Development and Evolution of the Lateral Line System in Cichlid Fishes

(Funded by NSF Grant IOS-0843307, RI NSF EPSCoR, and URI’s College of the Environment and Life Sciences)

We have been studying the lateral line system of cichlid fishes for many years. Early work described the morphology and post-embryonic development of the lateral line system in tilapia and convict cichlid (Webb 1989, 1990; Tarby and Webb, 1993). In the past 10 years, we have been using cichlids as a model system to explore modularity and integration of the lateral line canals in the dermatocranium, and the behavioral role of the lateral line system in fishes with widened lateral line canals (NSF Grant IOS-0843307).

There are five cranial lateral line canal phenotypes found among bony fishes. Widened canals are known to be more sensitive than narrow canals to hydrodynamic stimuli and are considered to be an adaptation for the non-visual detection of prey.  However, species that have widened canals and are suitable for laboratory studies are rare. We are using two genera of Lake Malawi (Africa) cichlid fishes (Aulonocara stuartgranti [widened canals], and Tramitichromis sp. [narrow canals]) for comparative anatomical, developmental, and behavioral approaches that seek to understand structure-function-behavioral relationships in the lateral line system. Outcomes will also have important implications for our understanding of the evolution of feeding habits of cichlids in the African Rift Lakes, of marine and freshwater fishes that feed on benthic prey, and those in disturbed habitats in which non-visual predators may have an ecological advantage.

  1. The pattern and timing of development of widened and narrow canals and the sensory organs contained within them has been to determine the developmental basis for evolutionary change in the lateral line canal system (Bird and Webb, 2014; Becker et al., 2016; Becker MS Thesis, Carter MS Thesis).
  2. The sensory basis of prey detection in Aulonocara and Tramitichromis was studied using a novel behavioral assay and live benthic prey (tethered adult brine shrimp; Schwalbe PhD dissertation). The presentation of live and dead prey under light or dark conditions revealed that Aulonocara can detect live prey in the dark (Schwalbe et al., 2012). The elimination of vision (in the dark, and with decreasing light intensity) and the lateral line system (with cobalt chloride inactivation) allowed the determination of differences in the relative roles of vision and lateral line input in prey detection in these two taxa (Schwalbe and Webb, 2014; Schwalbe and Webb, 2015). Operant conditioning with a food reward was used to train Aulonocara to detect artificial water flows emerging from sandy substrates. This allowed us to define the role of the lateral line system in flow detection, and to document, for the first time, the temporal course of lateral line recovery after cobalt chloride inactivation (Schwalbe et al., 2016).
  3. The convergent evolution of widened canals among teleost fishes is being studied in order to define common features of anatomy that might reveal convergent functional attributes.
  4. We have demonstrated the utility of µCT in the imaging and quantification of the morphology of the cranial lateral line canal system among species (e.g., Webb, et al., 2014). See the µCT Imaging page.
Donald- GoldfishHorizSection2.5X

Goldfish – horizontal section through anterior vertebrae

AB17-12-PandaBrain

Aulonocara baenschi – transverse section through brain

Resources Available for Use by Collaborators

Histology – Ontogenetic series (hatch through juvenile) of all of our study species (Metriaclima zebra, Labeotropheus fuelleborni, Tramitichromis sp., Aulonocara baenschi and A. stuartgranti) were paraffin-embedded and serial transverse sections (8µm thickness) of the head of larvae and juveniles were generated. Tissue was stained with the HBQ stain (BK Hall, 1986), which highlights cell nuclei, bone, cartilage and connective tissue. In addition to its utility for the analysis of the development of the lateral line system (neuromasts and canals), this material is also suitable for analyses of other aspects of the teleost head, including the skeleton, sensory systems (olfactory organs, taste buds, ear, retina) and central nervous system. See: Bird and Webb, 2014; Webb et al. 2014.

CT Images – We have 2-D data (transverse slices) and 3-D µCT reconstructions (in dorsal, lateral, and ventral views) for Metriaclima zebraLabeotropheus fuelleborniTramitichromis sp.Aulonocara baenschi and A. stuartgranti. All published CT images were generated using OsiriX (http://www.osirix-viewer.com).  See the CT Imaging page for more information

Potential collaborators interested in using any of this this material or using images derived from this material for use in publications are encouraged to contact us.

Publications

  1. Webb, JF. 1989.  Neuromast morphology and lateral line trunk canal ontogeny in two species of cichlids: An SEM Study. Morphology. 202: 53-68.
  2. Webb, JF. 1990. Ontogeny and phylogeny of the trunk lateral line system in cichlid fishes.  Journal of Zoology (London) 221: 405-418.
  3. Tarby, ML and Webb, JF. 2003.  Development of the supraorbital and mandibular lateral line canals in the cichlid, Archocentrus nigrofasciatus. J. Morphology 254: 44-57.
  4. Schwalbe, MAB, Bassett DK and Webb JF. 2012. Feeding in the dark: Lateral line mediated feeding behavior in the peacock cichlid, Aulonocara stuartgranti. Journal of Experimental Biology. 215: 2060-2071.
  5. Schwalbe, MAB and Webb, JF. 2014. Sensory basis for detection of benthic prey in two Lake Malawi cichlids. Zoology. 117: 112-121 http://sx.doi.org/10.1016/j.zool.2013.09.003
  6. Webb, JF, Bird, NC, Carter, L, Dickson, J. 2014. Comparative development and evolution of two morphologically and functionally distinct lateral line phenotypes in Lake Malawi cichlids. Journal of Morphology. 275(6): 678-692. (and Cover Photo)
  7. Bird, NC and Webb, JF. 2014. Heterochrony, modularity, and the functional evolution of the lateral line canal system of fishes. EvoDevo 2014, 5:21. DOI: 10.1186/2041-9139-5-21. Open Access   
  8. Schwalbe, MAB and Webb, JF. 2015. Light environment influences prey detection behavior in two sand-dwelling Lake Malawi cichlids.  J. Comp. Physiol. A.  201: 341-356.   
  9. Schwalbe MAB, Sevey, B and Webb JF. 2016. Detection of artificial water flows by the lateral line system of a benthic feeding cichlid fish. J. Exper. Biol. 219: 1050-1059.
  10. Becker, EA, Bird, NC, and Webb, JF.  2016. Post-embryonic development of canal and superficial neuromasts and the generation of two cranial lateral line phenotypes.  J. Morphol. 277: 1273-1291.  doi: 10.1002/jmor.20574
  11. Webb JF, Maruska KP, Butler JM and Schwalbe MAB. 2017? The mechanosensory lateral line system of cichlid fishes: anatomy to behavior. In: Abate ME & Noakes DLG (eds.). The Behavior, Ecology and Evolution of Cichlid Fishes: A Contemporary Modern Synthesis. Springer Academic. INVITED. Submitted Nov 2016.
  12. Becker, EA and Webb, JF. Susceptibility and recovery of canal and superficial neuromasts to cobalt chloride and gentamicin ablation in two Lake Malawi cichlid fishes. In prep.

Post-Docs and Graduate Students Trained

  1. Melissa Tarby (MS student, 1996-1998; BS Villanova University) Post-embryonic development of the lateral line system in the convict cichlid, Archocentrus nigrofasciatus. [had been histologist at Wyeth; now a Registered Nurse]
  2. Dr. Daniel K. Bassett (Post-Doc, 2007-2008; PhD., Univ. Auckland, New Zealand, lab of Dr. John Montgomery) – Lateral line-mediated prey search and feeding behavior in Aulonocara, a cichlid with widened lateral line canals from Lake Malawi; the relationship between sensory biology and success of invasive freshwater fishes. Supported by Institutional funds; generated preliminary data for NSF grant. [now post-doc at Memorial University (Newfoundland), and University of Auckland (New Zealand); now in tech industry in New Zealand].
  3. Dr. Margot A. B. Schwalbe (PhD student 2008-2013; BS, MS, U. Minnesota, Duluth) – Lateral line-mediated feeding behavior in two Lake Malawi cichlids. (Biological Sciences Teaching Excellence Award, URI Graduate Research Fellowship) [now Post-Doc at Tufts University, lab of Eric Tytell, and Tufts TEACHR Fellow]
  4. Emily Becker (MS student, 2011-2013; BS, University of Rhode Island) – The distribution and ontogeny of neuromast receptor organs and a comparison of methods for chemical ablation of the lateral line system in two cichlid fishes. [had been Manager of a commercial fish farm (in Maryland), and then Assistant Director, Zebrafish Facility at Duke University Medical School; now Aquaculture researcher for South Carolina Department of Natural Resources]
  5. Lauren Carter (MS student,  2012-2014.; BS, University of Rhode Island) MS (2012-2014) – Development of the pores in the lateral line canals of Lake Malawi cichlids. [now working at NOAA, Narragansett, RI]
  6. Dr. Nathan Bird (Post-Doc, 2012-2014; PhD., George Washington University, lab of Dr. Patricia Hernandez) – Heterochrony and modularity in the evolution of the lateral line system of Lake Malawi cichlids. [now Ass’t Prof. of Biology, Univ. Northern Iowa]
  7. Julia Johnstone (MS student, 2014-2017; BS, Smith College) – “Investigating Lateral Line Canal Morphogenesis as a Bone Remodeling Process in Two Lake Malawi Cichlids” ( Honorable Mention NSF Graduate Research Fellowship) [Now PhD student at University of Maine]

  Undergraduate Research Students

  1. Oliver Bender (2014-2015; Marine Biology major) – animal husbandry and analysis of neuromast patterning on the trunk of Aulonocara and Tramitichromis. (poster presented at 2015 ASIH meeting) [MS student at Univ. New Hampshire]
  2. Benjamin Sevey (2011-2014; Marine Biology/Computer Science major; NOAA Hollings Scholar; 2012 URI Coastal Fellow; Spring and Fall 2012 EPSCoR URE) – Behavioral studies of prey detection by cichlid fishes. (co-author on poster at SICB; co-author on Schwalbe et al., in prep.) [teaching]
  3. Christopher Holland (2012-2014; Animal Science major; Spring 2013 EPSCoR URE) – Sound production in cichlids [PhD. student in Animal Behavior (G. Rosenthal Lab, Texas A&M].
  4. Callie Veelenturf (2012-2013; Marine Biology major/Wildlife Conservation minor, Spring 2012 EPSCoR URE: NOAA Hollings Scholar) – Neuromast distribution in Tramitichromis sp. using fluorescent stains. [MS Student at Purdue University]
  5. Rebecca Scott (2012-2013; Marine Biology major/Wildlife Conservation major; Spring 2012 EPSCoR URE; 2012 URI Coastal Fellow) – Neuromast distribution in Tramitichromis sp. using fluorescent stains. [had been Ecosystem Modeler, NOAA; now graduate student at Georgia Southern Univ.]
  6. Lauren Carter (2011-2012; Biological Science major) – cichlid lateral line development and morphology; stayed on as MS student in Webb Lab [now working for NOAA Fisheries in Narragansett, RI]
  7. Tom Franklin (2011-2012; Biomedical Engineering major) – CT image analysis
  8. Kevin Borsay (Spring 2011; Ocean Engineering major) – design of artificial stimulus delivery apparatus [Now working in industry]
  9. Adam Arrighi (Summer 2011; Ocean Engineering major) – construction and evaluation of artificial stimulus delivery apparatus.
  10. Timothy Alberg (2009-2011; Biomedical Engineering major; 2011 Academic Excellence Award in Biomedical Engineering) – µCT imaging and post-processing; wrote user guide to µCT imaging software. [Now working as Biomedical Engineer in industry]

Animal Husbandry Team

  1. Emma Shoemaker (2015-2016; Marine Biology major)
  2. Renee Bakker (2014; Marine Biology major)
  3. Sean Duffey (2014; Marine Biology major; doing MO at Graduate School of Oceanography)
  4. Ryan Kennealy (Spring 2012; Marine Biology major)
  5. Michael Pettipas (Spring 2012; Marine Biology major)
  6. Brandon Fuller (2009-2012; Marine Biology major) – [MS in Environmental Science and Management at URI]
  7. Eilea Knotts (2011-2012; Marine Biology major; NOAA Hollings Scholar) [Now PhD student at U. South Carolina in invertebrate physiology]
  8. Russell Dauksis (2011; Marine Biology major; NOAA Hollings Scholar; Goldwater Scholar) –  [Now MS student at Cal. State Fullerton in Fish Ecology]
  9. Emily Becker (Spring 2010-2011; Marine Biology major) – Fish husbandry, stayed on as MS student. [Had been Asst. Dir. Zebrafish Facility, Duke Univ. Med. School; manager of a fish farm; now running zebrafish facility at Georgia Southern Univ.]
  10. Joshua Hower (2010-2011; Marine Biology major) [DVM, UPenn Veterinary School, Class of 2015; practicing veterinary medicine in North Carolina]

Conference Presentations

  1. Bassett, DK and Webb, JF. 2008. Is search behavior and prey detection mediated by the widened lateral line canal system in the Lake Malawi cichlid, Aulonocara hansbaenchi?  Ecological and Evolutionary Ethology of Fishes, Boston MA, June 2008.
  2. Bassett, DK and Webb, JF. 2008. Is search behavior and prey detection mediated by the widened lateral line canal system in the Lake Malawi cichlid, Aulonocara hansbaenchi?  American Society of Ichthyologists and Herpetologists ASIH, Montreal, July 2008.
  3. Bassett, DK and Webb, JF. 2009. Lateral line-mediated prey detection in the Lake Malawi cichlid, Aulonocara hansbaenchi. SICB, Boston, January 2009.
  4. Webb, JF. 2009. MicroCT imaging of the lateral line system of teleost fishes. Providence RI, Oct. 2009. Northeast Regional DVM/SICB, Providence RI, October 2009.
  5. Dickson, J. and Webb, JF. 2010. Development of the widened lateral line canals in a Lake Malawi cichlid: Insights into lateral line evolution. SICB, Seattle WA, January 2010.
  6. Bergstrom, MA. and Webb, JF.  2010. Hydrodynamic detection of different prey species by the widened lateral line canal system of a Lake Malawi cichlid. American Society of Ichthyologists and Herpetologists, Providence, 2010
  7. Alberg, T, Moore, DC and Webb, JF. 2010. µCT Imaging of the cranial lateral line canal system of teleost fishes. American Society of Ichthyologists and Herpetologists, Providence, RI, July 2010.
  8. Dickson, J. and Webb, JF. Comparative Development of Lateral Line Canals in Three Lake Malawi Cichlids: Insights into the Evolution of Widened Canals. American Society of Ichthyologists and Herpetologists, Providence, 2010
  9. Bergstrom, ME and Webb, JF. 2011. Linking hydrodynamic stimuli and lateral line-mediated feeding behavior in a Lake Malawi cichlid. SICB, Salt Lake City, UT, Jan 2011.
  10. Webb, JF. and Alberg T. 2011. Convergent Evolution of an Adaptive Phenotype in the Mechanosensory Lateral Line System: It’s not that Simple. SICB, Salt Lake City, Jan 2011.
  11. Dickson, J. and Webb JF. 2011. Comparative post-embryonic development of the cranial lateral line canal system in cichlid fishes: Temporal and spatial patterns. SICB, Salt Lake City, UT, Jan 2011 (presented by Webb).
  12. Bergstrom, ME and Webb, JF. 2011. Feeding behavior in peacock cichlids is mediated by non-visual senses. American Behavior Society, Indianapolis, IN, July 2011.
  13. Bergstrom, ME and Webb, JF. 2011. Feeding in the dark: Peacock cichlids detect prey using the lateral line system. International Congress on Flow Sensing in Water and Air, Bonn Germany, July 2011 (poster, presented by Webb).
  14. Bergstrom, ME, Becker, E and Webb, JF. 2011. Probing the role of the lateral line system in feeding behavior using chemical ablation with cobalt chloride. Northeast Regional Meeting of the Division of Vertebrate Morphology, SICB – Fall 2011 at URI
  15. Bergstrom, ME and Webb, JF. 2011. Feeding in the dark: Peacock cichlids detect prey using the lateral line system. International Congress on Flow Sensing in Water and Air.
  16. Schwalbe, MAB, and Webb, JF. 2012. Same prey, different strategies: how sensory morphology and behavior differ between two species of Lake Malawi cichlids.” 10th International Congress of Neuroethology, College Park, Maryland. Selected for Participant Symposium.
  17. Becker, E, Scott, R & Webb, JF. 2013. Diversity of adult lateral line morphologies is not explained by differences in neuromast patterning in two Lake Malawi cichlids. SICB, San Francisco.
  18. Schwalbe, MAB, & Webb, JF. 2013.  Contributions of sensory morphology and prey detection behavior to trophic niche differentiation in two sand-feeding Lake Malawi cichlids. SICB, San Francisco.
  19. Bird, NC and Webb, JF. 2013. Evolution of the lateral line system of fishes via dissociated heterochrony. NE Regional Meeting, Division of Vertebrate Morphology, SICB. Oct. 2013 at Yale University.
  20. Bird, NC and Webb, JF. 2014. Modularity and heterochrony in the adaptive evolution of the lateral line system of fishes. SICB Jan. 2014, Austin, TX.
  21. Carter, L and Webb, JF. 2014.  A comparison of the development of the pores of the cranial lateral line canals in two species of cichlid fishes with functionally distinct canal morphologies. SICB Jan. 2014, Austin, TX.
  22. Schwalbe, MAB, Sevey BJ & Webb, JF. 2014.  Conditioned behavioral responses to artificial water flows by the lateral line system in a cichlid fish. SICB Jan. 2014, Austin, TX.
  23. Schwalbe, MAB, Webb, JF. 2014.  Artificial vs. natural stimuli: How conditioned responses to artificial water flows reveal the sensory basis for prey detection in a cichlid fish.  SICB Jan. 2014, Austin, TX.
  24. Holland C, Schwalbe, MAB, Webb JF. 2014. Aggression and reproductive behavior in two cichlid fish species that differ in their sensory biology. SICB Jan. 2014, Austin, TX. Integrative and Comparative Biology, in press.
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