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Is the Well-Trodden Path Always the Correct Path? New Insights Into the Role of Footprint Hydrocarbons During Ant Foraging

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Is the Well-Trodden Path Always the Correct Path? New Insights Into the Role of Footprint Hydrocarbons During Ant Foraging Is the well-trodden path always the correct path? New insights into the role of footprint hydrocarbons during ant foraging. Phillip Buckham-Bonnett MSc (by research) The University of York Department of Biology March 2013 Abstract Positive feedback and negative feedback are crucial mechanisms in the regulation of biological systems and whilst the role of positive feedback has been well studied in social insect networks, the role of negative feedback has not. This thesis presents evidence of a novel negative feedback mechanism at work during foraging by the ant Lasius niger. In a foraging context, cuticular hydrocarbons, passively deposited on substrate by ants as they walk, can act as a repellent cue. This effect can be measured through branch selection by foraging workers at a trail bifurcation. Evidence from both a highly controlled experimental set up and a more natural foraging context are provided to support this claim. The possible role of this signal in ant foraging networks is considered and comparisons with other known negative feedback mechanisms in ant foraging networks are drawn. Experiments with the ant Monomorium pharaonis were unable to show negative feedback signals being used to optimise food search tactics and this finding is evaluated in relation to the ecology of M. pharaonis. Circumstantial evidence is also presented in support of the hypothesis that L. niger workers can use alarm pheromones to recruit nest mates to unexplored territory. The need for further work testing this hypothesis is highlighted. The communication role of ant interactions during foraging is discussed and, based on new observations with L. niger workers, the position of the signaller relative to the recipient during the interaction is proposed as a possible component of the signalling mechanism. Further possible experiments based on both empirical observations and computational models are proposed to help augment the findings presented in this study. - 2 - Contents Page Figures 6 Tables 7 Acknowledgements 8 Declaration 8 Chapter 1 – Introduction 9 1.1 Negative and Positive Feedback in Biological Systems 9 1.2 The Use of Positive Feedback Mechanisms During Foraging by Social Insects 9 1.2.1 Recruitment to Food by Social Insects (Other than Ants) 9 1.2.2 Mass Recruitment to Food by Ants 10 1.3 The Use of Negative Feedback Mechanisms During Foraging by Insects 11 1.3.1 Ants 11 1.3.2 Other Social Insects 12 1.3.3 Non-social insects 13 1.4 The Remit of this study 13 1.4.1 Research Question 13 1.4.2 Study Species 13 Chapter 2 – General Materials and Methods 15 2.1 Ant Husbandry 15 2.1.1 Pharaoh’s Ant 15 2.1.2 Black Garden Ant 16 2.2 Apparatus 17 2.3 Statistical methods 19 Chapter 3 – When searching for food do workers of the Pharaoh’s ant leave a repellent 20 signal to help nestmates avoid researching unrewarding areas? 3.1 Ecological context of experiments. 20 3.2 Set up for experiments 20 3.3 Experiment M1- Does the passage of workers over unmarked substrate result in a 21 chemical deposit that subsequent workers avoid? 3.3.1 Methods: Set up Phase 21 3.3.2 Methods: Test Phase 22 3.3.3 Methods: Analysis 22 3.4 Experiment M2 - Does the passage of workers over home range marked substrate 23 result in a chemical deposit that subsequent workers avoid? 3.4.1 Protocol 23 3.5 Results from Experiment M1 - Does the passage of workers over unmarked 23 substrate result in a chemical deposit that subsequent workers avoid? 3.6 Results from Experiment M2 - Does the passage of workers over home range 24 marked substrate result in a chemical deposit that subsequent workers avoid? 3.7 Discussion of Monomorium Results 25 - 3 - Chapter 4 – Does the passage of Lasius niger over unmarked substrate in either the 27 presence or absence of trail pheromone result in a chemical deposit that subsequent workers avoid, and if so, can the likely identity of this chemical be determined? 4.1 Ecological context of experiments 27 4.2.1 General techniques for use in Lasius experiments. 27 4.2.1.1 General techniques (set up phase) 27 4.2.1.2 General Techniques (test phase). 29 4.2.1.3 Replicates 30 4.2.2 Experiment L1 - Do exploring workers prefer unmarked substrate, or substrate 30 previously crossed by 20 workers? 4.2.3 Experiment L2 - Do naive workers following a pheromone trail prefer a branch 32 previously walked over by twenty unfed ants or a branch previously walked over by no ants? 4.2.4 Experiment L3 - Can a decay of the effect of the signal that was observed in 33 experiment L2 be detected? 4.2.5 Experiment L4 - Is the effect observed in experiment L2 a result of paper crossed 34 by unfed ants being repellent, or a result of unmarked paper being attractive? 4.2.6 Experiment L5 - Can the effect observed in experiment L1 be explained by the 35 presence of footprint hydrocarbons deposited by the twenty ants during the set up phase? 4.2.7 Experiment L6 - Can the effect observed in experiment L2 be explained by the 36 presence of footprint hydrocarbons deposited by the twenty ants during the set up phase? 4.2.8 Summary of the main differences between experiments 37 4.3 Results 37 4.3.1 Experiment L1 - Do exploring workers prefer unmarked substrate, or substrate 37 previously crossed by twenty workers? 4.3.2 Experiment L2 - Do naive workers following a pheromone trail prefer a branch 37 previously walked over by twenty unfed ants or a branch previously walked over by no ants? 4.3.3 Experiment L3 - Can a decay of the effect of the signal that was observed in 37 experiment L2 be detected? 4.3.4 Experiment L4 - Is the effect observed in experiment L2 a result of paper crossed 37 by unfed ants being repellent, or a result of unmarked paper being attractive? 4.3.5 Experiment L5 - Can the effect observed in experiment L1 be explained by the 38 presence of footprint hydrocarbons deposited by the twenty ants during the set up phase? 4.3.6 Experiment L6 - Can the effect observed in experiment L2 be explained by the 38 presence of footprint hydrocarbons deposited by the twenty ants during the set up phase? 4.4 Discussion 39 4.4.1 Evidence for negative chemotaxis as a response to footprint hydrocarbons by 39 pheromone trail following workers. 4.4.2 Evidence for positive chemotaxis towards substrate recently explored by 40 nestmates. - 4 - Chapter 5 – the behaviour of ants on unmarked and home range marked substrate in the 42 presence or absence of trail pheromone. 5.1 General Introduction 42 5.2 Gaster Vibrations 42 5.3 Methods 43 5.3.1 Video Analysis 44 5.3.2 Statistical analysis 45 5.4 Results 45 5.5 Discussion 47 5.5.1 Was alarm pheromone a sensible hypothesis? 47 Chapter 6 – The combined role of trail pheromone and footprint hydrocarbons in a real 49 foraging context 6.1 Introduction 49 6.2 Method 49 6.3 Analysis 51 6.3.1 Analysis: The pheromone-only model 51 6.3.2 Analysis: The combined model 52 6.3.2.1 Estimating B 52 6.3.2.2 Estimating A 53 6.3.3 Comparing the pheromone only and combined models to experimental 54 observations 6.4 Discussion 55 6.4.1 Pheromone Only Model vs Combined model. 55 Chapter 7 – The communication role of interactions between workers during foraging 56 7.1 Introduction 56 7.2 Method 56 7.3 Results 57 7.4 Interaction mechanism 57 7.5 Discussion 58 Chapter 8 – Discussion 60 8.1 Summary of Findings 60 8.2 Discussion of findings and further work 61 8.2.1 Discussion and Further Work: The repellent role of footprint hydrocarbons during 61 foraging 8.2.2 Discussion and Further Work: Recruitment of workers to unmarked territory 63 8.2.3 Discussion and Further Work: The communication role of trail interactions during 63 foraging 8.3 The link between ecology and foraging strategy 63 8.4 Final note 64 Appendix 1 – further detail relating to the results presented in Chapter 3 65 1.1 Monomorium Experiment 1 65 1.2 Monomorium Experiment 2 65 - 5 - Appendix 2 - further detail relating to the results presented in Chapter 4 66 2.1 Experiment L1 - Do exploring workers prefer unmarked substrate, or substrate 66 previously crossed by 20 workers? 2.2 Experiment L2 - Do naive workers following a pheromone trail prefer a branch 67 previously walked over by twenty unfed ants or a branch previously walked over by no ants? 2.3 Experiment L3 - Can a decay of the effect of the signal that was observed in 68 experiment L2 be detected? 2.4 Experiment L4 - Is the effect observe in experiment L2 a result of paper crossed by 69 unfed ants being repellent, or a result of unmarked paper being attractive? 2.5 Experiment L5 - Can the effect observed in experiment L1 be explained by the 70 presence of footprint hydrocarbons deposited by the 20 ants during the set up phase? 2.6 Experiment L6 - Can the effect observed in experiment L2 be explained by the 70 presence of footprint hydrocarbons deposited by the 20 ants during the set up phase? Appendix 3 - further detail relating to the results presented in Chapter 5 71 3.1 Speed 71 3.2 Zigzags 71 3.3 Number of Stops 72 Appendix 4 - further detail relating to the results presented in Chapter 6 73 4.1 Sensitivity testing for combined model 73 4.2 Interactions 74 References 75 Figures Page Figure 1 - The trail pheromone (3,4- dihydro-8-hydroxy-3,5,7-trimethylisocoumarin) and 14 alarm pheromone (undecane) of Lasius niger.
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