ISSN 0013–8738, Entomological Review, 2011, Vol. 91, No. 3, pp. 292–300. © Pleiades Publishing, Inc., 2011. Original Russian Text © S.Ya. Reznik, 2011, published in Entomologicheskoe Obozrenie, 2011, Vol. 90, No. 1, pp. 17–27.
Host Plant Population Density and Distribution Pattern as Factors Limiting Geographic Distribution of the Ragweed Leaf Beetle Zygogramma suturalis F. (Coleoptera, Chrysomelidae) S. Ya. Reznik Zoological Institute, Russian Academy of Sciences, St. Petersburg, 199034 Russia Received January 19, 2009
Abstract—Field sampling conducted in 2005–2007 in Voronezh and Rostov provinces and in Stavropol and Krasnodar territories (south-west of European Russia) suggested that the climatic effect on geographic distribution of the ragweed leaf beetle, Zygogramma suturalis is mediated by the abundance of its host plant, Ambrosia artemisiifolia. At the periphery of the common ragweed invasion area Z. suturalis was absent or its population density was below the detection threshold. A pivotal role was played by the sufficient percentage of small but relatively stable plots with high ragweed population density, rather than by the mean rate of the ragweed infestation. Inside the geographic range of the ragweed leaf beetle all relatively stable habitats were infested by A. artemisiifolia and in more than half of plots inspected, common ragweed percent cover was higher than 5%. In regions where such infestation was recorded on less than 20% of the plots studied, Z. suturalis was absent, most likely due to its low ability for long-range search for a host plant. DOI: 10.1134/S001387381103002X
INTRODUCTION The geographic ranges of insects can be limited by a large variety of different causes. Climatic factors can influence the geographical distribution of insects both directly and indirectly via the changes in the biotic environmental parameters, of which the most important is the presence of suitable food. The limits of the geographic ranges of phytophagous insects, particularly those with strict host specificity, often coincide with the limits of the geographical distribution of their host plants. For some species of insects, not only the presence of certain plant species, but also sufficiently high population density can be important. Such cases were rather often reported by insect taxonomists and faunists (Emeljanov, 1970; Korotyaev, 2000), but rarely became objects of special studies (Emeljanov, 1967). The issue of the factors determining the limits of geographic ranges is particularly important in connection with biological invasions, one of the most actual problems in modern fundamental and applied ecology (Elton, 1960; Alimov et al., 2004; Fitzpatrick and Weltzin, 2005; Guisan and Thuiller, 2005). As well as the borders of the natural distribution ranges, the potential limits of the extra-range dispersal depend on
various environmental parameters, but for invasive phytophagous insects, suitable food is often a limiting factor. For example, more and more American pests of potatoes, among which the Colorado potato beetle Leptinotarsa decemlineata Say is the most known and well studied species, invade Eurasia in the wake of their host plant (Ivanchik and Izhevski, 1981; Fasulati, 2007; Izhevski, 2008). Extra-range dispersal of the ragweed leaf beetle Zygogramma suturalis F., which was introduced by O.V. Kovalev with the aim to control common ragweed Ambrosia artemisiifolia L., the most noxious invasive weed in Russia, was also thoroughly studied (Kovalev et al., 1983; Kovalev, 1989а; Reznik, 2004, 2009). In particular, investigations on these rather closely related leaf beetles have revealed an interesting difference. Although the geographic ranges of both species do not reach the northern boundaries of distributions of their host plants, the invasion zone of the Colorado potato beetle is directly limited by climate (Fasulati, 2007), while the ragweed leaf beetle was recorded only in regions with a sufficiently high average rate of infestation by common ragweed (Reznik, 2009). The earlier studies conducted in the environs of Stavropol, near the first Z. suturalis introduction site, have
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showed that its population density is strongly dependent on the population density of ragweed (Reznik, 1985; Reznik et al., 1990). The present work was devoted to the analysis of new data that had been collected from a much wider area. MATERIALS AND METHODS This study was based on the results of quantitative sampling conducted in 2005–2007 in 20 regions infested with common ragweed in Voronezh and Rostov provinces and in Stavropol and Krasnodar territories of Russia. All the records were made in the second half of July or in August, i.e. immediately after the mass emergence of adults of the first generation of the ragweed leaf beetle. With the aim of conducting such a wide-scale study during a relatively short period of time, a new method was elaborated, because the method of sampling plots used earlier (Reznik, 1985) was too time consuming, while the five-grade scale elaborated later (Reznik et al., 1990) was too crude. The sampling methods that were used in the present study have been described in a number of earlier publications (Reznik and Spasskaya, 2006; Reznik, 2009). A site with more or less uniform vegetation separated from other sites by some borders (road, field boundary, etc.) was considered as a sampling unit. The site size varied from hundreds of square meters (separated patches of ragweed) to tens of hectares (agricultural fields). For each site, its approximated size, the average height and percent cover of ragweed were estimated. For the data treatment, all the inspected sites were divided into 2 groups: “unstable” (arable fields) and “relatively stable” (field margins, roadsides, wastelands, old fields, etc.). In relatively stable habitats the ragweed leaf beetle population density is known to be higher than that in crop rotations (Reznik et al., 1990). Moreover, the probability of a successful biological control of a weed increases with the rate of the habitat stability (Hall and Ehler, 1979; Harris, 1991). The ragweed leaf beetle population density was estimated by two methods: by sweeping (the mean number of beetles per 10 sweeps) and by visual counting (the number of beetles per sampled square unit). The number of sweeps and the size of a visually inspected sample area depended on the size of a site. The samples were taken along the country roads, all the plots adjoining the road being inspected with particular attention being paid to local patches of ragweed. In ENTOMOLOGICAL REVIEW Vol. 91 No. 3 2011
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each region, from 15 to 25 sites were inspected with a total of 371 sites. As expected, the estimations of the ragweed leaf beetle population density made by sweeping and by visual counting were closely correlated (Pearson correlation coefficient r = 0.77, n = 149, p < 0.001, only sites where at least one beetle was found were included in the analysis). The linear regression equation was Zv = 0.128 Zs, where Zv is the mean number of beetles per 1 m2 obtained by visual counting and Zs is the mean number of beetles per 10 sweeps at the same plot. For further statistical treatment, the averaged index Z = (Zv + 0.128 Zs) / 2 was used. If the leaf beetle population density at a plot was estimated only by visual counting, Z was taken to be equal to Zv, if only sweeping was used, Z was taken to be equal to 0.128 Zs. Preliminary statistical treatment (two-factor regression analysis of the ranked data) showed that the ragweed leaf beetle population density was significantly dependent both on the percent cover of common ragweed (p = 0.002) and on its height (p < 0.001). The preference of ovipositing females for higher plants of the same phytomass has been demonstrated earlier (Reznik, 1985). In addition, the ragweed height is an indirect indicator of a very important factor, the habitat stability: in July–August, when the records were made, the low ragweed plants usually testified to recent moving. That is why for further analysis, the index of “ragweed abundance” (the mean height of common ragweed multiplied by its mean percent cover on the plot) was used. Naturally, the ragweed leaf beetle population density was also significantly dependent on the ragweed abundance (p < 0.001), the correlation coefficient (r = 0.58) being practically the same as that for the two-factor regression equation (r = 0.60). Most of the parameters characterizing populations of common ragweed and of ragweed leaf beetle were not normally distributed. Hence, the data were described by medians and quartiles, paired comparisons were made with the Kruskall–Wallis test or with the Tukey test applied to the ranked data. As the size variation among plots was very high, in certain cases the weighted mean was used, data were weighted by the plot size. Other statistical methods are described below. RESULTS AND DISCUSSION First, one should note that the regions where the ragweed leaf beetle was not found during the special
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Fig. 1. Map of the studied regions of the European part of Russian Federation: 1, the regions where the ragweed leaf beetle was found; 2, the regions where only ragweed was found.
quantitative sampling are located at the periphery of the common ragweed invasion area (Fig. 1). The factors determining the current geographical distribution of A. artemisiifolia were thoroughly discussed in the preceding paper (Reznik, 2009). The data available suggest that in the European part of the Russian Federation the northern border of the invasion area of this noxious weed is determined by the average September temperature of no less than 15°C and the northeastern border is determined by the total precipitations of the warm period (April–October) of no less than 200–250 mm. As for Z. suturalis, its absence in the most northern populations of common ragweed (the north of Rostov Province and the south of Voronezh Province) cannot be explained by the limiting effect of climate. The sum of effective temperatures required for the development of one generation of the ragweed leaf beetle constituted, according to our data (Kovalev et al., 1983), 425 degree-days with a threshold of 11.5°C. These thermal parameters of development are close to those of the Colorado potato beetle (300–400 degree-days with a threshold of 10–12°C) whose current geographic range extends up to Northwest Russia (Ushatinskaya and Kochetova, 1981; Minder, 1981; Fasulati, 2007). It should be assumed that the influence of climate on the geographical distribution of Z. suturalis is me-
diated by the food plant abundance, i.e., the “boundary” regions where the phytophage is absent (or its population density is extremely low) are characterized by the relatively low population density of common ragweed. Indeed, the data (Fig. 2) suggested that in the inspected regions where the ragweed leaf beetle was found, both medians and weighted means of the ragweed abundance were higher, although the difference between the medians was much more significant (p < 0.001, the Kruskall–Wallis test) than that between the means (p = 0.03). This distinction in statistical significance and in magnitude of difference between two types of regions estimated with the two parameters of the ragweed abundance deserves special attention. When the median is calculated, the common ragweed population densities at all plots of a given region are equally important, while the weighted mean mostly depends on the common ragweed population densities at the largest plots. Thus, the weighted mean gives an estimate of the average ragweed abundance in a whole region, while the median indicates the proportion of plots (independently of the size) with the high ragweed population density. These two parameters are naturally correlated (Spearmen rank correlation coefficient r = 0.68, n = 20, p < 0.01) but it is clear that it is the proportion of plots with the high host plant population density which determines the geographical distribution of the ragweed leaf beetle (Fig. 2). ENTOMOLOGICAL REVIEW Vol. 91 No. 3 2011
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Fig. 2. Indicators of the ragweed abundance in the plots of the inspected regions. Abscissa, the weighted means (data were weighted by the plot square); ordinate, medians; 1, the regions where the ragweed leaf beetle was found; 2, the regions where only ragweed was found.
Fig. 3. Medians of the ragweed abundance in the plots of the inspected regions. Abscissa, grades of the ragweed abundance; ordinate, the percentage of plots in a given grade; (a) crop rotation fields, (b) relatively stable plots; 1, the regions where the ragweed leaf beetle was found; 2, the regions where only ragweed was found. Sample sizes (the number of inspected plots): 1а, 69; 2а, 45; 1b, 181; 2b, 76.
The same is suggested when comparing the distribution of the ragweed abundance at plots of the regions where the ragweed leaf beetle was found and where it was not found. The difference between the inspected agricultural fields (Fig. 3a) was not significant (p = 0.15), although in the regions where Z. suturalis was not found, the proportion of ragweed-free fields is somewhat higher and fields heavily infested with ragweed were not recorded. The difference between the relatively stable plots (field margins, roadsides, etc.), on the contrary, was highly significant (p < 0.001). From Fig. 3b it is clear that in the regions where the ragweed leaf beetle was found, all the relatively stable biocenoses were infested with ragweed and more than in half of these plots the index of the ragweed abundance was higher than 10 (with the average ragweed ENTOMOLOGICAL REVIEW Vol. 91 No. 3 2011
height of 1.0–1.5 m this corresponded to the percent cover of 6–10%). It is the presence of practically uninterrupted “bands” or “nets” consisting of small but relatively stable plots with a high host plant population density that seems to determine the geographical range of the phytophage. However, the ragweed leaf beetle was also found in almost half of the agricultural fields subjected to crop rotation, although its population density was much lower there (Fig. 4). As for the relatively stable biotopes, Z. suturalis was found in 80% of the inspected plots of this type and in 5% of these plots its population density was higher than 1 adult / m2. This difference in the distribution of the ragweed leaf beetle population density between the two types of plots was
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Fig. 4. The ragweed leaf beetle population densities in crop rotation fields and in relatively stable plots. Abscissa, grades of the ragweed leaf beetle population density (beetles / m2); ordinate, the percentage of plots in a given grade. 1, crop rotation fields (n = 69); 2, relatively stable plots (n = 181). Only the data for the regions where the ragweed leaf beetle was found are given.
Fig. 5. Dependence of the ragweed leaf beetle population density on the ragweed population density. Abscissa, grades of the ragweed abundance; ordinates: 1, the ragweed leaf beetle population density in plots of a given grade (the left axis, beetles / m2, medians and quartiles), values indicated by different Latin letters are significantly different (p < 0.05, the Tukey test, pairwise comparing of the ranked data); 2, the percentage of plots where at least one beetle was found (the right axis, %). Only the data for the regions where the ragweed leaf beetle was found are given.
most probably determined by the corresponding difference in the distribution of ragweed population density (comp. Figs. 3a and 3b). The ragweed leaf beetle population density was earlier shown to be correlated with the ragweed population density independently of the degree of plot stability (Reznik, 2009). Fig. 5 shows the data on the ragweed leaf beetle population density in plots with different levels of infestation by ragweed. It can be seen that Z. suturalis was found in more than half of the plots where the index of ragweed abundance was not higher than 1 (with the average ragweed height of 1 m this corresponded to the plant cover less than 1%), but the beetle population density was very low there. In the plots where the ragweed abundance was from 1 to 10, the leaf beetle was found more often and its population density was higher. Finally, Z. suturalis was
found in 80% of the plots where the ragweed abundance exceeded 10, and the median beetle population density was about 0.1 adults / m2, but further increase in the ragweed abundance did not cause any significant increase in the ragweed leaf beetle population density. As noted above, the border between regions where the ragweed leaf beetle was found and where it was not found also corresponded to the ragweed abundance from 1 to 10 (Fig. 2). In the regions where Z. suturalis was not found, in more than 20% of plots, the ragweed abundance exceeded 10 (Fig. 3), but this relatively low proportion of the highly infested plots was obviously not sufficient to support stable populations of the ragweed leaf beetle. On the other hand, in the regions where Z. suturalis was recorded, sporadic adults were found in more than half of the plots with very low ENTOMOLOGICAL REVIEW Vol. 91 No. 3 2011
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ragweed abundance (Fig. 5). Most probably, these individuals migrated from the neighboring plots which were much more heavily infested by ragweed. Thus, the different methods of data analysis have supported the hypotheses that the ragweed abundance equal to 10 (plant cover of 6–10% with the average plant height of 1.0–1.5 m) is limiting the habitat ability to support stable population of the ragweed leaf beetle and that the presence of a sufficient number of such habitats determines the geographical range of Z. suturalis. The probability of the long-term stability of a phytophage population is known to increase with the size and density of its host plant population (Emeljanov, 1967; Korotyaev, 2000; Haynes et al., 2006; Rabasa et al., 2008), that is why host specific insect phytophages relatively more often feed on dominant plants (Emeljanov, 1967; Marques et al., 2000). Special investigations have proved that it is the presence of sufficient food resources that determines the geographical ranges of certain host-specific phytophagous insects from different orders (Emeljanov, 1967, 1970; Koizumi et al., 1999; Ferrer et al., 2007). However, in the above mentioned Colorado potato beetle (as well as in many other oligophagous and monophagous insects) the northern limits of geographical distribution are directly determined by climate, rather than by the climate-dependent host plant population density (Ivanchik and Izhevskij, 1981; Ushatinskaya and Kochetova, 1981; Minder, 1981; Bird and Hodkinson, 2005; Fasulati, 2007).
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field is sufficient to significantly decrease early summer damage (Hsiao, 1976; May and Ahmad, 1983; Hare, 1990; Voss and Ferro, 1990; Follet et al., 1996). The ragweed leaf beetle disperses mostly by crawling (Reznik and Kovalev, 1989), therefore even the necessity to move several tens of meters searching for food can cause a sharp decrease in the phytophage population density. The earlier studies (Reznik et al., 1990; Reznik, 1996; Reznik, 2004) suggested that it was low dispersal and food search ability that was limiting the mean population densities of the ragweed leaf beetle and its efficacy for biological control of common ragweed. The present research suggests that the same factor is also limiting the geographic range of this beneficial phytophage.
Dependence of the phytophage population density on population density of its host plant has been demonstrated for many insect species (Stanton, 1983; Honěk,1991; Cowley et al., 2001; Rhainds and English-Loeb, 2003; Rabasa et al., 2008). Ovipositing females of phytophagous insects often prefer sites with a high density of their host plant population and this behavioral peculiarity can be an important prerequisite for successful biological control of invasive weeds (Myers et al., 1981; Murdoch et al., 1985; Murdoch, 1992; Hoffmann and Moran, 1992). However, the pattern of a phytophagous insect reaction to the host plant population density is, in its turn, largely dependent on the specificity of the search activity of an insect (Stanton, 1983; Bach, 1988a, 1988b; Murdoch, 1992).
O.V. Kovalev (Kovalev, 1989a, 1989b; Kovalev and Polovinkina, 2001) suggested that the ultra-high population densities that have been recorded in the moving “population wave” induced in Z. suturalis some irreversible inheritable changes and, in particular, all the individuals have acquired the ability to fly which was initially absent. However, this hypothesis seems unlikely since, as seen from the literature, neither incidence nor range of flights in adults of the “flying form of the ragweed leaf beetle” has ever been estimated quantitatively. In some publications (e.g., Kovalev, 1989b), it was stated that “in 1984 already thousands of insects simultaneously took the air,” but the exact numbers were not given. Nevertheless, two important conclusions can be made from these data. First, given that there were millions of beetles in one field, the presence of the thousands of flying individuals agree well with the results obtained in 1982 when at the moment of recording up to 5% of adults flew or attempted to fly (Reznik and Kovalev, 1989). Second, this “mass flight” had been observed by O.V. Kovalev already in 1984, i.e. one year before the first “moving population waves” emerged and were investigated (Kovalev and Vechernin, 1986; Kovalev, 1989а, 1989b). It cannot be ruled out that the phenomenon of “flying beetles” is really connected with the ultra-high population densities, but the mechanism of this correlation can be quite different: if the real flight occurred very rarely and in only few individuals, the probability of its recording becomes relatively high only when many thousands of individuals fall within the observer’s view.
It is known that the Colorado potato beetle can easily fly from one field to another but still the distance of 400–500 m between overwintering site and potato
Laboratory experiments have demonstrated that the movement activity of ovipositing females of the ragweed leaf beetle increased with the rate of the ragweed
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damage (Reznik, 1989; Reznik, 1991). Thus, it is conceivable that the flight can be directly or indirectly (via the increase in the rate of the ragweed damage) induced by a high population density. It is also possible that migration activity in American and Palaearctic populations of Z. suturalis is significantly different as has been earlier demonstrated e.g. for the Colorado potato beetle (Ivanchik and Izhevski, 1981). However, these hypotheses can be verified only by special studies including the exact estimation of the ragweed leaf beetle capability to fly for a long distance.
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CONCLUSIONS (1) The influence of climate on the geographical distribution of the ragweed leaf beetle is mediated by the food plant (common ragweed) abundance, the crucial role being played by the presence of small but relatively stable plots with a high host plant population density rather than by the average infestation rate of a region. (2) Within the geographical range of the ragweed leaf beetle all relatively stable biocenoses were infested with ragweed and in more than half of inspected plots the ragweed cover exceeded 5%. (3) At the periphery of the common ragweed invasion area, where the ragweed cover exceeded 5% in less than 20% of inspected plots, the ragweed leaf beetle was not found, which could be most probably explained by its relatively low ability to actively search for the host plant.
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ACKNOWLEDGMENTS I am deeply grateful to I.A. Spasskaya (Zoological Institute, Russian Academy of Sciences, St. Petersburg), V.M. Kalinkin (Slavyansk Experimental Plant Protection Station, All-Russian Institute of Plant Protection, Slavyansk-on-Kuban), E.S. Kotenev (Voronezh State University), E.V. Ilyina (Dagestan State University, Makhachkala), and many other colleagues who have helped to organize and to conduct the field studies in 2005–2007. This work was partly funded by the grant “Scientific bases of the conservation of biodiversity in Russia,” from the Presidium of the Russian Academy of Sciences.
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