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Observations on the thistle-feeding tortoise , rubiginosa (Coleoptera: Chrysomelidae)

Michael G. Cripps AgResearch, Lincoln Email: [email protected]

Abstract The thistle-feeding tortoise beetle, Cassida rubiginosa Müller (Coleoptera: Chrysomelidae) was released in 2007 in New Zealand as a biological control agent against the weed Californian thistle (Cirsium arvense). The beetle’s development and its defoliation of Californian thistle were monitored at Lincoln over the spring/summer of 2012/2013. One complete generation of the beetle was observed from 4 October 2012 to 8 February 2013. Over this period, feeding by the beetle occasionally resulted in shoot death, and on average resulted in 62.7% defoliation by the end of the beetle’s development. These observations are indicative of a successful biocontrol agent, but controlled experiments are needed to evaluate the effectiveness of this agent over multiple years and under realistic conditions.

Introduction The tortoise beetle, Cassida rubiginosa Müller (Coleoptera: Chrysomelidae) (hereafter Cassida) is a herbivorous beetle of Eurasian origin that was released in 2007 in New Zealand (NZ) as a biocontrol agent against Californian thistle (Cirsium arvense). The beetle has been well studied in its native range, particularly in Europe and Japan, and also in North America (NA) were it was inadvertently introduced sometime prior to 1901 (Majka & Lesage 2008). Much of the interest in Cassida has focused on its potential as a biocontrol agent, since it is a conspicuous feeder on thistles, including some of the worst agricultural weeds. The primary host plant of Cassida is Californian thistle, although it is an oligophagous

6 Michael Cripps feeder with many host plants in the thistle tribe Cardueae, including most species in the subtribe Carduinae (Zwölfer & Eichhorn 1966). Studies from the native range (Bacher & Schwab 2000; Cripps et al. 2010) and NA (Ang et al. 1995) indicated a potential for Cassida to have an impact on Californian thistle, although under natural field conditions its effectiveness is often limited by high rates of predation and parasitism (Ward & Pienkowski 1978b; Schenk & Bacher 2002). The demonstrated potential impact was part of the rationale for releasing Cassida in NZ. In addition there was good reason to predict the effectiveness of this agent would be greater in NZ since the absence of native Cardueae and the absence of close native relatives to Cassida should offer some relief from parasitism. Cassida is now well-established in many parts of NZ where anecdotal reports of impressive levels of damage to Californian thistle suggest that the beetle has started to have an impact in some areas (M. Deverson, personal communication). While these anecdotal reports are encouraging, more rigorous assessment is needed on how this beetle is responding to its novel environment in NZ, and the impact it is having on Californian thistle and other thistles. Obtaining a better understanding of the biology, ecology, and behaviour of the beetle in NZ will enable more effective utilisation of this species for biological control of thistle weeds. This paper presents some initial observations on the beetle in NZ, highlights the impact of this biocontrol agent, and suggests future research needs.

Methods At Lincoln, on the grounds of Landcare Research there is a small population of Cassida that has been there since 2007 (H. Gourlay, personal communication). The population of is present adjacent to a native vegetation patch in an unmown buffer strip (ca. 6m x 30m) predominantly composed of cocksfoot (Dactylis glomerata L.) and Yorkshire fog (Holcus lanatus L.). Californian thistle is also common in this strip, along with a lesser number of Scotch thistle (Cirsium vulgare (Savi) Ten.). Previously, during the summer of 2011/2012, substantial feeding damage to Californian

The Weta 45:5-13 7 thistle was observed in this area by Dr Simon Fowler (Landcare Research) who suggested this site would be useful for monitoring this biocontrol agent.

The progress of the beetle’s development and its associated damage on Californian thistle was monitored over the spring/summer of 2012/2013. In this buffer strip, 15 individual Californian thistle shoots were labelled with numbered aluminium tags tied near the base of the shoot on 4 October 2012. Seven assessments of these shoots were made starting on 4 October 2012, and subsequently on 18 October, 1 November, 21 November, 20 December 2012, 16 January, and 8 February 2013. At each assessment date, the growth stage, shoot height, and percent defoliation was recorded for each of the labelled shoots. On the first assessment date, nine shoots had initial signs of Cassida feeding damage, and 6 shoots had no signs of damage. Percent defoliation was assessed separately for the lower and upper halves of each shoot. The assessments were made visually and assigned a score of 0, 1, 5, 10, 25, 50, 75, or 100 percent defoliation. The number of each growth stage (adults, egg masses, and larvae) of Cassida on each shoot was also recorded. By the end of the monitoring period only 12 of the 15 shoots remained. One near the strip edge was mown by the second assessment date. Another two shoots were not found again after the 21 November assessment.

Results and Discussion The progression of Cassida life stages, the abundance of individuals per shoot, and corresponding defoliation of Californian thistle are depicted in Figures 1 and 2. On the initial assessment (4 October) the average defoliation was 4.3% for the lower leaves and <1.0% for the upper leaves. Given these low levels of feeding damage it is likely that the adult beetles had emerged recently. Feeding damage by the adult beetles increased steadily, primarily on the lower leaves of shoots, where defoliation reached approximately 20% prior to the emergence of larvae. The first larvae were found on 29 October in

8 Michael Cripps the vicinity of the study area, although not on the shoots being monitored. Larvae on the monitored shoots were first recorded on 21 November. At this point no adults were observed, conforming with the known biology of this beetle in its native range where most adults die after the spring egg-laying period. However, it would not be surprising to find low numbers of adults throughout the spring and summer since mark-recapture studies in the native range show a small proportion of adults in the population survive for 2 or 3 years (Koji & Nakamura 2006). Following the emergence of larvae there was a sharp increase in the percent defoliation reaching an average of 62.7% defoliation on the lower leaves by the fifth assessment on 20 December. The lag in the defoliation of upper leaves appears to be a result of shoot growth initially exceeding consumption by the beetle. By midsummer the thistle shoots ceased to elongate, the beetle larvae continued to move up the shoots in search of new food, and eventually consumed the upper leaves. By 16 January the damage on the lower and upper leaves was equivalent, and by the end of the feeding period on 8 February the mean combined total of lower and upper leaf defoliation was 62.7%.

The first new generation adults were observed on 20 December, along with several pupal exuviae found on the leaves, indicating emergence was very recent. The peak of the new generation adults was on 16 January, when 18 new generation adults were recorded (mean = 1.5 beetles/shoot, Figure 1). It is likely that many of the new generation adults moved to other nearby thistle plants, or quickly entered into an aestivo-hibernal dormancy, as reported in the native range (Koji & Nakamura 2006). In their native range the beetles are reported to overwinter as adults in nearby forest edges under the leaf litter (Kosior 1975). Greater establishment has been noted at release sites in NZ that are nearby hedge-rows, suggesting that protected overwintering areas are important for the survival of the beetle (M. Deverson, personal communication).

The observations reported here show that Cassida can cause severe defoliation of Californian thistle, and even shoot death. However,

The Weta 45:5-13 9 the impact of this defoliation on the population dynamics of Californian thistle over multiple years under realistic farm management scenarios is unknown in NZ and elsewhere. Furthermore, while there is limited information documenting impacts of Cassida on Californian thistle, even less is known about the potential impact on other thistle weed species (Kok 2001).

Sustaining high population numbers will be important for Cassida to be an effective biocontrol agent. The drop in mean larvae per shoot from 10 to 6.8 over the month-long period from 21 November to 20 December (Figure 1) is most easily explained by shoot death. Some larvae probably died due to complete consumption of their food resource. For example, on 21 November, 33 larvae were recorded on one shoot, and by the next assessment date on 20 December the same shoot was dead, with only one live found on it. Similarly, the two shoots that were not found after the 21 November assessment had 14 and 18 larvae at that time, and they too may have died due to heavy defoliation by the larvae. Overall, the shoots that survived (and could be found) over this month-long period maintained fairly constant numbers of larvae. This would suggest that the larval stages are experiencing some enemy-free space in NZ, in contrast to the native range where 53.4% mortality was recorded one week after a field release of 1200 first to second instar Cassida larvae (Cripps et al. 2010).

Larvae are confined to the shoots on which they hatch, or to adjacent overlapping shoots, but cannot move across the ground to new shoots (Tipping 1993; M. Cripps, personal observation). This creates a scenario where there is potential for intraspecific competition, and exhaustion of the food resource. Not all of the shoots in the study area were monitored in detail, but it was obvious that many shoots in the area escaped with only very minor feeding damage, and flowered and produced seed. Some larval feeding was also noted on Scotch thistle (Figure 2), although to a much lesser degree than on Californian thistle. Clearly much is dependent on the

10 Michael Cripps oviposition choices of adult females, and the relative importance of the selection pressures driving these choices (e.g. intraspecfic competition, enemy-free space, host plant nutritional quality). Understanding how and why adult females choose a particular host plant for oviposition might offer insights into the effectiveness of this biocontrol agent under different thistle weed conditions (e.g. density, spatial arrangement, and species composition).

Even if Cassida experiences relaxed predation and parasitism in NZ, environmental conditions could play a more important role in the demographics of this beetle. Under ideal conditions in the laboratory, the beetle was reported to produce an average of 815 eggs per female (Ward & Pienkowski 1978a). However, under natural field conditions the beetle typically realises only about 10% of its potential fecundity (Koji et al. 2012). It is assumed that adverse weather conditions (e.g. cool temperatures, wind, and rain) play a critical role in the realised fecundity of the beetle in the field (Kosior 1975). In addition to these natural factors affecting demographics of Cassida, it will be important to understand how farm management practices (e.g. grazing regime, fertilisation, and use of pesticides) affect its survival and fecundity. Comparative demographic studies in the native vs. introduced range might reveal biotic and abiotic factors that influence the beetle’s success as a biocontrol agent. Utilising this biocontrol agent to its fullest potential will require a greater understanding of its biology, behaviour, and factors limiting its population numbers.

Acknowledgements This work was supported by the Ministry for Business Innovation and Employment through the Undermining Weeds programme. I thank Simon Fowler for encouraging me to undertake this project, and Graeme Bourdôt for helpful comments on the manuscript.

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100 16 Defoliation Lower leaves 14 80 Upper leaves Cassida 12 Adults 10 60 Egg masses Larvae 8

40 6

Defoliation (%) Defoliation

Cassida / shoot / Cassida

4 20 2

0 0 Oct Nov Dec Jan Feb

Figure 1. Mean (±SE) percent leaf defoliation of the lower and upper halves of Cirsium arvense shoots (n = 13 to 15 shoots) by Cassida rubiginosa at Lincoln NZ from 4 October 2012 to 8 February 2013. The stacked bars represent the mean abundance per shoot of C. rubiginosa (adults, egg masses, and larvae) at each assessment date.

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The Weta 45:5-13 13 Ward RH, Pienkowski RL 1978b Mortality and parasitism of Cassida rubiginosa, a thistle-feeding shield beetle accidentally introduced into North America. Environmental Entomology 7: 5360540.

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Figure 2. Life stages and feeding damage of Cassida rubiginosa at Lincoln 2012/2013. Clockwise from top left to bottom left: Adult C. rubiginosa on Californian thistle, Cirsium arvense (September 2012); Egg mass and early instar larvae on the underside of Californian thistle leaf (November); Late instar larvae and leaf- feeding damage on Californian thistle (December); Feeding damage to Scotch thistle, Cirsium vulgare (January).