Sensory Ontogeny of a Coral Reef Goby

The Role of Larval Orientation Behavior in Determining Population Connectivity – In collaboration with PM Buston, J Atema (Boston University), CB Paris (U. Miami).

Funded by NSF Grant Ocean Sciences -1459546 (2015 – Pres.)

Understanding the patterns and causes of larval dispersal and their consequences for fish populations is a major goal of 21st century marine ecology. Patterns of larval dispersal determine the probability of larval exchange, or connectivity, among populations. In turn, population connectivity has major consequences for metapopulation dynamics and evolution within metapopulations. Further, understanding population connectivity is critical for the design of effective networks of marine reserves and for development of sustainable fisheries. This project entails a a comprehensive, integrated, and potentially transformative investigation of how marine larvae orient in the pelagic environment in order to find suitable settlement sites. It is being done using the neon goby, Elacatinus lori and there are three motives for the choice of study system: i) direct genetic methods have already been used to describe the complete dispersal kernel for this species, and these observations indicate that dispersal is less extensive than predicted by a high-resolution biophysical model; ii) E. lori can be reared in the lab from hatching to settlement providing a reliable source of larvae of all ages for proposed experiments; iii) a new, proven behavioral observation platform, the Drifting In Situ Chamber (DISC, pioneered by Dr. Paris), allows measurements of larval orientation behavior in open water.  This collaborative project has three specific objectives: 1) to understand ontogenetic changes in larval orientation capabilities, by correlating larval orientation behavior with developmental sensory anatomy; 2) to analyze variation in the precision of larval orientation in different environmental contexts through ontogeny; 3) to test alternative hypotheses for the goal of larval orientation behavior, i.e., to determine where larvae are heading, as they develop.

The anatomy and function of individual sensory systems has been studied in a limited number of coral reef fish species. Their late stage larvae are known to respond to olfactory, auditory and/or visual cues during navigation and/or settlement. It is known that fish larvae can swim directionally at rates faster than prevailing currents, but the way in which larvae of any one species orients (from hatching to transformation and settlement) has not been investigated. This will be the first integrated study of the ontogeny of multiple senses and larval orientation behavior, and the first such analysis of the sensory biology of a member of the family Gobiidae, the largest family of reef fishes and one that is a critical component of coral reef fish communities.

GobyHistology_2014Version2FINALSensory anatomy of Elacatinus lori settler (9 mm SL). a) Olfactory organ is blind sac with olfactory epithelium (oe), and one of two nares (n) visible. Oral valves (v) in buccal cavity (bc) bounded ventrally by mandible (md). b) Flat olfactory epithelium (oe) with superficial neuromasts (sn) and cupular remnant (blue); c) Eyes with retina (r), lens (l), iris (ir), cornea (c); medial supraorbital LL canal grooves (so). d) Inner ear, lateral to the hindbrain (hb), showing semicircular canal (sc), otolithic organ (saccule, sa), and innervation by auditory nerve (VIII); distance between asterisks indicates otolith size (dissolved in prep.). e) SEM of mandible (ventral view) with neuromasts (arrows). Inset = neuromast with hair cells and orientation (arrow). f) Example of DASPEI-stained neuromasts (dorsal side of head, E. lobeli adult). Scale bars: a, c, d = 100 µm; e = 100 µm (inset = 2 µm), b = 50 µm, f = 1 mm.

Methods: Histological analysis, vital fluorescent staining, scanning electron microscopy (SEM) and µCT imaging will be used to document the development of the olfactory, gustatory, auditory, and lateral line systems. The number and thickness of retinal layers and retinal mosaic will be analyzed using histology and flat mount preparations. Finally, histological analysis and µCT will be used to analyze the relative size of the olfactory, visual, auditory and lateral line centers of the brain providing a first approximation of the relative importance of the senses as they may change through the larval and juvenile phases of development.

Post-Docs and Graduate Students Trained:

  1. Dr. Yinan Hu (PhD in Craig Albertson lab, U. Mass Amherst) – Sept. 2015-Pres. – sensory ontogeny in Elacatinus spp.
  2. Katie Nickles (MS student, Fall 2017-Pres.; BS in Marine Biology URI) – Development of the lateral line and visual systems in Elacatinus spp.

Undergraduate Researchers:

  1. Oliver Bender (Marine Biology major, URI) – Summer 2015 – Development of olfactory and gustatory systems in Elacatinus spp. (MS student at Univ. New Hampshire, as of Fall 2016)
  2. Katie Nickles (Marine Biology major, URI) – Summer 2016 – August 2017 – Development of mechanosensory lateral line system in Elacatinus spp.

Conference Presentations:

  1. Webb, JW. Sensory ontogeny in fishes: It’s all in the timing. Ecology and Evolutionary Ethology of Fishes, Tallahassee, FLA – June 2016.
  2. Hu Y. and Webb, JF. Ontogeny of the olfactory and gustatory systems in Elacatinus spp. (Gobiidae): Potential for chemosensory-guided navigation in pelagic larvae? Joint Meeting of Ichthyologists and Herpetologists, New Orleans, LA. July 2016.
  3. Hu, Y, Majoris, JE*, Buston, PM, and Webb, JF. Development of the nose and internal taste buds in two species of neon gobies (Elacatinus spp): Potential to facilitate navigation of pelagic larvae. SICB, New Orleans, LA. Jan. 2017. Integrative and Comparative Biology. In Press.
  4. Nickles K*, Hu Y, Majoris JE*, Buston PM and Webb JF. Ontogeny of the Lateral Line System in a Caribbean Reef Goby, Elacatinus lori.  ASIH/JMIH annual meeting – Austin TX July 2017.

Publications:

  1. Hu, Y., Majoris, J., Buston, P and Webb, JF. Development of the olfactory and gustatory systems in a goby with a comparison to other coral reef fishes. In prep. for Marine Biology.
  2. Hu, Y. and Webb, JF. Development of the ear in a goby …….In prep.
  3. Nickles, K., Hu, Y., and Webb, JF. The lateral line system of Elacatinus lori (Gobiidae): Organization and ontogeny of neuromast distributions. In prep.

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