Award Abstract # 1356966
Collaborative Research: Turbulence-spurred settlement: Deciphering a newly recognized class of larval response

NSF Org: OCE
Division Of Ocean Sciences
Recipient: UNIVERSITY OF CALIFORNIA, DAVIS
Initial Amendment Date: January 13, 2014
Latest Amendment Date: September 2, 2016
Award Number: 1356966
Award Instrument: Standard Grant
Program Manager: Michael Sieracki
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: February 1, 2014
End Date: January 31, 2018 (Estimated)
Total Intended Award Amount: $305,067.00
Total Awarded Amount to Date: $305,067.00
Funds Obligated to Date: FY 2014 = $305,067.00
History of Investigator:
  • Brian Gaylord (Principal Investigator)
    bpgaylord@ucdavis.edu
Recipient Sponsored Research Office: University of California-Davis
1850 RESEARCH PARK DR STE 300
DAVIS
CA  US  95618-6153
(530)754-7700
Sponsor Congressional District: 04
Primary Place of Performance: Bodega Marine Laboratory - UC Davis
2099 Westside Road
Bodega Bay
CA  US  94923-0247
Primary Place of Performance
Congressional District:
02
Unique Entity Identifier (UEI): TX2DAGQPENZ5
Parent UEI:
NSF Program(s): BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001415DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 4444, 9169
Program Element Code(s): 165000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Overview: With this award the investigators will explore a habitat-scale oceanographic process that has the potential to integrate studies of larval delivery with an understanding of how larvae respond to substrate-associated cues. This work will build on published and preliminary data indicating that turbulent shear characteristic of high-energy near shore environments primes larvae to initiate settlement and to transform into the juvenile stage. These prior findings suggest that: 1) Because turbulence intensity varies predictably as a function of the strength of wave breaking and other factors, turbulence could operate as an indicator for larvae of their approach to suitable habitat, providing a link between larger-scale dispersal phenomena, and near-bottom search and selection behaviors; and. 2) The larval response to turbulence acts in an unprecedented fashion. In contrast to typical cues, turbulence does not induce settlement directly, but rather spurs otherwise "pre-competent" larvae that are refractory to chemical cues to become "competent", thereby causing them to acquire responsiveness to such cues and undergo settlement. The interdisciplinary team has combined expertise in larval biology, sensory ecology, and organism-flow interactions necessary to address this topic. They will employ a phylogenetically robust approach to explore the scope and adaptive significance of the turbulence response in a widespread and ecologically important class of organisms (echinoids; sea urchins and their relatives), and will determine whether the response is aligned with environmental conditions characteristic of these organisms' adult habitat. They will also test for ecologically important functional consequences of precocious, turbulence-induced settlement. This work will provide a detailed look at an entirely new class of settlement inducer, one with strong potential for changing current conceptualizations of dispersing larval stages, their ability to detect signatures of habitat across multiple scales, and the ways in which organism-level traits might influence population connectivity.

Intellectual Merit : How organisms with dispersing life stages find their way back to adult habitat is a fundamental question in marine ecology. Considerable research has explored links between transport, delivery, settlement, and recruitment, with important advances in knowledge. However, a complete understanding of the larval recruitment process remains elusive. Standard tools for estimating dispersal (e.g., numerical circulation models) have limited spatial resolution, which prevents them from predicting at scales below a few hundred meters how larvae will interact with the shore. Studies investigating larval attachment have focused on chemical, tactile, or near-bottom hydrodynamic cues active across microns to centimeters. The novelty of the present project is that it will focus on processes at habitat scales -- between transport and settlement -- where there is a gap in the understanding of processes.

Broader Impacts: This project will provide a framework for integrating key concepts of propagule dispersal and settlement, two fundamental but largely disjunct themes in marine science. The understanding that will come from this study will provide key information for ecosystem based management of coastal marine resources. The findings of the study will be communicated via publications and conference presentations. There will also be a robust education and public outreach effort. The investigators will develop a "Surfing to Settlement" virtual lab activity based on their research that will be incorporated into the VirtualUrchin web platform, a widely exploited educational resource at Stanford that gets thousands of unique users per month. Through connections to the San Francisco Bay National Estuarine Research Reserve, they will integrate the "Surfing to Settlement" activity into one of NERRs professional development workshops for central California educators, thus disseminating this resource to and gaining valuable feedback from dozens of teachers and thousands of students. The project will also continue an existing partnership with a local community college (Santa Rosa Community College) that provides a means for undergraduates who would otherwise get little exposure to the research enterprise to receive training and mentorship in the scientific process via extended internships. In addition, the investigators will expand development of a high-quality video/photo resource that documents early development, larval morphology and behavior in a phylogenetically broad array of animal phyla, and will disseminate this resource to the public via an existing collaboration with the internationally known Monterey Bay Aquarium.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Heyland, A and J. Hodin "A detailed staging scheme for late larval development in Strongylocentrotus purpuratus focused on readily-visible juvenile structures within the rudiment." BMC Developmental Biology , v.14 , 2014 , p.22 doi:10.1186/1471-213X-14-22
Heyland, A., J. Hodin, and C. Bishop. "Manipulation of developing juvenile structures in purple sea urchins (Strongylocentrotus purpuratus) by morpholino injection into late stage larvae." PLoS One , v.9 , 2014 , p.e113866
Hodin J., K. Lutek and A. Heyland "A newly identified left?right asymmetry in larval sea urchins" Royal Society Open Science , v.3 , 2016 , p.160139
Hodin J., K. Lutek, and A. Heyland "A newly identified left?right asymmetry in larval sea urchins" Royal Society Open Science , v.3 , 2016 , p.160139
Hodin, J., M.C. Ferner, C.J. Lowe, G. Ng, and B. Gaylord "Rethinking competence in marine life cycles: ontogenetic changes in the settlement response of sand dollar larvae exposed to turbulence" Royal Society Open Science , v.2 , 2015 , p.150114 doi.org/10.1098/RSOS.150114
Jason Hodin, Matthew C. Ferner, Gabriel Ng,Christopher J. Lowe, and Brian Gaylord "Rethinking competence in marine life cycles:ontogenetic changes in the settlement response of sand dollar larvae exposed to turbulence" Royal Society Open Science , v.2 , 2015 , p.150114 http://dx.doi.org/10.1098/rsos.150114
Jurgens, L.J. and B. Gaylord "Edge effects reverse facilitation by a widespread foundation species" Scientific Reports , v.6 , 2016 , p.37573 doi:10.1038/srep37573
Jurgens, L.J., and B. Gaylord "Physical effects of habitat-forming species override latitudinal trends in temperature" Ecology Letters , v.21 , 2018 , p.190
Jurgens, L., L. Rogers-Bennett, P.T. Raimondi, L.M. Schiebelhut, M.N. Dawson, R.K. Grosberg, and B. Gaylord "Severe mass mortality of rocky shore invertebrates across 100 km of coastline" PLoS One , v.10 , 2015 , p.e0126280 doi:10.1371/journal.pone.0126280
Nickols, K.J., J.W. White, J.L. Largier, and B. Gaylord "Marine population connectivity: reconciling large-scale dispersal and high self-retention" American Naturalist , v.185 , 2015 , p.196

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

NSF AWARD OCE-1356966

TURBULENCE-SPURRED SETTLEMENT: DECIPHERING A NEWLY RECOGNIZED CLASS OF LARVAL RESPONSE

PROJECT OUTCOMES

 

A dominant majority of shoreline-dwelling animals in the ocean produce microscopic offspring that live for days to months in the plankton, drifting in waters offshore of the coast. These tiny larval stages often look completely different in form compared to the juveniles and adults that they grow into, and which inhabit the rocky shores and beaches with which most people interface. The transition between these two stages is therefore one of the most notable and crucial steps in the life cycles of organisms in the sea.

In the research conducted by means of this grant, our team explored the transition that tiny larvae take in moving from the plankton to the shore, focusing in particular on sea urchins and their kin.  Our efforts were directed at understanding details of a recent discovery that we made just before the grant was awarded.  We found that the attainment of ‘competency,’ the ability of larvae to respond to chemical cues indicative of suitable habitat on the shore, can be triggered by physical attributes of the environment.  More specifically, we determined that exposure of sea urchin larvae to intense turbulence characteristic of wave-exposed coasts preferred by adults could cause the larvae to precociously enter the competent state.  Previously it had been thought that the timing of competency was determined simply by a hard-wired and therefore largely immutable developmental program. Learning that larvae at this key life transition are notably sensitive to a range of environmental experiences has important implications.  For example, knowledge concerning potential triggers of competency could substantially modify our  understanding of how populations of ecologically and commercially valuable species like sea urchins -- one of several invertebrates fished for human food -- are maintained.

We highlight here several novel findings that originated from this grant.  First, we documented through laboratory experiments that the turbulence response exhibited by a particular type of sea urchin (Strongylocentrotus purpuratus, the purple sea urchin) is not unique to just that species.  Other types of sea urchins, as well as a more distantly related invertebrate, the Pacific sand dollar, show a similar reaction to turbulence, in that the progression to competency is accelerated as a result of just a few minutes of exposure to intense turbulence.  This early shift to competency can shorten the minimum time spent in the water column by 20%.  Interestingly, the response is not universal in sea urchins nor is it limited to only urchins.  Several urchin species that we have tested whose adults dwell in deeper habitats where turbulence is weaker do not show any acceleration in competency in response to turbulence.  On the other hand, turbulence does appear to influence the manifestation of competency in more distantly related species, including a brittle star and marine snail.  Second, we demonstrated that the level of responsiveness of larvae to turbulence, and thus their propensity to become competent following such an environmental stimulus, increases as they get older.  This phenomenon includes a tendency for larvae to become less choosy about habitat.  At the same time, larvae that transition early to shoreline habitat bear a cost in that they are smaller and thus more vulnerable to physical stressors and predators.  A third finding of our research is that the response of larvae to turbulence can be long-lasting.  Larvae that experience intense turbulence, but which then are placed back into quiescent waters, do not regress to their original condition; rather, they remain competent.  This result suggests a physiological change that is not readily reversible.  Fourth, we have indications of population-level genetic variation in the turbulence response.

The project additionally contributed to the advancement of several graduate students who were supported by the grant, led to results covered by the popular media, and funded a freely-accessible web-based educational module on the VirtualUrchin platform (http://virtualurchin.org) that serves hundreds of thousands of secondary school students yearly.  Specifically, we produced a new interactive educational game for VirtualUrchin based upon our research called 'Surfing to Settlement', where the student controls a larval avatar that needs to find food and grow and ultimately locate a safe place to settle near to its kin, while avoiding planktonic predators and excessive offshore drift.

Together these research efforts have advanced our understanding of one of the most important life cycle transitions characterizing marine species, including a number that people rely on for food.

 


Last Modified: 04/30/2018
Modified by: Brian P Gaylord

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