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Functional Diversity of the Lateral Line System Among Populations of a Native Australian Freshwater Fish Lindsey Spiller1, Pauline F

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Functional Diversity of the Lateral Line System Among Populations of a Native Australian Freshwater Fish Lindsey Spiller1, Pauline F © 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 2265-2276 doi:10.1242/jeb.151530 RESEARCH ARTICLE Functional diversity of the lateral line system among populations of a native Australian freshwater fish Lindsey Spiller1, Pauline F. Grierson1, Peter M. Davies2, Jan Hemmi1,3, Shaun P. Collin1,3 and Jennifer L. Kelley1,* ABSTRACT Montgomery, 1999b; Bleckmann and Zelick, 2009; Montgomery Fishes use their mechanoreceptive lateral line system to sense et al., 1997). Correspondingly, ecological variables such as nearby objects by detecting slight fluctuations in hydrodynamic predation pressure (McHenry et al., 2009), habitat (Beckmann motion within their immediate environment. Species of fish from et al., 2010; Vanderpham et al., 2013) and water velocity (Wark and different habitats often display specialisations of the lateral line Peichel, 2010) may partly explain the diversity in lateral line system, in particular the distribution and abundance of neuromasts, morphology that is often observed in species occupying different but the lateral line can also exhibit considerable diversity within a habitats. species. Here, we provide the first investigation of the lateral line The functional link between lateral line morphology, habitat system of the Australian western rainbowfish (Melanotaenia variation and behaviour remains very poorly understood. For australis), a species that occupies a diversity of freshwater habitats example, while it is clear that the lateral line is used by larval across semi-arid northwest Australia. We collected 155 individuals zebrafish to respond to suction-feeding predators (McHenry et al., from eight populations and surveyed each habitat for environmental 2009), only one study has shown that exposure to environmental factors that may contribute to lateral line specialisation, including cues, such as predation risk, can affect the development of the lateral water flow, predation risk, habitat structure and prey availability. line system in fishes (Fischer et al., 2013). Interestingly, it has ’ Scanning electron microscopy and fluorescent dye labelling were recently been revealed that variation in an individual s lateral line used to describe the lateral line system in M. australis, and to examine morphology can determine the intensity of the rheotactic response whether the abundance and arrangement of superficial neuromasts (Jiang et al., 2017). Nonetheless, with the exception of the (SNs) varied within and among populations. We found that the SNs of abovementioned studies, we understand surprisingly little about M. australis were present in distinct body regions rather than lines. the relationship between lateral line diversity and the ecology and The abundance of SNs within each body region was highly variable, behaviour of fishes. and also differed among populations and individuals. Variation in SN The lateral line system comprises a series of bundles of hair cells abundance among populations was best explained by habitat (neuromasts) that extend over the head and the lateral flank of fishes structure and the availability of invertebrate prey. Our finding that (Carton and Montgomery, 2004; Webb, 1989; Wellenreuther et al., specific environmental factors explain among-population variation in 2010). These neuromasts comprise two distinct types, superficial a key sensory system suggests that the ability to acquire sensory neuromasts (SNs) and canal neuromasts (CNs), which differ in their information is specialised for the particular behavioural needs of the performance and function despite similarities in basic structure. SNs animal. are located on the surface of the skin (Carton and Montgomery, 2004) and mostly function to sense the velocity of the surrounding KEY WORDS: Population variation, Altered flow regimes, Sensory water (Dijkgraaf, 1963). SNs are able to respond to flow that is not evolution, Adaptation orthogonal to their orientation axis, while the response amplitude of the CNs follows a cosine function and is maximised when water INTRODUCTION flow is in the direction of the canal axis (Janssen, 2004). SNs also Fishes possess a unique sensory organ, the lateral line system, which facilitate rheotaxis (body orientation into currents), as these cells are allows them to receive both physical and biological information constantly stimulated by water flow (Baker and Montgomery, about their environment (reviewed by Mogdans and Bleckmann, 1999a). The CNs, in contrast, usually occur in a distinct line at the 2012). The lateral line system forms the basis of many key survival base of a canal running and extending over the head and flank. The traits in fishes (Bleckmann and Zelick, 2009; Engelmann et al., CNs have a high threshold sensitivity (i.e. the minimum detectable 2002) and underlies many behavioural adaptations, including stimulus) over a broad frequency range (<1 to >100 Hz; van Netten predator avoidance (Montgomery and Macdonald, 1987), social and McHenry, 2013) and are therefore used for both the detection communication (Butler and Maruska, 2016; Partridge and Pitcher, and discrimination of objects, such as predators and prey in the 1980) and orientation to water flow or ‘rheotaxis’ (Baker and fishes’ local environment (Mogdans and Bleckmann, 2012). Thus, the discrete functional characteristics of these two neuromast types, 1School of Biological Sciences, The University of Western Australia, 35 Stirling coupled with their distributions across the body, can provide Highway, Crawley, Western Australia 6009, Australia. 2Centre of Excellence in valuable insights into the sensory requirements of a species Natural Resource Management, The University of Western Australia, Albany, occupying a particular habitat. Western Australia 6332, Australia. 3UWAOceans Institute, The University of Western Australia, 35 Stirling Highway, Crawley, Western Australia 6009, Australia. It has long been recognised that environmental factors such as water flow can result in the evolution of particular functional *Author for correspondence ([email protected]) morphologies of the lateral line system. For example, some studies J.L.K., 0000-0002-8223-7241 have found that limnophilic species that live in quieter, slower environments tend to have more SNs than rheophilic species that Received 17 October 2016; Accepted 6 April 2017 live in ‘noisier’, fast-paced environments (Bleckmann, 1994; Journal of Experimental Biology 2265 RESEARCH ARTICLE Journal of Experimental Biology (2017) 220, 2265-2276 doi:10.1242/jeb.151530 Coombs et al., 1988; Dijkgraaf, 1963; Engelmann et al., 2002; The diversity of freshwater habitats present in the Pilbara thus Jakubowski, 1967; Janssen, 2004; Teyke, 1990). However, other provides a unique opportunity to examine whether fish exhibit studies have reported no relationship between SN abundance and specialist adaptations of the lateral line system in response to water flow in the species’ habitat (e.g. Beckmann et al., 2010). It has extreme hydrological variability. recently become apparent that the lateral line system can exhibit Despite western rainbowfish being common throughout variation among populations and individuals of a single species. northwest Australia, there have been very few ecological studies Threespine sticklebacks (Gasterosteus aculeatus) inhabiting of this species, and its lateral line system has never been formally marine, stream and lake habitats show a similar arrangement of described. In this study, we first describe the morphology of the SNs, but fish inhabiting freshwater streams have a higher abundance lateral line system in the western rainbowfish, using a combination of SNs than those occupying marine habitats (Wark and Peichel, of scanning electron microscopy (SEM) and fluorescent labelling 2010). Such divergence in neuromast abundance among freshwater (DASPEI) and light microscopy. We captured adult rainbowfish (pond) and marine populations has also been reported in ninespine from eight locations across the Pilbara region (subject to available stickleback (Pungitius pungitius) (Trokovic et al., 2011). When freshwater habitat during the dry season), and quantified the comparing discrete ‘ecotypes’ of threespine sticklebacks, fish from abundance and distribution of neuromasts across the body using limnetic habitats had fewer neuromasts than those from benthic fluorescence microscopy. During our field surveys, we evaluated habitats, suggesting that habitat or resource specialisation may drive the habitat characteristics of each sample site, including the sensory adaptation (Wark and Peichel, 2010). Variation in predation abundance of surface and benthic invertebrates, water depth, flow pressure can also influence lateral line diversity; for example, rate, turbidity, predation risk and habitat complexity. We then guppies (Poecilia reticulata) inhabiting streams with high risk of adopted a modelling approach to evaluate the environmental predation have a greater abundance of SNs than those occurring in predictors (and their interactions) that best explained the observed low predation sites (Fischer et al., 2013). Species can also exhibit population variation in neuromast abundance. Several previous variation in the canal system of the lateral line; for example, studies have revealed a link between hydrodynamic variability and common bully (Gobiomorphus cotidianus) from rivers have more neuromast abundance (Carton and Montgomery, 2004; Dijkgraaf, canal pores on the head than those collected from lakes 1963; Engelmann
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