Rosemary S. Hails

Identification of 100 fundamental ecological questions

Summary 1. Fundamental ecological research is both intrinsically interesting and provides the basic knowledge required to answer applied questions of importance to the management of the natural world. The 100th anniversary of the British Ecological Society in 2013 is an opportune moment to reflect on the current status of ecology as a science and look forward to high-light priorities for future work.

Baculovirus resistance in the noctuid Spodoptera exempta is phenotypically plastic and responds to population density

Parasite resistance mechanisms can be costly to maintain. We would therefore predict that organisms should invest in resistance only when it is likely to be required. Insects that show density–dependent phase polyphenism, developing different phenotypes at high and low population densities, have the opportunity to match their levels of investment in resistance with the likelihood of exposure to pathogens. As high population densities often precipitate disease epidemics, the high–density form should be selected to invest relatively more in resistance. We tested this prediction in larvae of the noctuid Spodoptera exempta. Larvae reared at a high density were found to be considerably more resistant to a nuclear polyhedrosis virus than those reared in isolation. A conspicuous feature of the high–density phase of S. exempta and other phase–polyphenic Lepidoptera is cuticular melanization. As melanization is controlled by the phenoloxidase enzyme system, which is also involved in the immune response, this suggests a possible mechanism for increased resistance at high population densities. We demonstrated that melanized S. exempta larvae were more resistant than non–melanized forms, independent of rearing density. We also found that haemolymph phenoloxidase activity was correlated with cuticular melanization, providing further evidence for a link between melanization and immunity. These results suggest that pathogen resistance in S. exempta is phenotypically plastic, and that the melanized cuticles characteristic of the high–density form may be indicative of a more active immune system.

A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators

There is evidence that in Europe and North America many species of pollinators are in decline, both in abundance and distribution. Although there is a long list of potential causes of this decline, there is concern that neonicotinoid insecticides, in particular through their use as seed treatments are, at least in part, responsible. This paper describes a project that set out to summarize the natural science evidence base relevant to neonicotinoid insecticides and insect pollinators in as policy-neutral terms as possible. A series of evidence statements are listed and categorized according to the nature of the underlying information. The evidence summary forms the appendix to this paper and an annotated bibliography is provided in the electronic supplementary material.

A mathematical model of exposure of non- target Lepidoptera to Bt-maize pollen expressing Cry1Ab within Europe

Genetically modified (GM) maize MON810 expresses a Cry1Ab insecticidal protein, derived from Bacillus thuringiensis (Bt), toxic to lepidopteran target pests such as Ostrinia nubilalis. An environmental risk to non-target Lepidoptera from this GM crop is exposure to harmful amounts of Bt-containing pollen deposited on host plants in or near MON810 fields. An 11-parameter mathematical model analysed exposure of larvae of three non-target species: the butterflies Inachis io (L.), Vanessa atalanta (L.) and moth Plutella xylostella (L.), in 11 representative maize cultivation regions in four European countries. A mortality–dose relationship was integrated with a dose–distance relationship to estimate mortality both within the maize MON810 crop and within the field margin at varying distances from the crop edge. Mortality estimates were adjusted to allow for physical effects; the lack of temporal coincidence between the susceptible larval stage concerned and the period over which maize MON810 pollen is shed; and seven further parameters concerned with maize agronomy and host-plant ecology. Sublethal effects were estimated and allowance made for aggregated pollen deposition. Estimated environmental impact was low: in all regions, the calculated mortality rate for worst-case scenarios was less than one individual in every 1572 for the butterflies and one in 392 for the moth.

Challenges in modelling complexity of fungal entomopathogens in semi-natural populations of insects

The use of fungal entomopathogens as microbial control agents has driven studies into their ecology in crop ecosystems. Yet, there is still a lack of understanding of the ecology of these insect pathogens in semi-natural habitats and communities. We review the literature on prevalence of fungal entomopathogens in insect populations and highlight the difficulties in making such measurements. We then describe the theoretical host-pathogen models available to examine the role that fungal entomopathogens could play in regulating insect populations in semi-natural habitats, much of the inspiration for which has been drawn from managed systems, particularly forests. We further emphasise the need to consider the complexity, and particularly the heterogeneity, of semi-natural habitats within the context of theoretical models and as a framework for empirical studies. We acknowledge that fundamental gaps in understanding fungal entomopathogens from an ecological perspective coupled with a lack of empirical data to test theoretical predictions is impeding progress. There is an increasing need, especially under current rapid environmental change, to improve our understanding of the role of fungi in insect population dynamics beyond the context of forestry and agriculture.

Effects of phenotypic plasticity on pathogen transmission in the field in a Lepidoptera-NPV system

Abstract In models of insect–pathogen interactions, the transmission parameter (ν) is the term that describes the efficiency with which pathogens are transmitted between hosts. There are two components to the transmission parameter, namely the rate at which the host encounters pathogens (contact rate) and the rate at which contact between host and pathogen results in infection (host susceptibility). Here it is shown that in larvae of Spodoptera exempta (Lepidoptera: Noctuidae), in which rearing density triggers the expression of one of two alternative phenotypes, the high-density morph is associated with an increase in larval activity. This response is likely to result in an increase in the contact rate between hosts and pathogens. Rearing density is also known to affect susceptibility of S. exempta to pathogens, with the high-density morph showing increased resistance to a baculovirus. In order to determine whether density-dependent differences observed in the laboratory might affect transmission in the wild, a field trial was carried out to estimate the transmission parameter for S. exempta and its nuclear polyhedrosis virus (NPV). The transmission parameter was found to be significantly higher among larvae reared in isolation than among those reared in crowds. Models of insect–pathogen interactions, in which the transmission parameter is assumed to be constant, will therefore not fully describe the S. exempta-NPV system. The finding that crowding can influence transmission in this way has major implications for both the long-term population dynamics and the invasion dynamics of insect–pathogen systems.

Transmission Dynamics of a Virus in a Stage-Structured Insect Population

Despite the blossoming interest in host-microparasite epidemiology, and in use of viruses in the biological control of insect pests, few empirical studies have attempted to quantify transmission and mortality rates under field conditions. We report a laboratory and field study in which the transmission parameter (v) and mortality rate (Ux) due to nuclear polyhedrosis virus (NPV) are measured in different larval instars of the cabbage moth, Mamestra brassicae (Lepidoptera: Noctuidae). Laboratory studies of food consumption and virus susceptibility were used to produce crude estimates of relative transmission rates in successive instars. Increases in the rate of feeding outstrip increases in virus resistance with instar, so we predict that transmission rates should increase in older larvae (assuming rate of intake of virus to be proportional to rate of feeding). This prediction was tested in a field experiment in which a constant initial density of susceptible and infected (moribund) larvae were reared together on cabbage plants for 2-8 d. Estimates of the linear transmission parameter (v) did not differ between instars and gave a mean value of 2.16 X 10-12 for all instars and time points. Causes for the discrepancy between predictions based on laboratory data and field measurements are discussed. Differences were found between instars in the time from infection to death (T) (equivalent to 1/cV, where ax is the rate of mortality due to viral infection). Second-instar larvae died more rapidly once infected than third instars, which, in turn, died more rapidly than fourth instars. The effect of host population stage structure on patterns of viral infection can be pronounced and if recognized, may signifi- cantly increase the accuracy and predictive value of models of host pathogen systems.

Feral genetically modified herbicide tolerant oilseed rape from seed import spills: are concerns scientifically justified?

One of the concerns surrounding the import (for food and feed uses or processing) of genetically modified herbicide tolerant (GMHT) oilseed rape is that, through seed spillage, the herbicide tolerance (HT) trait will escape into agricultural or semi-natural habitats, causing environmental or economic problems. Based on these concerns, three EU countries have invoked national safeguard clauses to ban the marketing of specific GMHT oilseed rape events on their territory. However, the scientific basis for the environmental and economic concerns posed by feral GMHT oilseed rape resulting from seed import spills is debatable. While oilseed rape has characteristics such as secondary dormancy and small seed size that enable it to persist and be redistributed in the landscape, the presence of ferals is not in itself an environmental or economic problem. Crucially, feral oilseed rape has not become invasive outside cultivated and ruderal habitats, and HT traits are not likely to result in increased invasiveness. Feral GMHT oilseed rape has the potential to introduce HT traits to volunteer weeds in agricultural fields, but would only be amplified if the herbicides to which HT volunteers are tolerant were used routinely in the field. However, this worst-case scenario is most unlikely, as seed import spills are mostly confined to port areas. Economic concerns revolve around the potential for feral GMHT oilseed rape to contribute to GM admixtures in non-GM crops. Since feral plants derived from cultivation (as distinct from import) occur at too low a frequency to affect the coexistence threshold of 0.9% in the EU, it can be concluded that feral GMHT plants resulting from seed import spills will have little relevance as a potential source of pollen or seed for GM admixture. This paper concludes that feral oilseed rape in Europe should not be routinely managed, and certainly not in semi-natural habitats, as the benefits of such action would not outweigh the negative effects of management.

Prey selection and baculovirus dissemination by carabid predators of Lepidoptera

Abstract. 1 The interaction between coleopteran predators and baculovirus‐infected larvae was studied in the laboratory and the field in order to assess the potential role of predators in the dissemination of a nucleopolyhedrovirus (NPV). 2 Preference tests using three carabid species, Harpalus rufipes De Geer, Pterostichus melanarius Illiger and Agonum dorsale Pont, showed no evidence of discrimination between healthy and diseased larvae of the cabbage moth Mamestra brassicae L. (Lepidoptera: Noctuidae) as prey items. 3 Virus infectivity was maintained after passage through the predators gut. NPV mortality ranged from 97% to 20% when test larvae were exposed to faeces collected immediately after and 15 days post‐infected meal respectively. 4 The potential for transfer of inoculum in the environment was estimated in the laboratory by soil bioassay. Carabids continuously passed infective virus to the soil for at least 15 days after feeding on infected larvae. 5 Field experiments showed that carabids which had previously fed on diseased larvae transferred sufficient virus to the soil to cause low levels of mortality in larval populations of the cabbage moth at different instars.

Behavior of a recombinant baculovirus in lepidopteran hosts with different susceptibilities.

ABSTRACT Insect pathogens, such as baculoviruses, that are used as microbial insecticides have been genetically modified to increase their speed of action. Nontarget species will often be exposed to these pathogens, and it is important to know the consequences of infection in hosts across the whole spectrum of susceptibility. Two key parameters, speed of kill and pathogen yield, are compared here for two baculoviruses, a wild-type Autographa californica nucleopolyhedrovirus (AcNPV), AcNPV clone C6, and a genetically modified AcNPV which expresses an insect-selective toxin, AcNPV-ST3, for two lepidopteran hosts which differ in susceptibility. The pathogenicity of the two viruses was equal in the less-susceptible host, Mamestra brassicae, but the recombinant was more pathogenic than the wild-type virus in the susceptible species, Trichoplusia ni. Both viruses took longer to kill the larvae of M. brassicae than to kill those of T. ni. However, whereas the larvae of T. ni were killed more quickly by the recombinant virus, the reverse was found to be true for the larvae ofM. brassicae. Both viruses produced a greater yield inM. brassicae, and the yield of the recombinant was significantly lower than that of the wild type in both species. The virus yield increased linearly with the time taken for the insects to die. However, despite the more rapid speed of kill of the wild-type AcNPV in M. brassicae, the yield was significantly lower for the recombinant virus at any given time to death. A lower yield for the recombinant virus could be the result of a reduction in replication rate. This was investigated by comparing determinations of the virus yield per unit of weight of insect cadaver. The response of the two species (to both viruses) was very different: the yield per unit of weight decreased over time for M. brassicae but increased for T. ni. The implications of these data for risk assessment of wild-type and genetically modified baculoviruses are discussed.