Parasite or mutualist: the functional role of intracellular symbionts in shaping communities of agriculturally beneficial spiders

Gibbons, Alastair Tristan Russell (2020) Parasite or mutualist: the functional role of intracellular symbionts in shaping communities of agriculturally beneficial spiders. PhD thesis, University of Nottingham.

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By the year 2050 the world's population is expected to grow to almost 10 billion. In order to meet future food demands a transformative change, at the global scale, in agricultural and food systems is required. Yet, the current trend for the overall growth of yields has slowed. Productivity has been hampered by the degradation of natural resources as well as the spread of pests and disease, including those that are developing resistance to agro-chemicals. In addition, the biodiversity decline, fuelled by intensive monocultures, uniform habitats and the excessive use of agro-chemicals is one of the greatest challenges society faces, and what is concurrent in the literature, is that these practices are becoming increasingly unsustainable.

Spiders (order Araneae) are a group of beneficial arthropods that persist in agricultural systems throughout the year. They are ubiquitous, generalist predators of invertebrates capable of suppressing and maintaining insect pests below economically damaging levels. In the future, enhancing the efficacy of biological control is essential and is nowadays considered an economically valuable ecosystem service. In conjunction, it is well established that spiders harbour a range of intracellular bacterial symbionts, also referred to as endosymbionts. Wolbachia, Rickettsia, Spiroplasma and Cardinium are maternally inherited endosymbionts commonly found in arthropods, and have a profound influence on host life history, physiology, behavioural traits and ultimately fitness. Yet in spiders, the main focus of studies are limited to their distribution as well as rate of infection, and not, their consequences.

The primary aim of this thesis is to determine the functional role that endosymbionts have on survival and important behaviours associated with biological control, on hosts found within European agricultural systems. To investigate this, this thesis consists of four studies. First, drivers of spider abundance in arable wheat fields were examined by investigating local and landscape factors. Then, the distribution and frequency of endosymbiont infection was monitored over the period of a year in three spider families: Lycosidae: species of Pardosa, Clubionidae: species of Clubiona and Linyphiidae: Erigone atra. It was found that local factors were more important than landscape factors in determining spider abundance and endosymbiont infection varied among families, seasons and habitats.

Second, the functional role of endosymbiont infection was investigated in Philodromus cespitum. Important behaviours associated with the biological control of pests were measured and then individuals were examined for endosymbiont infection. Spiders infected with strains of Wolbachia were more active but those infected with strains of Cardinium had a lower capture rate in comparison to those uninfected. In the third experiment the importance of these behaviours and endosymbiont infection were studied in the context of diet, or the trophic niche. Foraging aggressiveness was a particularly prominent trait, and individuals that scored highly were more likely to capture prey, capture more difficult prey and engage in superfluous killing. Cardinium infection altered the trophic niche, as infected individuals consumed fewer collembolans.

In arthropods, there are conflicting studies which show endosymbiont infection either increases the susceptibility of the host to insecticides or confers protection. In the fourth experiment, Phylonetta impressa were exposed to one of four neonicotinoids and differences in mortality and behaviour were recorded. Then, spiders were examined for the presence of endosymbionts. Spiders exposed to imidacloprid and thiacloprid showed the most adverse effects in comparison to thiamethoxam, acetamiprid or the control. Furthermore spiders infected with bacterial endosymbionts were able to survive treatment with the neonicotinoid insecticides, imidacloprid and thiacloprid, better than those that were uninfected. Infection with the endosymbiont Cardinium was the most prevalent in this study, and when analysed independently, showed that Cardinium-infected individuals survived neonicotinoid treatment better than those that were uninfected.

Results from these studies suggest that the biology and evolution of many arthropod species cannot be fully understood, without also considering their endosymbionts. They are ubiquitous throughout arthropod taxa with varying frequencies but these studies show that infection has the potential to impact the host, in a way which may have consequences downstream. Different species, especially Cardinium, are associated with a variety of functions, and future studies should elucidate further behavioural, physiological and even reproductive manipulations induced by endosymbionts on arachnid hosts. Furthermore, it is important to understand to what degree endosymbionts can impact important traits, such as those in biological control. From a practical perspective, endosymbionts have been used to control a variety of pest species but their role in generalist predators is not well understood.

Item Type: Thesis (University of Nottingham only) (PhD)
Supervisors: Goodacre, S.L.
Majerus, T.O.
Keywords: spider, Araneae, symbiosis, endosymbiont, symbiont, Wolbachia, Cardinium, trophic niche, behaviour, agricultural systems
Subjects: Q Science > QL Zoology
Faculties/Schools: UK Campuses > Faculty of Medicine and Health Sciences > School of Life Sciences
Item ID: 59695
Depositing User: Gibbons, Alastair
Date Deposited: 17 Jul 2020 04:40
Last Modified: 17 Jul 2022 04:30

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