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Effects of soil conditions and drought on egg hatching and larval survival of the clover root weevil (Sitona lepidus)
Applied Soil Ecology 44 (2010) 75–79
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Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil
Effects of soil conditions and drought on egg hatching and larval survival of the clover root weevil (Sitona lepidus) Scott N. Johnson a,c,*, Peter J. Gregory a,c, James W. McNicol b, Yasmina Oodally c,1, Xiaoxian Zhang d, Philip J. Murray e a
Scottish Crop Research Institute, Invergowrie, Dundee, Scotland DD2 5DA, United Kingdom Biomathematics & Statistics Scotland, Scottish Crop Research Institute, Dundee DD2 5DA, United Kingdom Department of Soil Science, University of Reading, Whiteknights, Reading RG6 6DW, United Kingdom d Department of Engineering, University of Liverpool, Brownlow Street, Liverpool L69 3GQ, United Kingdom e North Wyke Research, Okehampton, Devon EX20 2SB, United Kingdom b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 6 July 2009 Received in revised form 5 October 2009 Accepted 7 October 2009
Soil-dwelling insect herbivores are significant pests in many managed ecosystems. Because eggs and larvae are difficult to observe, mathematical models have been developed to predict life-cycle events occurring in the soil. To date, these models have incorporated very little empirical information about how soil and drought conditions interact to shape these processes. This study investigated how soil temperature (10, 15, 20 and 25 8C), water content (0.02 (air dried), 0.10 and 0.25 g g 1) and pH (5, 7 and 9) interactively affected egg hatching and early larval lifespan of the clover root weevil (Sitona lepidus Gyllenhal, Coleoptera: Curculionidae). Eggs developed over 3.5 times faster at 25 8C compared with 10 8C (hatching after 40.1 and 11.5 days, respectively). The effect of drought on S. lepidus eggs was investigated by exposing eggs to drought conditions before wetting the soil (2–12 days later) at four temperatures. No eggs hatched in dry soil, suggesting that S. lepidus eggs require water to remain viable. Eggs hatched significantly sooner in slightly acidic soil (pH 5) compared with soils with higher pH values. There was also a significant interaction between soil temperature, pH and soil water content. Egg viability was significantly reduced by exposure to drought. When exposed to 2–6 days of drought, egg viability was 80–100% at all temperatures but fell to 50% after 12 days exposure at 10 8C and did not hatch at all at 20 8C and above. Drought exposure also increased hatching time of viable eggs. The effects of soil conditions on unfed larvae were less influential, except for soil temperature which significantly reduced larval longevity by 57% when reared at 25 8C compared with 10 8C (4.1 and 9.7 days, respectively). The effects of soil conditions on S. lepidus eggs and larvae are discussed in the context of global climate change and how such empirically based information could be useful for refining existing mathematical models of these processes. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Belowground herbivore Insect cuticle Macro-fauna Soil pH Soil temperature Soil water
1. Introduction Soil-dwelling insect herbivores are increasingly recognised both as major crop pests and key drivers of terrestrial ecosystem processes (e.g. Villani and Wright, 1990; Johnson and Murray, 2008). Life-cycles vary depending on taxa, but most consist of an aboveground adult stage that lays eggs that hatch in the soil and give rise to root-feeding larvae (Brown and Gange, 1990). Because
* Corresponding author at: Scottish Crop Research Institute, Environment–Plant Interactions, Invergowrie, Dundee, Scotland DD2 5DA, United Kingdom. Tel.: +44 01382 560016; fax: +44 01382 568502. E-mail address: [email protected] (S.N. Johnson). 1 Current address: Regional Grants Coordination, International Fund for Agricultural Development, Rome, Italy. 0929-1393/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2009.10.002
egg development and larval feeding takes place in the soil, it has been more challenging to observe these aspects of the lifecycle (Hunter, 2001; Johnson et al., 2007a). This has prompted researchers to develop a series of mathematical models to predict egg development patterns for some of the more economically important soil insects, including the vine weevil (Otiorhynchus sulcatus F.; Son and Lewis, 2005), the pea weevil (Sitona lineatus L.; Lerin, 2004) and the western corn rootworm (Diabrotica virgifera virgifera Le Conte; Schaafsma et al., 1993). More recently, such modelling approaches have been extended to include larval survival, in addition to egg development, for the clover root weevil (S. lepidus Gyllenhal; Johnson et al., 2007b). The benefits of forage legumes, such as white clover (Trifolium repens L.), in agricultural systems have long been known, primarily because of their capacity to fix atmospheric nitrogen and their high
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nutritional value for livestock. The clover root weevil is a particularly destructive pest of white clover (Murray and Clements, 1994). The adult weevil feeds on leaves of the plant and can cause significant damage. Eggs hatch in the soil and give rise to soil-dwelling larvae that then attack root nodules housing symbiotic Rhizobium spp. bacteria (Murray and Clements, 1998; Gerard, 2001; Johnson et al., 2005). Such damage can impose heavy losses in pastoral industries dependent on white clover by impairing nitrogen fixation and causing a diminution of white clover in the sward (Goldson et al., 2005). In common with other models of soil insect development (e.g. Schaafsma et al., 1993; Lerin, 2004; Son and Lewis, 2005) models describing egg hatching and larval behaviour of S. lepidus (Zhang et al., 2006; Johnson et al., 2007b) do not explicitly consider how multiple soil conditions may interactively affect developmental processes. Moreover, the few models that do include environmental parameters usually consider only temperature. This is surprising given that eggs and soil-dwelling larvae are in constant physical contact with the soil matrix and so likely to be affected by a range of soil conditions (see Villani and Wright, 1990). The purpose of this study was to investigate how key soil properties (temperature, pH and water content) and soil drought exposure interact to affect S. lepidus egg hatching time and the survival time of unfed emergent larvae. While some studies have examined the role of individual soil properties on the eggs and larvae of some other root feeding insects (Villani and Wright, 1990; Addison et al., 1998; Pacchioli and Hower, 2004), to our knowledge, none have examined the interactive effects of temperature, pH and water content. Moreover, the present study adopted a more realistic approach by conducting experiments in soil rather than artificial media (e.g. filter paper). Such empirical information will be essential to validate and refine existing mathematical models for S. lepidus (e.g. Zhang et al., 2006; Johnson et al., 2007b). We used a range of soil conditions relevant to conditions in Southern England during July–August when egg laying by S. lepidus is at its peak. Four temperatures (10, 15, 20 and 25 8C) were investigated, corresponding to the typical temperature range for the upper 5 cm of soil (Payne and Gregory, 1988). In addition to drought conditions (0.02 g g 1), soil water contents of 0.10 and 0.25 g g 1 were used to correspond to low and ambient summer rainfall during 2004 (Staley et al., 2007). Soil pH values of 5, 7 and 9 were used to represent the typical pH range of grassland soils in the region (Jarvis, 1968; Rowell, 1988). 2. Materials and methods Cultures of S. lepidus were maintained at 18 8C, 16L:8D as described by Johnson et al. (2004). Freshly laid eggs (<12-h-old) were harvested from female insects and combined at random to avoid influences of maternal origin in subsequent experiments.
wilting point) and 80 tubes were provided with 0.25 ml distilled H2O (0.25 g g 1 gravimetric water content, equivalent to field capacity). A single egg was embedded into the soil surface using a fine brush, before sealing the tube lids and dividing them between four temperature regimes; 10, 15, 20 and 25 8C. In summary, the experiment consisted of 20 replicates of each combination of soil pH (5, 7 and 9), soil water (0.02, 0.10 and 0.25 g g 1) and temperature (10, 15, 20 and 25 8C). Tubes were opened daily (providing ventilation) and inspected at 50 magnification to ascertain whether eggs had hatched. 2.2. Exposure of eggs to drought conditions at different temperatures This experiment explored how long S. lepidus eggs could withstand dry conditions before they became unviable. Four hundred and eighty micro-centrifuge tubes were filled with 1 ml pH 7 soil (details as in experiment 2.1) and divided into groups representing four temperature regimes (10, 15, 20 and 25 8C; 120 tubes each). A single egg was embedded into the soil in each tube which was then sealed. After two days, the soil was watered in 20 of the tubes at each temperature regime with 0.25 ml distilled H2O to give a gravimetric water content of 0.25 g g 1 (80 tubes in total). This was repeated for a different group of 20 tubes at each temperature regime at two day intervals up to 12 d later. Tubes were opened and examined daily to ascertain when, if at all, eggs hatched. 2.3. Impacts of soil temperature, pH and water content on larval survival time This experiment determined how long unfed neonatal S. lepidus larvae could survive under the soil conditions described in experiment 2.1. The bases of twenty-four Petri dish plates (Ø 9 cm) were covered with a c. 1 mm layer of soil (5 g, details as above, except sieved <75 mm). Soils were: pH 5, pH 7 and pH 9 (eight plates of each). For each group of plates, four were watered with 0.5 ml H2O and four were watered with 1.25 ml to give gravimetric water contents of 0.10 and 0.25 g g 1, respectively. Eggs harvested from the population were incubated at room temperature in separate Petri dish plates until larvae emerged. Ten of the larvae were placed randomly into each soil-filled Petri dish, and the lid sealed with Parafilm (Alpha Laboratories, Hampshire, UK). Each of the four plates was then stored at 10, 15, 20 and 25 8C so that there was a plate representing combinations of pH (5, 7 and 9), water content (10 and 25 g g 1 and temperature (10, 15, 20 and 25 8C). Plates were examined daily by removing lids to minimise the effects of air humidity. Mortality was recorded until all larvae had died, aided by lighting the plates from beneath and removing larvae as they died. 2.4. Statistical analysis
2.1. Impacts of soil temperature, pH and water content on egg hatching time The interactive effects of soil temperature, soil pH and soil water content on hatching of S. lepidus eggs were measured in this experiment. Three samples (approximately 250 g each of Sonning series B horizon sandy loam soil of pH 5; Jarvis, 1968) were air dried, sterilised and sieved to <1 mm particle size. Soil pH was altered by progressively adding CaCO3 to two of the samples to raise pH to 7 and 9, respectively, according to Rowell (1994). Two hundred and forty 2 ml micro-centrifuge tubes (Fisher, UK) were filled with 1 ml of soil of each pH (i.e. 720 tubes in total). For each group of tubes, 80 were left to air dry (water content was measured to be 0.02 g g 1), 80 tubes were given 0.1 ml distilled H2O (0.1 g g 1 gravimetric water content, equivalent to permanent
The effects of soil conditions and drought exposure on egg hatching time (experiments 2.1 and 2.2) were analysed with a generalized linear mixed model (GLMM) with Poisson error structure and log-link function (McCullagh and Nelder, 1989), to account for increasing variability in response with increasing temperature. Interactions between all soil factors were determined. Egg viability (experiment 2.2) was analysed with a generalised linear mixed model with a binomial distribution and logit-link function. Temperature was included as a random block term in mixed models and the dispersion parameter estimated. The effect of soil conditions on larval longevity (experiment 2.3) was analysed using analysis of variance with ‘temperature’ and ‘plate’ included as the block term. Two-way interactions between soil factors were determined for larval
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Fig. 1. Sitona lepidus egg hatching time (period between maternal oviposition and hatching) in response to soil temperature, soil pH and soil water content.
longevity, but the three-way interaction (temperature pH water content) was not reported due to the reduced denominator degrees of freedom. All analysis was conducted in GENSTAT (VSN International, Hemel Hempstead, UK).
3. Results 3.1. Impacts of soil temperature, pH and water content on egg hatching time Eggs kept in air dry soil did not hatch at any temperature regime, and were therefore excluded from the analysis. All eggs hatched in the 0.10 and 0.25 g g 1 soil water treatments. Soil temperature was by far the most significant driver of egg hatching time, with higher soil temperatures significantly reducing egg hatching time (Fig. 1 and Table 1). Soil pH also affected egg hatching time, with eggs hatching more quickly in slightly acidic (pH 5) soil (Fig. 1 and Table 1). Soil water content and soil pH did not significantly affect egg hatching time, although both had interactive effects with soil temperature (Table 1). Soil pH had an interactive effect with soil temperature (Table 1) whereby eggs hatched more quickly in pH 5 soil at 15 8C compared to other temperatures (Fig. 1) and there was a three-way interaction between temperature, pH and soil water content in which 0.25 g g 1 soil water content reduced hatching time of eggs in pH 5 soil at 20 and 25 8C more so than at cooler temperatures. 3.2. Exposure of eggs to drought conditions at different temperatures Egg viability was reduced with longer drought exposure (Table 2 and Fig. 2A). In particular, all eggs hatched with two days of drought exposure but progressively fewer eggs hatched with increasing exposure to drought. In terms of statistical significance, there was no interactive effect of temperature and Table 1 Analysis of the impacts of soil conditions on egg hatching time using a generalised linear mixed model with Poisson error structure and log-link function. ‘Temperature’ also fitted as the random block term. Statistically significant (P < 0.05) factors indicated in bold. Factor
DF
F value
P
Temperature Temperature water content Temperature pH Temperature pH water content Water content Water content pH pH
3, 3, 6, 6,
449 449 449 449
7.25 0.26 3.23 2.32
<0.001 0.854 0.004 0.032
1, 449 2, 449 2, 449
1.54 0.99 3.17
0.215 0.373 0.043
drought exposure, although drought reduced egg viability far more at higher temperatures (Fig. 2A). Indeed, no eggs hatched after 12 days exposure to drought above 20 8C. Temperature and drought exposure significantly affected the time taken for eggs to hatch; increasing temperature reduced egg hatching time, whereas increasing drought exposure increased hatching time (Table 2 and Fig. 2B). For hatching time, there was no interaction between temperature and drought exposure. 3.3. Impacts of soil temperature, pH and water content on larval survival time In this experiment, larval lifespan was much less affected by soil conditions than the eggs (Table 3), although temperature significantly reduced larval lifespan, with larvae surviving significantly longer in colder soils (Fig. 3 and Table 3). 4. Discussion This study aimed to empirically test how key soil conditions and drought exposure affected egg hatching rates and the lifespan of unfed S. lepidus larvae. We found that soil temperature was the most important factor driving these processes, but that other soil conditions also had significant effects. In particular, drought conditions severely affected egg viability. Soil water relations are known to affect soil insect eggs and larvae, with several species becoming desiccated under dry conditions (reviewed by Brown and Gange, 1990). In the present study, S. lepidus eggs did not hatch at all under very dry conditions, and became increasingly less viable as the period between oviposition and soil wetting increased. A similar pattern was seen
Table 2 Analysis of the impacts of drought on (A) egg viability and (B) egg hatching time at different temperatures using generalised linear mixed models with (A) a binomial error structure and logit-link function and (B) a Poisson error structure and log-link function. ‘Temperature’ fitted as the random block term. Statistically significant (P < 0.05) factors indicated in bold. Factor
DF
F value
P
A. Egg viability Temperature Drought exposure Temperature drought exposure
3, 456 5, 456 15, 456
1.06 19.54 0.68
0.367 <0.001 0.804
B. Egg hatching time Temperature Drought exposure Temperature drought exposure
3, 324 5, 324 13, 324
525.16 3.99 0.89
<0.001 0.001 0.560
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Table 3 Analysis of the impacts of soil conditions on larval lifespan using analysis of variance including ‘temperature’ and ‘plate’ as the block term. Statistically significant (P < 0.05) factors indicated in bold. Factor
DF
F value
P
Temperature Temperature water content Temperature pH Water content Water content pH pH
3, 3, 6, 1, 2, 2,
12.02 0.71 1.34 0.14 0.43 2.77
0.006 0.581 0.364 0.720 0.670 0.140
6 6 6 6 6 6
with some chafers (Potter, 1983) and corn rootworms (Krysan, 1976) which must imbibe water prior to hatching. Using the low and ambient rainfall conditions (0.10 and 0.25 g g 1 soil water content) described in Staley et al. (2007), we found no significant difference in how the two levels affected S. lepidus eggs or larvae. While some soil insects appear to benefit
Fig. 2. (A) Sitona lepidus egg viability as affected by exposure to drought (time between oviposition and soil wetting) at four different soil temperatures. (B) Impacts of drought exposure and temperature on egg hatching time.
from relatively damper soils (Lummus et al., 1983; Staley et al., 2007) there are also numerous studies reporting no effects (Brown and Gange, 1990). In field experiments, Addison et al. (1998) reported that there was no difference between irrigated and nonirrigated paddocks in terms of numbers of S. lepidus eggs and larvae, which is broadly consistent with the laboratory observations reported here. It seems, therefore, that while very dry conditions have extremely detrimental effects on S. lepidus eggs and larvae, the water content thereafter appears to be much less influential. In the northern hemisphere, predictive models consistently indicate that drought conditions will become a dominant feature of the summer growing season due to increased evaporation in the spring, reduced precipitation in summer and generally warmer soil temperatures (McCarthy et al., 2001; Wang, 2005). Under such circumstances, sporadic episodes of egg mortality in S. lepidus could occur during summer months, although this has to be considered against the potentially improved performance of larvae due to other factors such as elevated CO2 (Gregory et al., 2009). Soil temperature had the most significant and consistent effects on S. lepidus egg hatching rates and larval lifespan. Increasing temperature accelerated S. lepidus egg hatching rates but reduced larval survival (probably due to more rapid desiccation). The negative effects of drought exposure on egg development were exacerbated at higher temperatures, further emphasising the vulnerability of eggs and larvae to desiccation at higher soil temperatures. Temperature tolerances and thresholds of soil insects often reflect their geographical range with those from mid–high latitudes able to survive at soil temperatures of 10 8C (e.g. Block et al., 1987) whereas those from warmer regions can require minimum threshold temperatures of 20 8C (e.g. King et al., 1981). Moreover, soil temperature strongly affects the behavioural responses of soil insects, with many moving vertically in the soil profile to avoid adverse (too warm or cool) temperatures (Dowdy, 1944; Villani and Wright, 1990). Global climate change is predicted to increase temperature in the upper soil (0–5 cm) by 1.6–3.4 8C by 2100 (Anderson, 1992), which is likely to have several effects on soil insects (Collier et al., 1991; Briones et al., 1997; Staley and Johnson, 2008) including S. lepidus. In particular, higher temperatures could speed up egg development resulting in more than one generation per year in the UK, which would be akin to S. lepidus in New Zealand (Gerard et al., 1999; Goldson and Gerard, 2008). Conversely, the time available for larvae to locate suitable host plants before starvation would be reduced at higher soil temperatures, unless searching efficiency and burrowing speeds increased at higher temperatures (see Johnson et al., 2006). Soil pH affected egg hatching time but did not affect larval lifespan. In particular, there seemed to be a trend for shorter hatching periods in slightly acidic soil (pH 5). Studies concerning
Fig. 3. Larval lifespan of newly hatched and unfed S. lepidus larvae in response to soil temperature, soil pH and soil water content.
S.N. Johnson et al. / Applied Soil Ecology 44 (2010) 75–79
the effect of pH on soil insects are scarce and often conflicting (Brown and Gange, 1990) and have focussed on larval stages rather than eggs in the soil. Exactly why acidic soils speed up S. lepidus egg hatching time is unclear, but it has been suggested that the egg chorion (hardened egg shell) of foliar insects can dissolve more easily under acidic conditions which eases the emergence of larvae (Helio¨vaara et al., 1992). Moreover, weak acids can act as sterilising agent which make insect eggs less susceptible to pathogens (e.g. Neuvonen et al., 1990). While soil temperature is probably the most important environmental factor to include in mathematical models for S. lepidus egg hatching and larval survival (Johnson et al., 2007b), other soil properties clearly have important effects. A significant conclusion of this study was that soil conditions (soil temperature, pH and water content) interact to affect egg hatching time. This is an important consideration for developing mathematical models, since existing models tend to only incorporate single environmental factors (usually soil temperature) if at all. Such considerations are likely to become more relevant in predictive models because of the effects of global climate change on soils (Anderson, 1992). In presenting these results, we hope to encourage soil ecologists to further investigate the complex and interacting effects of soil conditions on root-feeding insects to provide an empirical basis for future mathematical models. In turn, more accurate predictive models of egg hatching and larval lifespan could help to develop more integrated control strategies (e.g. targeted insecticide application) for some of the most significant insect pests in managed ecosystems (Blackshaw and Kerry, 2008). Acknowledgements The authors would like to thank Denise Headon of the North Wyke Research for collecting insects from the field, Dr Glyn Bengough, Dr Jane Wishart and two anonymous referees for their suggestions for improving this manuscript. This work was financially supported by the BBSRC (project 45/D14536). References Addison, P.J., Willoughby, B.E., Hardwick, S., Gerard, P.J., 1998. Clover root weevil: observations on differences between 1997 and 1998 summer populations in the Waikato. Proc. New Zeal. Plant Protection Conf. 51, 1–4. Anderson, J.M., 1992. Responses of soils to climate change. Adv. Ecol. Res. 22, 163– 210. Blackshaw, R.P., Kerry, B.R., 2008. Root herbivory in agricultural ecosystems. In: Johnson, S.N., Murray, P.J. (Eds.), Root Feeders—An Ecosystem Perspective. CABI, Wallingford, UK, pp. 35–53. Block, W., Turnock, W.J., Jones, T.H., 1987. Cold resistance and overwintering survival of the cabbage root fly, Delia radicum (Anthomyiidae), and its parasitoid, Trybliographa rapae (Cynipidae), in England. Oecologia 71, 332–338. Briones, M.J.I., Ineson, P., Piearce, T.G., 1997. Effects of climate change on soil fauna: responses of enchytraeids, Diptera larvae and tardigrades in a transplant experiment. Appl. Soil Ecol. 6, 117–134. Brown, V.K., Gange, A.C., 1990. Insect herbivory below ground. Adv. Ecol. Res. 20, 1– 58. Collier, R.H., Finch, S., Phelps, K., Thompson, A.R., 1991. Possible impact of global warming on cabbage root fly (Delia radicum) activity in the UK. Ann. Appl. Biol. 118, 261–271. Dowdy, W.W., 1944. The influence of temperature on vertical migration of invertebrates inhabiting different soil types. Ecology 25, 449–460. Gerard, P.J., Addison, P.J., Hardwick, S., Willoughby, B.E., 1999. Establishment of the invader: insights into the life history and biology of Sitona lepidus in the Waikato region of New Zealand. In: Proceedings of the Seventh Australasian Conference on Grassland and Invertebrate Ecology. pp. 43–51. Gerard, P.J., 2001. Dependence of Sitona lepidus (Coleoptera: Curculionidae) larvae on abundance of white clover Rhizobium nodules. B. Entomol. Res. 91, 149–152. Goldson, S.L., Rowarth, J.S., Caradus, J.R., 2005. The impact of invasive invertebrate pests in pastoral agriculture: a review. New Zeal. J. Agric. Res. 48, 401–415. Goldson, S.L., Gerard, P.J., 2008. Using biocontrol against root-feeding pests with particular reference to Sitona root weevils. In: Johnson, S.N., Murray, P.J. (Eds.), Root Feeders—An Ecosystem Perspective. CABI, Wallingford, UK, pp. 115–133.
79
Gregory, P.J., Johnson, S.N., Newton, A.C., Ingram, J.S.I., 2009. Integrating pests and pathogens into the climate change/food security debate. J. Exp. Bot. 60, 2827– 2838. Helio¨vaara, K., Va¨isa¨nen, R., Varama, M., 1992. Acidic precipitation increases egg survival in Neodiprion sertifer. Entomol. Exp. Appl. 62, 55–60. Hunter, M.D., 2001. Out of sight, out of mind: the impacts of root-feeding insects in natural and managed systems. Agr. Forest Entomol. 3, 3–9. Jarvis, R.A., 1968. Soils of the Reading district. Memoir of the Soil Survey of Great Britain—England & Wales. Harpenden, Herts, UK. Johnson, S.N., Gregory, P.J., Murray, P.J., Zhang, X., Young, I.M., 2004. Host plant recognition by the root-feeding clover weevil Sitona lepidus (Coleoptera: Curculionidae). B. Entomol. Res. 94, 433–439. Johnson, S.N., Gregory, P.J., Greenham, J.R., Zhang, X., Murray, P.J., 2005. Attractive properties of an isoflavonoid found in white clover root nodules on the clover root weevil. J. Chem. Ecol. 31, 2223–2229. Johnson, S.N., Zhang, X.X., Crawford, J.W., Gregory, P.J., Hix, N.J., Jarvis, S.J., Murray, P.J., Young, I.M., 2006. Effects of CO2 on the searching behaviour of the rootfeeding clover weevil. B. Entomol. Res. 96, 361–366. Johnson, S.N., Crawford, J.W., Gregory, P.J., Grinev, D.V., Mankin, R.W., Masters, G.J., Murray, P.J., Wall, D.H., Zhang, X.X., 2007a. Non-invasive techniques for investigating and modelling root-feeding insects in managed and natural systems. Agric. Forest Entomol. 9, 39–46. Johnson, S.N., Zhang, X., Crawford, J.W., Gregory, P.J., Young, I.M., 2007b. Egg hatching and survival time of soil-dwelling insect larvae: a partial differential equation model and experimental validation. Ecol. Model. 202, 493–502. Johnson, S.N., Murray, P.J. (Eds.), 2008. Root Feeders—An Ecosystem Perspective. CABI, Wallingford, UK. King, P.D., Mercer, C.F., Meekings, J.S., 1981. Ecology of black beetle, Heteronychus arator (Coleoptera Scarabaeidae)—influence of temperature on feeding, growth, and survival of the larvae. New Zeal. J. Zool. 8, 113–117. Krysan, J.L., 1976. Moisture relationships of the egg of the Southern corn rootworm Diabrotica undecimpunctata howardi (Coleoptera Chrysomelidae). Entomol. Exp. Appl. 20, 154–162. Lerin, J., 2004. Modeling embryonic development in Sitona lineatus (Coleoptera: Curculionidae) in fluctuating temperatures. Environ. Entomol. 33, 107–112. Lummus, P.F., Smith, J.C., Powell, N.L., 1983. Soil moisture and texture effects on survival of immature Southern corn rootworms, Diabrotica undecimpunctata howardi Barber (Coleoptera Chrysomelidae). Environ. Entomol. 12, 1529–1531. McCarthy, J.J., Canziani, O.F., Leary, N.A., Dokken, D.J., White, K.S., 2001. Hydrology and water resources. In: McCarthy, J.J., Canziani, O.F., Leary, N.A., Dokken, D.J., White, K.S. (Eds.), Climate Change 2001: Impacts, Adaptation and Vulnerability. Cambridge University Press, Cambridge, pp. 191–234. McCullagh, P., Nelder, J.A., 1989. Generalized Linear Models. Chapman & Hall, New York. Murray, P.J., Clements, R.O., 1994. Investigations of the host feeding preferences of Sitona weevils found commonly on white clover (Trifolium repens) in the UK. Entomol. Exp. Appl. 71, 73–79. Murray, P.J., Clements, R.O., 1998. Transfer of nitrogen between clover and wheat: effect of root herbivory. Eur. J. Soil Biol. 34, 25–30. Neuvonen, S., Saikkonen, K., Haukioja, E., 1990. Simulated acid rain reduces the susceptibility of the European pine sawfly (Neodiprion sertifer) to its nuclear polyhedrosis virus. Oecologia 83, 209–212. Pacchioli, M.A., Hower, A.A., 2004. Soil and moisture effects on the dynamics of early instar clover root curculio (Coleoptera: Curculionidae) and biomass of alfalfa root nodules. Environ. Entomol. 33, 119–127. Payne, D., Gregory, P.J., 1988. The temperature of the soil. In: Wild, A. (Ed.), Russell’s Soil Conditions and Plant Growth. Longman, Harlow, UK, pp. 282–297. Potter, D.A., 1983. Effect of soil moisture on oviposition, water absorption, and survival of Southern masked chafer (Coleoptera, Scarabaeidae) eggs. Environ. Entomol. 12, 1223–1227. Rowell, D.L., 1988. Soil acidity and alkalinity. In: Wild, A. (Ed.), Russell’s Soil Conditions and Plant Growth. Longman, Harlow, UK, pp. 844–898. Rowell, D.L., 1994. Soil Science: Methods And Applications. Longman, Harlow, UK. Schaafsma, A.W., Fuentes, J.D., Gillespie, T.J., Whitfield, G.H., Ellis, C.R., 1993. Performance of a model for egg hatching of the Western corn rootworm Diabrotica virgifera virgifera Le Conte, using measured and modeled soil temperatures as input. Int. J. Biometeorol. 37, 11–18. Son, Y., Lewis, E.E., 2005. Modelling temperature-dependent development and survival of Otiorhynchus sulcatus (Coleoptera: Curculionidae). Agric. Forest Entomol. 7, 201–209. Staley, J.T., Hodgson, C.J., Mortimer, S.R., Morecroft, M.D., Masters, G.J., Brown, V.K., Taylor, M.E., 2007. Effects of summer rainfall manipulations on the abundance and vertical distribution of herbivorous soil macro-invertebrates. Eur. J. Soil Biol. 43, 189–198. Staley, J.T., Johnson, S.N., 2008. Climate change impacts on root herbivores. In: Johnson, S.N., Murray, P.J. (Eds.), Root Feeders—An Ecosystem Perspective. CABI, Wallingford, UK, pp. 192–213. Villani, M.G., Wright, R.J., 1990. Environmental influences on soil macroarthropod behavior in agricultural systems. Annu. Rev. Entomol. 35, 249–269. Wang, G.L., 2005. Agricultural drought in a future climate: results from 15 global climate models participating in the IPCC 4th assessment. Clim. Dynam. 25, 739– 753. Zhang, X., Johnson, S.N., Gregory, P.J., Crawford, J.W., Young, I.M., Murray, P.J., Jarvis, S.C., 2006. Modelling the movement and survival of the root-feeding clover weevil, Sitona lepidus, in the root-zone of white clover. Ecol. Model. 190, 133– 146.
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Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil
Effects of soil conditions and drought on egg hatching and larval survival of the clover root weevil (Sitona lepidus) Scott N. Johnson a,c,*, Peter J. Gregory a,c, James W. McNicol b, Yasmina Oodally c,1, Xiaoxian Zhang d, Philip J. Murray e a
Scottish Crop Research Institute, Invergowrie, Dundee, Scotland DD2 5DA, United Kingdom Biomathematics & Statistics Scotland, Scottish Crop Research Institute, Dundee DD2 5DA, United Kingdom Department of Soil Science, University of Reading, Whiteknights, Reading RG6 6DW, United Kingdom d Department of Engineering, University of Liverpool, Brownlow Street, Liverpool L69 3GQ, United Kingdom e North Wyke Research, Okehampton, Devon EX20 2SB, United Kingdom b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 6 July 2009 Received in revised form 5 October 2009 Accepted 7 October 2009
Soil-dwelling insect herbivores are significant pests in many managed ecosystems. Because eggs and larvae are difficult to observe, mathematical models have been developed to predict life-cycle events occurring in the soil. To date, these models have incorporated very little empirical information about how soil and drought conditions interact to shape these processes. This study investigated how soil temperature (10, 15, 20 and 25 8C), water content (0.02 (air dried), 0.10 and 0.25 g g 1) and pH (5, 7 and 9) interactively affected egg hatching and early larval lifespan of the clover root weevil (Sitona lepidus Gyllenhal, Coleoptera: Curculionidae). Eggs developed over 3.5 times faster at 25 8C compared with 10 8C (hatching after 40.1 and 11.5 days, respectively). The effect of drought on S. lepidus eggs was investigated by exposing eggs to drought conditions before wetting the soil (2–12 days later) at four temperatures. No eggs hatched in dry soil, suggesting that S. lepidus eggs require water to remain viable. Eggs hatched significantly sooner in slightly acidic soil (pH 5) compared with soils with higher pH values. There was also a significant interaction between soil temperature, pH and soil water content. Egg viability was significantly reduced by exposure to drought. When exposed to 2–6 days of drought, egg viability was 80–100% at all temperatures but fell to 50% after 12 days exposure at 10 8C and did not hatch at all at 20 8C and above. Drought exposure also increased hatching time of viable eggs. The effects of soil conditions on unfed larvae were less influential, except for soil temperature which significantly reduced larval longevity by 57% when reared at 25 8C compared with 10 8C (4.1 and 9.7 days, respectively). The effects of soil conditions on S. lepidus eggs and larvae are discussed in the context of global climate change and how such empirically based information could be useful for refining existing mathematical models of these processes. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Belowground herbivore Insect cuticle Macro-fauna Soil pH Soil temperature Soil water
1. Introduction Soil-dwelling insect herbivores are increasingly recognised both as major crop pests and key drivers of terrestrial ecosystem processes (e.g. Villani and Wright, 1990; Johnson and Murray, 2008). Life-cycles vary depending on taxa, but most consist of an aboveground adult stage that lays eggs that hatch in the soil and give rise to root-feeding larvae (Brown and Gange, 1990). Because
* Corresponding author at: Scottish Crop Research Institute, Environment–Plant Interactions, Invergowrie, Dundee, Scotland DD2 5DA, United Kingdom. Tel.: +44 01382 560016; fax: +44 01382 568502. E-mail address: [email protected] (S.N. Johnson). 1 Current address: Regional Grants Coordination, International Fund for Agricultural Development, Rome, Italy. 0929-1393/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2009.10.002
egg development and larval feeding takes place in the soil, it has been more challenging to observe these aspects of the lifecycle (Hunter, 2001; Johnson et al., 2007a). This has prompted researchers to develop a series of mathematical models to predict egg development patterns for some of the more economically important soil insects, including the vine weevil (Otiorhynchus sulcatus F.; Son and Lewis, 2005), the pea weevil (Sitona lineatus L.; Lerin, 2004) and the western corn rootworm (Diabrotica virgifera virgifera Le Conte; Schaafsma et al., 1993). More recently, such modelling approaches have been extended to include larval survival, in addition to egg development, for the clover root weevil (S. lepidus Gyllenhal; Johnson et al., 2007b). The benefits of forage legumes, such as white clover (Trifolium repens L.), in agricultural systems have long been known, primarily because of their capacity to fix atmospheric nitrogen and their high
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nutritional value for livestock. The clover root weevil is a particularly destructive pest of white clover (Murray and Clements, 1994). The adult weevil feeds on leaves of the plant and can cause significant damage. Eggs hatch in the soil and give rise to soil-dwelling larvae that then attack root nodules housing symbiotic Rhizobium spp. bacteria (Murray and Clements, 1998; Gerard, 2001; Johnson et al., 2005). Such damage can impose heavy losses in pastoral industries dependent on white clover by impairing nitrogen fixation and causing a diminution of white clover in the sward (Goldson et al., 2005). In common with other models of soil insect development (e.g. Schaafsma et al., 1993; Lerin, 2004; Son and Lewis, 2005) models describing egg hatching and larval behaviour of S. lepidus (Zhang et al., 2006; Johnson et al., 2007b) do not explicitly consider how multiple soil conditions may interactively affect developmental processes. Moreover, the few models that do include environmental parameters usually consider only temperature. This is surprising given that eggs and soil-dwelling larvae are in constant physical contact with the soil matrix and so likely to be affected by a range of soil conditions (see Villani and Wright, 1990). The purpose of this study was to investigate how key soil properties (temperature, pH and water content) and soil drought exposure interact to affect S. lepidus egg hatching time and the survival time of unfed emergent larvae. While some studies have examined the role of individual soil properties on the eggs and larvae of some other root feeding insects (Villani and Wright, 1990; Addison et al., 1998; Pacchioli and Hower, 2004), to our knowledge, none have examined the interactive effects of temperature, pH and water content. Moreover, the present study adopted a more realistic approach by conducting experiments in soil rather than artificial media (e.g. filter paper). Such empirical information will be essential to validate and refine existing mathematical models for S. lepidus (e.g. Zhang et al., 2006; Johnson et al., 2007b). We used a range of soil conditions relevant to conditions in Southern England during July–August when egg laying by S. lepidus is at its peak. Four temperatures (10, 15, 20 and 25 8C) were investigated, corresponding to the typical temperature range for the upper 5 cm of soil (Payne and Gregory, 1988). In addition to drought conditions (0.02 g g 1), soil water contents of 0.10 and 0.25 g g 1 were used to correspond to low and ambient summer rainfall during 2004 (Staley et al., 2007). Soil pH values of 5, 7 and 9 were used to represent the typical pH range of grassland soils in the region (Jarvis, 1968; Rowell, 1988). 2. Materials and methods Cultures of S. lepidus were maintained at 18 8C, 16L:8D as described by Johnson et al. (2004). Freshly laid eggs (<12-h-old) were harvested from female insects and combined at random to avoid influences of maternal origin in subsequent experiments.
wilting point) and 80 tubes were provided with 0.25 ml distilled H2O (0.25 g g 1 gravimetric water content, equivalent to field capacity). A single egg was embedded into the soil surface using a fine brush, before sealing the tube lids and dividing them between four temperature regimes; 10, 15, 20 and 25 8C. In summary, the experiment consisted of 20 replicates of each combination of soil pH (5, 7 and 9), soil water (0.02, 0.10 and 0.25 g g 1) and temperature (10, 15, 20 and 25 8C). Tubes were opened daily (providing ventilation) and inspected at 50 magnification to ascertain whether eggs had hatched. 2.2. Exposure of eggs to drought conditions at different temperatures This experiment explored how long S. lepidus eggs could withstand dry conditions before they became unviable. Four hundred and eighty micro-centrifuge tubes were filled with 1 ml pH 7 soil (details as in experiment 2.1) and divided into groups representing four temperature regimes (10, 15, 20 and 25 8C; 120 tubes each). A single egg was embedded into the soil in each tube which was then sealed. After two days, the soil was watered in 20 of the tubes at each temperature regime with 0.25 ml distilled H2O to give a gravimetric water content of 0.25 g g 1 (80 tubes in total). This was repeated for a different group of 20 tubes at each temperature regime at two day intervals up to 12 d later. Tubes were opened and examined daily to ascertain when, if at all, eggs hatched. 2.3. Impacts of soil temperature, pH and water content on larval survival time This experiment determined how long unfed neonatal S. lepidus larvae could survive under the soil conditions described in experiment 2.1. The bases of twenty-four Petri dish plates (Ø 9 cm) were covered with a c. 1 mm layer of soil (5 g, details as above, except sieved <75 mm). Soils were: pH 5, pH 7 and pH 9 (eight plates of each). For each group of plates, four were watered with 0.5 ml H2O and four were watered with 1.25 ml to give gravimetric water contents of 0.10 and 0.25 g g 1, respectively. Eggs harvested from the population were incubated at room temperature in separate Petri dish plates until larvae emerged. Ten of the larvae were placed randomly into each soil-filled Petri dish, and the lid sealed with Parafilm (Alpha Laboratories, Hampshire, UK). Each of the four plates was then stored at 10, 15, 20 and 25 8C so that there was a plate representing combinations of pH (5, 7 and 9), water content (10 and 25 g g 1 and temperature (10, 15, 20 and 25 8C). Plates were examined daily by removing lids to minimise the effects of air humidity. Mortality was recorded until all larvae had died, aided by lighting the plates from beneath and removing larvae as they died. 2.4. Statistical analysis
2.1. Impacts of soil temperature, pH and water content on egg hatching time The interactive effects of soil temperature, soil pH and soil water content on hatching of S. lepidus eggs were measured in this experiment. Three samples (approximately 250 g each of Sonning series B horizon sandy loam soil of pH 5; Jarvis, 1968) were air dried, sterilised and sieved to <1 mm particle size. Soil pH was altered by progressively adding CaCO3 to two of the samples to raise pH to 7 and 9, respectively, according to Rowell (1994). Two hundred and forty 2 ml micro-centrifuge tubes (Fisher, UK) were filled with 1 ml of soil of each pH (i.e. 720 tubes in total). For each group of tubes, 80 were left to air dry (water content was measured to be 0.02 g g 1), 80 tubes were given 0.1 ml distilled H2O (0.1 g g 1 gravimetric water content, equivalent to permanent
The effects of soil conditions and drought exposure on egg hatching time (experiments 2.1 and 2.2) were analysed with a generalized linear mixed model (GLMM) with Poisson error structure and log-link function (McCullagh and Nelder, 1989), to account for increasing variability in response with increasing temperature. Interactions between all soil factors were determined. Egg viability (experiment 2.2) was analysed with a generalised linear mixed model with a binomial distribution and logit-link function. Temperature was included as a random block term in mixed models and the dispersion parameter estimated. The effect of soil conditions on larval longevity (experiment 2.3) was analysed using analysis of variance with ‘temperature’ and ‘plate’ included as the block term. Two-way interactions between soil factors were determined for larval
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Fig. 1. Sitona lepidus egg hatching time (period between maternal oviposition and hatching) in response to soil temperature, soil pH and soil water content.
longevity, but the three-way interaction (temperature pH water content) was not reported due to the reduced denominator degrees of freedom. All analysis was conducted in GENSTAT (VSN International, Hemel Hempstead, UK).
3. Results 3.1. Impacts of soil temperature, pH and water content on egg hatching time Eggs kept in air dry soil did not hatch at any temperature regime, and were therefore excluded from the analysis. All eggs hatched in the 0.10 and 0.25 g g 1 soil water treatments. Soil temperature was by far the most significant driver of egg hatching time, with higher soil temperatures significantly reducing egg hatching time (Fig. 1 and Table 1). Soil pH also affected egg hatching time, with eggs hatching more quickly in slightly acidic (pH 5) soil (Fig. 1 and Table 1). Soil water content and soil pH did not significantly affect egg hatching time, although both had interactive effects with soil temperature (Table 1). Soil pH had an interactive effect with soil temperature (Table 1) whereby eggs hatched more quickly in pH 5 soil at 15 8C compared to other temperatures (Fig. 1) and there was a three-way interaction between temperature, pH and soil water content in which 0.25 g g 1 soil water content reduced hatching time of eggs in pH 5 soil at 20 and 25 8C more so than at cooler temperatures. 3.2. Exposure of eggs to drought conditions at different temperatures Egg viability was reduced with longer drought exposure (Table 2 and Fig. 2A). In particular, all eggs hatched with two days of drought exposure but progressively fewer eggs hatched with increasing exposure to drought. In terms of statistical significance, there was no interactive effect of temperature and Table 1 Analysis of the impacts of soil conditions on egg hatching time using a generalised linear mixed model with Poisson error structure and log-link function. ‘Temperature’ also fitted as the random block term. Statistically significant (P < 0.05) factors indicated in bold. Factor
DF
F value
P
Temperature Temperature water content Temperature pH Temperature pH water content Water content Water content pH pH
3, 3, 6, 6,
449 449 449 449
7.25 0.26 3.23 2.32
<0.001 0.854 0.004 0.032
1, 449 2, 449 2, 449
1.54 0.99 3.17
0.215 0.373 0.043
drought exposure, although drought reduced egg viability far more at higher temperatures (Fig. 2A). Indeed, no eggs hatched after 12 days exposure to drought above 20 8C. Temperature and drought exposure significantly affected the time taken for eggs to hatch; increasing temperature reduced egg hatching time, whereas increasing drought exposure increased hatching time (Table 2 and Fig. 2B). For hatching time, there was no interaction between temperature and drought exposure. 3.3. Impacts of soil temperature, pH and water content on larval survival time In this experiment, larval lifespan was much less affected by soil conditions than the eggs (Table 3), although temperature significantly reduced larval lifespan, with larvae surviving significantly longer in colder soils (Fig. 3 and Table 3). 4. Discussion This study aimed to empirically test how key soil conditions and drought exposure affected egg hatching rates and the lifespan of unfed S. lepidus larvae. We found that soil temperature was the most important factor driving these processes, but that other soil conditions also had significant effects. In particular, drought conditions severely affected egg viability. Soil water relations are known to affect soil insect eggs and larvae, with several species becoming desiccated under dry conditions (reviewed by Brown and Gange, 1990). In the present study, S. lepidus eggs did not hatch at all under very dry conditions, and became increasingly less viable as the period between oviposition and soil wetting increased. A similar pattern was seen
Table 2 Analysis of the impacts of drought on (A) egg viability and (B) egg hatching time at different temperatures using generalised linear mixed models with (A) a binomial error structure and logit-link function and (B) a Poisson error structure and log-link function. ‘Temperature’ fitted as the random block term. Statistically significant (P < 0.05) factors indicated in bold. Factor
DF
F value
P
A. Egg viability Temperature Drought exposure Temperature drought exposure
3, 456 5, 456 15, 456
1.06 19.54 0.68
0.367 <0.001 0.804
B. Egg hatching time Temperature Drought exposure Temperature drought exposure
3, 324 5, 324 13, 324
525.16 3.99 0.89
<0.001 0.001 0.560
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Table 3 Analysis of the impacts of soil conditions on larval lifespan using analysis of variance including ‘temperature’ and ‘plate’ as the block term. Statistically significant (P < 0.05) factors indicated in bold. Factor
DF
F value
P
Temperature Temperature water content Temperature pH Water content Water content pH pH
3, 3, 6, 1, 2, 2,
12.02 0.71 1.34 0.14 0.43 2.77
0.006 0.581 0.364 0.720 0.670 0.140
6 6 6 6 6 6
with some chafers (Potter, 1983) and corn rootworms (Krysan, 1976) which must imbibe water prior to hatching. Using the low and ambient rainfall conditions (0.10 and 0.25 g g 1 soil water content) described in Staley et al. (2007), we found no significant difference in how the two levels affected S. lepidus eggs or larvae. While some soil insects appear to benefit
Fig. 2. (A) Sitona lepidus egg viability as affected by exposure to drought (time between oviposition and soil wetting) at four different soil temperatures. (B) Impacts of drought exposure and temperature on egg hatching time.
from relatively damper soils (Lummus et al., 1983; Staley et al., 2007) there are also numerous studies reporting no effects (Brown and Gange, 1990). In field experiments, Addison et al. (1998) reported that there was no difference between irrigated and nonirrigated paddocks in terms of numbers of S. lepidus eggs and larvae, which is broadly consistent with the laboratory observations reported here. It seems, therefore, that while very dry conditions have extremely detrimental effects on S. lepidus eggs and larvae, the water content thereafter appears to be much less influential. In the northern hemisphere, predictive models consistently indicate that drought conditions will become a dominant feature of the summer growing season due to increased evaporation in the spring, reduced precipitation in summer and generally warmer soil temperatures (McCarthy et al., 2001; Wang, 2005). Under such circumstances, sporadic episodes of egg mortality in S. lepidus could occur during summer months, although this has to be considered against the potentially improved performance of larvae due to other factors such as elevated CO2 (Gregory et al., 2009). Soil temperature had the most significant and consistent effects on S. lepidus egg hatching rates and larval lifespan. Increasing temperature accelerated S. lepidus egg hatching rates but reduced larval survival (probably due to more rapid desiccation). The negative effects of drought exposure on egg development were exacerbated at higher temperatures, further emphasising the vulnerability of eggs and larvae to desiccation at higher soil temperatures. Temperature tolerances and thresholds of soil insects often reflect their geographical range with those from mid–high latitudes able to survive at soil temperatures of 10 8C (e.g. Block et al., 1987) whereas those from warmer regions can require minimum threshold temperatures of 20 8C (e.g. King et al., 1981). Moreover, soil temperature strongly affects the behavioural responses of soil insects, with many moving vertically in the soil profile to avoid adverse (too warm or cool) temperatures (Dowdy, 1944; Villani and Wright, 1990). Global climate change is predicted to increase temperature in the upper soil (0–5 cm) by 1.6–3.4 8C by 2100 (Anderson, 1992), which is likely to have several effects on soil insects (Collier et al., 1991; Briones et al., 1997; Staley and Johnson, 2008) including S. lepidus. In particular, higher temperatures could speed up egg development resulting in more than one generation per year in the UK, which would be akin to S. lepidus in New Zealand (Gerard et al., 1999; Goldson and Gerard, 2008). Conversely, the time available for larvae to locate suitable host plants before starvation would be reduced at higher soil temperatures, unless searching efficiency and burrowing speeds increased at higher temperatures (see Johnson et al., 2006). Soil pH affected egg hatching time but did not affect larval lifespan. In particular, there seemed to be a trend for shorter hatching periods in slightly acidic soil (pH 5). Studies concerning
Fig. 3. Larval lifespan of newly hatched and unfed S. lepidus larvae in response to soil temperature, soil pH and soil water content.
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the effect of pH on soil insects are scarce and often conflicting (Brown and Gange, 1990) and have focussed on larval stages rather than eggs in the soil. Exactly why acidic soils speed up S. lepidus egg hatching time is unclear, but it has been suggested that the egg chorion (hardened egg shell) of foliar insects can dissolve more easily under acidic conditions which eases the emergence of larvae (Helio¨vaara et al., 1992). Moreover, weak acids can act as sterilising agent which make insect eggs less susceptible to pathogens (e.g. Neuvonen et al., 1990). While soil temperature is probably the most important environmental factor to include in mathematical models for S. lepidus egg hatching and larval survival (Johnson et al., 2007b), other soil properties clearly have important effects. A significant conclusion of this study was that soil conditions (soil temperature, pH and water content) interact to affect egg hatching time. This is an important consideration for developing mathematical models, since existing models tend to only incorporate single environmental factors (usually soil temperature) if at all. Such considerations are likely to become more relevant in predictive models because of the effects of global climate change on soils (Anderson, 1992). In presenting these results, we hope to encourage soil ecologists to further investigate the complex and interacting effects of soil conditions on root-feeding insects to provide an empirical basis for future mathematical models. In turn, more accurate predictive models of egg hatching and larval lifespan could help to develop more integrated control strategies (e.g. targeted insecticide application) for some of the most significant insect pests in managed ecosystems (Blackshaw and Kerry, 2008). Acknowledgements The authors would like to thank Denise Headon of the North Wyke Research for collecting insects from the field, Dr Glyn Bengough, Dr Jane Wishart and two anonymous referees for their suggestions for improving this manuscript. This work was financially supported by the BBSRC (project 45/D14536). References Addison, P.J., Willoughby, B.E., Hardwick, S., Gerard, P.J., 1998. Clover root weevil: observations on differences between 1997 and 1998 summer populations in the Waikato. Proc. New Zeal. Plant Protection Conf. 51, 1–4. Anderson, J.M., 1992. Responses of soils to climate change. Adv. Ecol. Res. 22, 163– 210. Blackshaw, R.P., Kerry, B.R., 2008. Root herbivory in agricultural ecosystems. In: Johnson, S.N., Murray, P.J. (Eds.), Root Feeders—An Ecosystem Perspective. CABI, Wallingford, UK, pp. 35–53. Block, W., Turnock, W.J., Jones, T.H., 1987. Cold resistance and overwintering survival of the cabbage root fly, Delia radicum (Anthomyiidae), and its parasitoid, Trybliographa rapae (Cynipidae), in England. Oecologia 71, 332–338. Briones, M.J.I., Ineson, P., Piearce, T.G., 1997. Effects of climate change on soil fauna: responses of enchytraeids, Diptera larvae and tardigrades in a transplant experiment. Appl. Soil Ecol. 6, 117–134. Brown, V.K., Gange, A.C., 1990. Insect herbivory below ground. Adv. Ecol. Res. 20, 1– 58. Collier, R.H., Finch, S., Phelps, K., Thompson, A.R., 1991. Possible impact of global warming on cabbage root fly (Delia radicum) activity in the UK. Ann. Appl. Biol. 118, 261–271. Dowdy, W.W., 1944. The influence of temperature on vertical migration of invertebrates inhabiting different soil types. Ecology 25, 449–460. Gerard, P.J., Addison, P.J., Hardwick, S., Willoughby, B.E., 1999. Establishment of the invader: insights into the life history and biology of Sitona lepidus in the Waikato region of New Zealand. In: Proceedings of the Seventh Australasian Conference on Grassland and Invertebrate Ecology. pp. 43–51. Gerard, P.J., 2001. Dependence of Sitona lepidus (Coleoptera: Curculionidae) larvae on abundance of white clover Rhizobium nodules. B. Entomol. Res. 91, 149–152. Goldson, S.L., Rowarth, J.S., Caradus, J.R., 2005. The impact of invasive invertebrate pests in pastoral agriculture: a review. New Zeal. J. Agric. Res. 48, 401–415. Goldson, S.L., Gerard, P.J., 2008. Using biocontrol against root-feeding pests with particular reference to Sitona root weevils. In: Johnson, S.N., Murray, P.J. (Eds.), Root Feeders—An Ecosystem Perspective. CABI, Wallingford, UK, pp. 115–133.
79
Gregory, P.J., Johnson, S.N., Newton, A.C., Ingram, J.S.I., 2009. Integrating pests and pathogens into the climate change/food security debate. J. Exp. Bot. 60, 2827– 2838. Helio¨vaara, K., Va¨isa¨nen, R., Varama, M., 1992. Acidic precipitation increases egg survival in Neodiprion sertifer. Entomol. Exp. Appl. 62, 55–60. Hunter, M.D., 2001. Out of sight, out of mind: the impacts of root-feeding insects in natural and managed systems. Agr. Forest Entomol. 3, 3–9. Jarvis, R.A., 1968. Soils of the Reading district. Memoir of the Soil Survey of Great Britain—England & Wales. Harpenden, Herts, UK. Johnson, S.N., Gregory, P.J., Murray, P.J., Zhang, X., Young, I.M., 2004. Host plant recognition by the root-feeding clover weevil Sitona lepidus (Coleoptera: Curculionidae). B. Entomol. Res. 94, 433–439. Johnson, S.N., Gregory, P.J., Greenham, J.R., Zhang, X., Murray, P.J., 2005. Attractive properties of an isoflavonoid found in white clover root nodules on the clover root weevil. J. Chem. Ecol. 31, 2223–2229. Johnson, S.N., Zhang, X.X., Crawford, J.W., Gregory, P.J., Hix, N.J., Jarvis, S.J., Murray, P.J., Young, I.M., 2006. Effects of CO2 on the searching behaviour of the rootfeeding clover weevil. B. Entomol. Res. 96, 361–366. Johnson, S.N., Crawford, J.W., Gregory, P.J., Grinev, D.V., Mankin, R.W., Masters, G.J., Murray, P.J., Wall, D.H., Zhang, X.X., 2007a. Non-invasive techniques for investigating and modelling root-feeding insects in managed and natural systems. Agric. Forest Entomol. 9, 39–46. Johnson, S.N., Zhang, X., Crawford, J.W., Gregory, P.J., Young, I.M., 2007b. Egg hatching and survival time of soil-dwelling insect larvae: a partial differential equation model and experimental validation. Ecol. Model. 202, 493–502. Johnson, S.N., Murray, P.J. (Eds.), 2008. Root Feeders—An Ecosystem Perspective. CABI, Wallingford, UK. King, P.D., Mercer, C.F., Meekings, J.S., 1981. Ecology of black beetle, Heteronychus arator (Coleoptera Scarabaeidae)—influence of temperature on feeding, growth, and survival of the larvae. New Zeal. J. Zool. 8, 113–117. Krysan, J.L., 1976. Moisture relationships of the egg of the Southern corn rootworm Diabrotica undecimpunctata howardi (Coleoptera Chrysomelidae). Entomol. Exp. Appl. 20, 154–162. Lerin, J., 2004. Modeling embryonic development in Sitona lineatus (Coleoptera: Curculionidae) in fluctuating temperatures. Environ. Entomol. 33, 107–112. Lummus, P.F., Smith, J.C., Powell, N.L., 1983. Soil moisture and texture effects on survival of immature Southern corn rootworms, Diabrotica undecimpunctata howardi Barber (Coleoptera Chrysomelidae). Environ. Entomol. 12, 1529–1531. McCarthy, J.J., Canziani, O.F., Leary, N.A., Dokken, D.J., White, K.S., 2001. Hydrology and water resources. In: McCarthy, J.J., Canziani, O.F., Leary, N.A., Dokken, D.J., White, K.S. (Eds.), Climate Change 2001: Impacts, Adaptation and Vulnerability. Cambridge University Press, Cambridge, pp. 191–234. McCullagh, P., Nelder, J.A., 1989. Generalized Linear Models. Chapman & Hall, New York. Murray, P.J., Clements, R.O., 1994. Investigations of the host feeding preferences of Sitona weevils found commonly on white clover (Trifolium repens) in the UK. Entomol. Exp. Appl. 71, 73–79. Murray, P.J., Clements, R.O., 1998. Transfer of nitrogen between clover and wheat: effect of root herbivory. Eur. J. Soil Biol. 34, 25–30. Neuvonen, S., Saikkonen, K., Haukioja, E., 1990. Simulated acid rain reduces the susceptibility of the European pine sawfly (Neodiprion sertifer) to its nuclear polyhedrosis virus. Oecologia 83, 209–212. Pacchioli, M.A., Hower, A.A., 2004. Soil and moisture effects on the dynamics of early instar clover root curculio (Coleoptera: Curculionidae) and biomass of alfalfa root nodules. Environ. Entomol. 33, 119–127. Payne, D., Gregory, P.J., 1988. The temperature of the soil. In: Wild, A. (Ed.), Russell’s Soil Conditions and Plant Growth. Longman, Harlow, UK, pp. 282–297. Potter, D.A., 1983. Effect of soil moisture on oviposition, water absorption, and survival of Southern masked chafer (Coleoptera, Scarabaeidae) eggs. Environ. Entomol. 12, 1223–1227. Rowell, D.L., 1988. Soil acidity and alkalinity. In: Wild, A. (Ed.), Russell’s Soil Conditions and Plant Growth. Longman, Harlow, UK, pp. 844–898. Rowell, D.L., 1994. Soil Science: Methods And Applications. Longman, Harlow, UK. Schaafsma, A.W., Fuentes, J.D., Gillespie, T.J., Whitfield, G.H., Ellis, C.R., 1993. Performance of a model for egg hatching of the Western corn rootworm Diabrotica virgifera virgifera Le Conte, using measured and modeled soil temperatures as input. Int. J. Biometeorol. 37, 11–18. Son, Y., Lewis, E.E., 2005. Modelling temperature-dependent development and survival of Otiorhynchus sulcatus (Coleoptera: Curculionidae). Agric. Forest Entomol. 7, 201–209. Staley, J.T., Hodgson, C.J., Mortimer, S.R., Morecroft, M.D., Masters, G.J., Brown, V.K., Taylor, M.E., 2007. Effects of summer rainfall manipulations on the abundance and vertical distribution of herbivorous soil macro-invertebrates. Eur. J. Soil Biol. 43, 189–198. Staley, J.T., Johnson, S.N., 2008. Climate change impacts on root herbivores. In: Johnson, S.N., Murray, P.J. (Eds.), Root Feeders—An Ecosystem Perspective. CABI, Wallingford, UK, pp. 192–213. Villani, M.G., Wright, R.J., 1990. Environmental influences on soil macroarthropod behavior in agricultural systems. Annu. Rev. Entomol. 35, 249–269. Wang, G.L., 2005. Agricultural drought in a future climate: results from 15 global climate models participating in the IPCC 4th assessment. Clim. Dynam. 25, 739– 753. Zhang, X., Johnson, S.N., Gregory, P.J., Crawford, J.W., Young, I.M., Murray, P.J., Jarvis, S.C., 2006. Modelling the movement and survival of the root-feeding clover weevil, Sitona lepidus, in the root-zone of white clover. Ecol. Model. 190, 133– 146.