The mechanosensory lateral line system is a structurally diverse sensory system present in all fishes that is responsible for detection of water flow (hydrodynamic) stimuli and is of critical importance in a variety of behavioral contexts. It is composed of sensory organs located on the skin and in bony lateral line canals that are contained in a subset of bones in the skull. One of the four types of canals, widened canals, are quite sensitive to hydrodynamic stimuli and is considered to be an adaptation for the non-visual detection of prey, which is of great ecological importance for fishes. Two genera of Lake Malawi (Africa) cichlid fishes (Aulonocara [widened canals], and Tramitichromis [narrow canals]), will be used for a study that uses comparative anatomical, developmental and behavioral approaches to address fundamental issues in fish sensory biology. First, the convergent evolution of widened canals will be assessed among cichlids and among fishes more generally to more precisely define common features of its anatomy. Second, the pattern and timing of development of widened and narrow canals and the sensory organs contained within them will be analyzed quantitatively to determine the developmental basis for evolutionary change in the lateral line canal system. Finally, the role of widened canals in the detection of sand-dwelling prey will be analyzed using a behavioral assay and video analysis. This work will have important implications for our understanding of the evolution of feeding habits of cichlids in the African Rift Lakes, and of marine and freshwater fishes that feed on benthic prey, especially those in disturbed habitats in which non-visual predators may have an ecological advantage. The PI will integrate research and education by involving undergraduates and graduate students in all aspects of this project. Collaborations with colleagues (re: genetics, biomechanical modeling, microCT imaging, design of stimulus delivery apparatus), will enhance the interdisciplinary nature of the PI's research program and provide new training opportunities for students. This funding will enhance research infrastructure in Rhode Island, an EPSCoR state with a research focus in marine life sciences.
Humans are intimately familiar with the five senses (vision, hearing, smell, taste, touch), but fishes (30,000+ species, from sharks to minnows and tunas) also have the ability to detect water flows with the mechanosensory lateral line system. The neuromast receptor organs of the lateral line system are composed of hair cells, like those of the inner ear, and are found within pored canals and on the skin on the head and on the body. Most often thought of as visual predators, many fishes also use their lateral line system to detect prey, which appears to be critical for species in deep water habitats or in dim light or darkness. This project used closely-related cichlid fishes from Lake Malawi, Africa (Aulonocara stuartgranti, Tramitichromis sp.) that are easily maintained and reared in the laboratory (Fig. 1). It asked fundamental questions about the comparative anatomy, development, and behavioral role of two types of lateral line systems (Fig. 2) - one typical of fishes (narrow canals, Tramitichromis) and one that evolved convergently in fishes that live in deep water or are active in low light conditions (widened canals, Aulonocara). Traditional anatomical methods, microCT imaging (Fig. 2), scanning electron microscopy (Fig. 3) and fluorescent imaging (Fig. 4), were used to contrast the morphology and development of narrow and widened canal systems for the first time. This study showed how a quantitative comparison of development can explain how widened canals evolved in Aulonocara. It also revealed an unappreciated degree of diversity among neuromast receptor organs within an individual and how they develop over time. These discoveries will have important implications for the ways in which fishes are able to successfully respond to behaviorally signficant water flows through their life history. Behavioral studies were used to test the hypothesis that the evolution of widened canals represents an adaptation for prey detection. Aulonocara and Tramitichromis were presented with prey (live and dead tethered adult brine shrimp, Fig. 5) as proxies for the prey that they detect in sandy substrates in nature. Video analysis under light and dark conditions, and in fishes with a functional or inactivated lateral line system (treatment with cobalt chloride), revealed that Tramitichromis is a visual predator, but that Aulonocara uses its lateral line system to detect prey, especially in the dark. To clarify the role of the lateral line system in the absence visual cues, aartificial flow stimuli were presented to Aulonocara using a pump and a series of tubes under the sand, and fish were trained (with food reward) to detect flows. Aulonocara detected flows with their lateral line system, and responded with biting behaviors. Another experiment demonstrated how flow detection behavior was eliminated by inactivating the neuromasts (with cobalt chloride), but that behavior returned within a week, thus demonstrating the link between cell level function (hair cells) with behavior. The relative contribution of the lateral line system to detection of prey in sandy sediments has important implications for the ecology of fishes dependent on benthic (bottom) habitats, and may explain how species that feed on the same benthic prey resource can co-exist in the same habitat. The work carried out has Broader Impacts re: integration of research and education, dissemination, broadening participation, and impacts on science and society. The PI taught five different Biology courses and gave lectures in Deep Sea Biology, Biomimetics (biology-inspired engineering design) and Marine Bioacoustics, all of which incorporated research outcomes. Undergraduates trained in the lab majoredin Biology, Computer Science, and Engineering. We gave lab tours to K-12 groups and public stakeholders, participated in on-campus science open houses, and the PI participated in a science immersion workshop for journalists. The PI gave 10 invited talks at other institutions and 2 invited/keynote talks at national and international conferences; members of the lab gave 20 conference papers. A post-doc (now a faculty member) and three graduate students (all women) were trained, and 16 undergraduates (mostly women) worked in the lab, including 9 who did research and were co-authors on publications and/or conference presentations. Four undergraduates are now in graduate school (one, a Rhode Island native, is a member of an underrepresented group and is now a PhD student), five are working (Engineering, NOAA), and one is in veterinary school. We established µCT as a tool for the quantification of lateral line anatomy, and interactions with colleagues in Biomechanics and Ocean Engineering will generate new collaborations. Our work has made important contributions in anatomy, development and behavior, and to the conceptual interactions among them. It has also made important contributions to our understanding of the relationship of development and evolution, the interaction of vision and lateral line in the formulation of critical behaviors, and the role of sensory biology in fish ecology, especially where fishes are threatened with changes in the sensory environment due to environmental degradation and/or climate change.
