nine cases, k increased when comparing egg and gall populations. This evidence suggests that the rate of gall establishment is dependent upon egg density within the bud. 396 E G E G E G TREE 1 TREE 2 TREE 3 Fig. 23.2. Comparing k of the negative binomial distribution for egg (E) and gall (G) distributions in different trees and different years. In seven out of nine cases k increases between the egg and gall populations, suggesting density dependent mortality in the establishments of galls. 2. Parasitism in the sexual generation: pp The sexual generation is attacked by a number of polyphagous parasitoids, mostly in the genus Mesopolobus (Pteromalidae). The principal species are Population dynamics of gall wasp Andricus quercuscalicis 397 Mesopolobus fuscipes (Walker), M. xanthocerus (Thomson) and M. tibialis (Westwood). These parasitoids attack the cynipid in the late larval/pupal stages. It has been shown that the gall distribution is aggregated, that is, there are many low density patches and relatively few high density patches. Is parasitism rate affected by gall density? This question can be asked in many different ways. For example, the parasitoid may respond to gall density at one spatial scale but not another. Gall distributions and parasitism at the level of the catkin, bud, shoot, and twig should therefore be considered (Hails and Crawley 1992). Much parasitism is found to be spatially density-dependent, but parasitism by any given species does not exhibit a consistent relationship with density. An illustration of this is provided by M. fuscipes: in Fig. 23.3a, there is a positive relationship with density. Those galls in high density patches are more likely to be parasitized than galls in low density patches. Such patterns are obtained when parasitoids are attracted to or spend more time in high density patches. However, in a different tree but at the same spatial scale, the same species of parasitoid shows an inverse relationship between parasitism and gall density (Fig. 23.3b). Such patterns may be obtained when parasitoids arrive at a patch and lay a fixed number of eggs and become egg- limited in high density patches. The third pattern is density-independent parasitism, in which there was no relationship between parasitism and gall density. In order that patterns of spatial density-dependence can have an impact upon the population dynamics of the gall wasp, they must translate into temporal density-dependence. However, the evidence we have from 8 years of data is that this is not the case. Total percentage parasitism is remarkably constant, fluctuating only between 20 and 30 per cent—although the contribution of individual species may vary considerably (Fig. 23.4). For this reason, parasitism was included as a density-independent term in the coupled equations. 3. Migration mortalities: ma and ms Mortalities incurred during dispersal are notoriously difficult to measure and we have two such migration mortalities in these equations. Attempts have been made at mark-release-recapture studies, but in spite of large numbers of mark -releases (> 1000), no recaptures have been made. Although we cannot quantify these losses in absolute terms, it is possible to say something about their relative magnitude. Due to the ratio of Q. robur to (X cerris in the study area (approximately 10: 1), it is likely that ma> ms. 398 Rosemary S. Hails LOG (GALL DENSITY) LOG (GALL DENSITY) Fig. 23.3. The relationship between the proportion of galls parasitized by M. juscipes and gall density in two trees within the same year. The analysis was conducted in logits and back transformed to produce the curved line. (a). Ln(p/q) = 3.993 + 0.73451n (gall density) and (b) Ln(p/q) = - 1.388 - 0.3991n(gall density), where p is the proportion parasitized and q=l~p. The first graph is an example of positive density dependence, whilst the second is an example of inverse density dependence. After Hails and Crawley (1992). 4. The resource junction: h(Rt) The resource function involves the agamic generation. Agamic gall density and acorn density have been recorded on 30 trees at Silwood Population dynamics of gall wasp Andricus quercuscalicis 399 50 YEAR Fig. 23.4. Percentage parasitism of the sexual generation of A. quercuscalicis over an 8- year period. Four species of polyphagous parasitoids attack the sexual gall: M. juscipes M. xanthocerus r, M. tibiali M. dubius ( . After Flails and Crawley (1992). Park for more than a decade (Fig. 23.5). Acorn crops on Q. robur exhibit an approximately alternating yield (possibly a defence against seed predators). Gall densities appear to track these acorn fluctuations very closely. In acorn-poor years, the suggestion is that they are resource- limited. If gall density is correlated with acorn density, there is a strong linear relationship (Fig. 23.6). This provides strong circumstantial evidence for resource-limitation in acorn-poor years. However, it would be unwise to extrapolate this linear relationship to very high acorn densities, as there may well be a predator satiation effect in acorn-rich years; there is a distinct suggestion that there is a curvilinear relationship in Fig. 23.6. This hypothesis is supported by the fact that there is a negative relationship between percentage galling and acorn density (r = - 0.635, p < 0.05). Individual trees differ greatly in their susceptibility to gall wasp attack, and these differences are consistent from year to year (Hails and Crawley 1991). Indeed, one tree produced a consistently high acorn crop, but was never galled. These differences were not correlated with other measurable factors, such as acorn density or location of nearest Turkey oak and we suspect that these differences in susceptibility result from genetic differences between the trees. This hypothesis has yet to be tested. 400 Rosemary S. Hails YEAR Fig. 23.5. Fluctuations in acorn crop and gall density over a 12-year period. The solid line represents total resource density (that is acorns plus those acorns which were attacked) whilst the dotted line represents galls. Both acorns and galls were measured per shoot and the mean calculated over the same 30 trees each year at Silwood Park. After Hails and Crawley (1992). Linking models with data: temporal trends in A. quercuscalicis 1. Generation to generation density trends When attempting to model the dynamics of a bivoltine insect, there are a number of options. Two questions need to be answered: the first concerns the closeness with which the two generations are coupled and the second concerns the regulatory and/or limiting factors that are important in determining the dynamics of the two generations. The two generations may be quite closely coupled, in which case a knowledge of one will provide predictive power about the other. Alternatively, the two generations may be only loosely coupled, in which case it may be more practical to describe the dynamics of one generation without reference to the other. For our data from Silwood Park, the number of agamies in the autumn is not correlated with the number of sexuals earlier that year, nor is the number of sexuals related to agamic density the pre vious year, (Fig. 23.7). The two difference equations presented earlier appear to be very loosely coupled, so that a knowledge one genera-