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Sexual Signalling and Noise Pollution in the Sea

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Sexual Signalling and Noise Pollution in the Sea Sexual signalling and noise pollution in the sea - Implications for courtship behaviour and reproductive success in two vocal species of gobies Eva-Lotta Blom Department of Biological and Environmental Sciences The Faculty of Science University of Gothenburg 2017 This doctoral thesis in Natural Sciences, specialising in Biology, is authorised by the Faculty of Science and will be publicly defended at 10:00 am on Friday the 15th of September, 2017, at the Department of Biological and Environmental Sciences, Medicinaregatan 18A, Gothenburg, Sweden. The opponent is Professor Andrew Radford. Professor of Behavioural Ecology, School of Biological Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, United Kingdom. Sexual signalling and noise pollution in the sea - Implications for courtship behaviour and reproductive success in two vocal species of gobies Eva-Lotta Blom Department of Biological and Environmental Sciences University of Gothenburg Box 463, SE-405-30 Gothenburg SWEDEN E-mail: [email protected] E-mail: [email protected] Copyright © Eva-Lotta Blom 2017 Published papers and respective figures in this thesis are reprinted with permission from the respective journals: Paper I – Environmental Biology of Fishes Paper II – PLOS ONE ISBN: 978-91-629-0248-3 (PDF) ISBN: 978-91-629-0249-0 (Print) Electronic version: Cover illustration: Eira och Malte Ekelin Printed by Ineko, Kållered, Sweden, 2017 DISSERTATION ABSTRACT Many marine animals use acoustic signals to mediate social interactions. Acoustic cues and signals are especially important in water because sound is unique as a sensory modality propagating with little attenuation over long distances, at all depths, and irrespective of the water current direction. Anthropogenic underwater noise is a global pollutant of increasing concern but its impact on reproduction in fish is largely unknown. Hence, a better understanding of this important link to fitness is crucial. Here, I compared different courtship traits, including courtship sounds, in two sympatric Pomatoschistus species and I found that courting males of the common goby Pomatoschistus microps sing louder and produce sounds of shorter duration than males of the sand goby Pomatoschistus minutus. Furthermore, eyes of P. minutus females turn black during courtship attempts, whereas this is not the case for females of P. microps. Dark eyes in females of P. minutus were more likely to be displayed by more gravid females, but males did not respond behaviourally or preferred dark-eyed females. I suggest that dark eyes are not a signal per se but may be an aspect of female mate choice, possibly related to vision. Furthermore, I examined if an experimentally altered body condition in P. minutus males affects acoustic and visual display and if it influences females’ decision to spawn or not. Visual and acoustic courtship and reproductive success was studied under two experimental food regimes (high food and low food) and compared to a control group (fish from the field). Condition did not affect visual or acoustic courtship, nor did it affect mating success. Females only spawned with males that produced sound and courtship sounds are likely to be important in female mate choice. To further understand how anthropogenic noise can affect mating success by masking the acoustic cue, I experimentally tested the impact of broadband noise exposure on the behaviour and reproductive success of P. microps. Noise treatment had similar frequency range as anthropogenic boat noise and was presented either continuously or intermittently. The continuous noise treatment had the most detrimental effect by reducing spawning probability, whereas male nest-building behaviour and active pre-spawning behaviour (including courtship) were unaffected. Additionally, females took longer to spawn under continuous noise than in the control. Egg density was significantly higher in both noise treatments compared to the control. Since sexual selection can be sensitive to changes in the environment I also investigated effects of noise on male mating success in P. minutus. I compared no added noise (‘silence’) to added artificial Brownian noise to create disturbance at moderate levels. In silent condition, successful males were significantly larger than unsuccessful males, which was not the case in the noise treatment. More males received eggs in the silent treatment compared to the noise treatment, creating a relaxed opportunity for sexual selection in the silent environment. However, here was no significant effect of treatment on the number of spawned eggs. The results suggest that disturbance caused by noise can influence mating decisions and traits under sexual selection. In conclusion, in this thesis I show that noise, particularly a continuous noise exposure, negatively affects reproductive success, highlighting its potential to impact fish demography. Future studies in natural conditions are required for a better understanding of the impact of noise on fish reproduction. Thus, I suggest that aquaria studies should be performed in a low noise environments, since noise clearly can affect the outcome of an experimental result. ii LIST OF PAPERS This thesis is based on the following papers, which are referred to in the text by their Roman numerals: Paper I: E-L. Blom, I. Mück, K. Heubel and O. Svensson Courtship sound and associated behaviours of two sympatric marine Gobiidae species – Pomatoschistus microps and Pomatoschistus minutus. Environmental Biology of Fish (2016) 99: 999–1007. Paper II: K. H Olsson, S. Johansson, E-L. Blom, K. Lindström, O. Svensson, H. Nilsson Sköld and C. Kvarnemo Dark eyes in female sand gobies indicate readiness to spawn. PLoS One, (2017) 12: e0177714. Paper III: E-L. Blom, J. Wilson, K. de Jong, C. Kvarnemo, T. Johansson, M.C.P. Amorim and O. Svensson. Acoustic display is an important cue for mate choice for females of Pomatoschistus minutus, but acoustic display is not affected by male condition. Manuscript Paper IV: E-L. Blom, C. Kvarnemo, S. Schöld, M. H. Andersson, O. Svensson and M. C. P. Amorim Continuous and intermittent noise has a negative impact on reproductive success in a marine fish with paternal care. Revised version re-submitted to Scientific Reports Paper V: K. de Jong, E-L. Blom, M. Nygård, M. H. Andersson, C. Kvarnemo and O. Svensson Disturbance caused by noise affects sexual selection in a marine fish. Manuscript iii Table of Contents DISSERTATION ABSTRACT ..................................................... ii LIST OF PAPERS ......................................................................... iii INTRODUCTION ........................................................................... 1 Sexual selection and Sexual signalling ........................................... 1 Cues and signals .............................................................................. 2 Visual displays ................................................................................ 3 Vocal displays ................................................................................. 3 Vocal signal interference ................................................................ 4 Sound in the sea ................................................................................ 6 Anthropogenic sound sources, their characteristics and effects ..... 6 Biological responses to anthropogenic noise .................................. 7 Continuous noise vs. intermittent noise .......................................... 8 AIMS ................................................................................................. 9 METHODS ..................................................................................... 10 Study species ................................................................................. 10 Study site and husbandry .............................................................. 10 Experimental setups ...................................................................... 11 Treatments ..................................................................................... 11 Food regimes ................................................................................. 12 Noise ............................................................................................. 12 Sound recordings and Sound analyses .......................................... 12 Lipid analysis ................................................................................ 14 Behavioural recordings and analysis ............................................ 14 RESULTS AND DISCUSSION .................................................... 15 Male visual courtship behaviour ................................................... 15 Female visual courtship behaviour ............................................... 15 Acoustic courtship ........................................................................ 18 Acoustic display is important in female mate choice ................... 21 Noise affects sexual selection ....................................................... 21 Noise effect on hatching ............................................................... 22 CONCLUSIONS ............................................................................ 25 Acknowledgements ........................................................................ 27 References ....................................................................................... 32 iv v INTRODUCTION In this thesis, I investigate the spawning behaviour
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