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Award Detail

Doing Business As Name:University of Hawaii
  • Daniel K Hartline
  • (808) 956-8003
  • Andrew Christie
Award Date:01/28/2015
Estimated Total Award Amount: $ 624,992
Funds Obligated to Date: $ 624,992
  • FY 2015=$624,992
Start Date:03/01/2015
End Date:08/31/2020
Transaction Type:Grant
Awarding Agency Code:4900
Funding Agency Code:4900
CFDA Number:47.050
Primary Program Source:040100 NSF RESEARCH & RELATED ACTIVIT
Award Title or Description:Collaborative Proposal: Optimizing Recruitment of Neocalanus copepods through Strategic Timing of Reproduction and Growth in the Gulf of Alaska
Federal Award ID Number:1459235
DUNS ID:965088057
Parent DUNS ID:009438664
Program Officer:
  • Cynthia Suchman
  • (703) 292-2092

Awardee Location

Street:2440 Campus Road, Box 368
Awardee Cong. District:01

Primary Place of Performance

Organization Name:University of Hawaii
Street:1993 East-West Rd
Cong. District:01

Abstract at Time of Award

The Gulf of Alaska supports a diverse and productive marine community that includes many commercially important fishes. Toward the base of this food web are small planktonic crustaceans that serve as the primary food source for many of these fish, as well as seabirds and marine mammals. The copepod Neocalanus flemingeri is one of these crustaceans, and it experiences rapid population growth during each spring's algal, or phytoplankton, bloom. An apparent mismatch between the presence of the youngest stages of the copepod, or nauplii, in early winter and the unpredictable timing of the spring phytoplankton bloom several months later raises important questions about when females reproduce and how this relates to survival and growth of nauplii. Two types of dormancy, diapause in adult females and physiological quiescence in nauplii, may be the key to the success of this copepod species. Timing and duration of the egg-laying period by adult females is linked to emergence from diapause. In addition, nauplii may enter a state of physiological quiescence while food resources are low, resuming growth after phytoplankton levels increase. This research will address a long-standing goal of biological oceanographers to understand dormancy and its role in controlling population cycles in marine copepods. It will use new technologies in molecular biology called transcriptomics to catalog the messages used by the cells to control copepod life processes, in this case those related to dormancy in adults and nauplii. Undergraduate students and a postdoctoral investigator will be trained in interdisciplinary research, and students from Native Hawaiian and Native Alaskan groups will be targeted for participation. Fishing is a major industry in the Gulf of Alaska, and outreach will focus on communicating the role copepods play in marine ecosystems. New content, including images, will be generated for existing websites: the Seward Line long-term observation program, the Alaska Ocean Observing System and the Gulf Watch Alaska Program. Recruitment to the Neocalanus flemingeri spring population is dependent on successful emergence from diapause followed by reproduction, survival, and growth of the next generation. Individual-based models have made significant progress in predicting population growth in calanoid copepods using food, temperature, and advection as key environmental factors. Few of these models include predictors for naupliar recruitment, however, because little is known about this part of the life cycle given sampling difficulties and the lack of biomarkers to evaluate physiological state. This study will leverage existing monitoring efforts to track the N. flemingeri population during the winter and early spring. The research team will combine laboratory and field approaches to determine duration and synchronization of reproduction in emerging females and strategies for naupliar survival during low food conditions. Zooplankton samples will be processed to enumerate nauplii to species and to determine physiological condition of both nauplii and adult females. Gene expression studies will develop molecular markers for female dormancy and reproductive readiness and for naupliar growth and possible dormancy, which in turn will be used to evaluate field collected individuals. This will be the first comprehensive study to combine molecular and traditional tools to connect diapausing adults, naupliar production, and the resulting spring population of copepodites.

Publications Produced as a Result of this Research

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Roncalli, V., Sommer, S. A., Cieslak, M. C., Clarke, C., Hopcroft, R. R., Lenz, P. H. "Physiological characterization of the emergence from diapause: A transcriptomics approach." Scientific Reports, v.8, 2018, p.12577. doi:10.1038/s41598-018-30873-0 

Lenz, P.H. and Roncalli, V. "Diapause within the context of life-history strategies in calanid copepods (Calanoida: Crustacea)" The Biological Bulletin, v.237, 2019, p.170. doi:DOI: 10.1086/705160 

Porter, M.L., Steck, M., Roncalli, V., Lenz, P.H. "Molecular characterization of copepod photoreception" Biological Bulletin, v.233, 2017, p.96. doi:10.1086/694564 

Christie, A.E., Roncalli, V. and Lenz, P.H. "Diversity of insulin-like peptide signaling system proteins in Calanus finmarchicus (Crustacea; Copepoda) ? Possible contributors to seasonal pre-adult diapause." General and Comparative Endocrinology, 236,, v.236, 2016, p.157.

Roncalli, V., Cieslak, M. C., Sommer, S. A., Hopcroft, R. R., & Lenz, P. H. "De novo transcriptome assembly of the calanoid copepod Neocalanus flemingeri: a new resource for emergence from diapause" Marine Genomics, v.37, 2018, p.114. doi:10.1016/j.margen.2017.09.002 

Roncalli, V., Cieslak, M.C., Germano, M., Hopcroft, R.R. and Lenz, P.H. "Regional heterogeneity impacts gene expression in the subarctic zooplankter Neocalanus flemingeri in the northern Gulf of Alaska" Communications Biology, v.2, 2019, p.1. doi: 

Cieslak, M.C., Castelfranco, A.M., Roncalli, V., Lenz, P.H. and Hartline, D.K. "t-Distributed Stochastic Neighbor Embedding (t-SNE): A tool for eco-physiological transcriptomic analysis." Marine Genomics,, v.26, 2019, p.100723. doi: 

Roncalli, V., Cieslak, M.C., Hopcroft, R.R. and Lenz, P.H. "Capital breeding in a diapausing copepod: A transcriptomics analysis" Frontiers in Marine Science, v.7, 2020, p.56. doi:doi: 10.3389/fmars.2020.00056 

Roncalli, V., Christie, A. E., Sommer, S. A., Cieslak, M. C., Hartline, D. K. & Lenz, P. H. "A deep transcriptomic resource for the copepod crustacean Labidocera madurae: a potential indicator species for assessing near shore ecosystem health" PLoS One, v.12, 2017, p.e0186794. doi:10.1371/journal.pone.0186794 

Lenz, Petra H. and Roncalli, Vittoria "Diapause within the Context of Life-History Strategies in Calanid Copepods (Calanoida: Crustacea)" The Biological Bulletin, v.237, 2019, p.. doi:10.1086/705160 Citation details  

Christie, A. E., Cieslak, M. C., Roncalli, V., Lenz, P. H., Major, K. M., Poynton, H.C. "Prediction of a peptidome for the ecotoxicological model Hyalella azteca (Crustacea; Amphipoda) using a de novo assembled transcriptome." Marine Genomics, v.38, 2018, p.67. doi:10.1016/j.margen.2017.12.003 

Christie, A .E., Yu, A., Pascual, M. G., Roncalli, V., Cieslak, M. C., Warner, A. N., Lameyer, T. J., Stanhope, M. E., Dickinson, P. S., Hull, J. J. "Circadian signaling in Homarus americanus: region-specific de novo assembled transcriptomes show that both the brain and eyestalk ganglia possess the molecular components of a putative clock system" Marine Genomics, v.40, 2018, p.25. doi:10.1016/j.margen.2018.03.002 

Project Outcomes Report


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.

The research produced data key to assessing the resilience to environmental stress of the highly productive fisheries in the high-latitude North Pacific. The focus of the study was on lipid-rich copepods, which are an important food source for larval fish and forage fishes. A critical phase in the life cycle of these copepods is the period of dormancy (diapause) that precedes reproduction in late winter. Understanding diapause and emergence from diapause is essential for predicting how the copepods might be impacted by future environmental perturbations. During a 4-year program of oceanographic cruises during the fall, plankton were collected from below 400-meters depth in Prince William Sound in Alaska and offshore in the Gulf of Alaska. Adult females of the target organism, the subarctic marine copepod Neocalanus flemingeri, were live-sorted for laboratory incubations for physiological profiling, size and lipid volume measurements and total egg production. A separate set of samples from different depth layers was preserved and counted. Physiological profiling was done by monitoring the messages, the "mRNA transcripts," produced by the copepod's genes to control its life processes using a state-of-the-art molecular biological approach. The first step was to generate a gene reference through a shotgun assembly of millions of short-sequence reads produced from the mRNA. This reference transcriptome was then used to measure the expression level (amount of message) of each gene in samples collected during different years and at different time points after females emerged from diapause. One discovery was that during diapause the N. flemingeri females express genes that allow them to conserve energy, lengthen their lifespan, arrest cellular processes and protect them from oxidative stress.

Diapause and post-diapause females represent two distinct physiological phases as determined from gene expression profiles. The transition from one phase to the next is a lengthy step-wise "post-diapause" restart process before egg development ("oogenesis") becomes the dominant process at one-week post-diapause. In addition, this study has uncovered an orchestrated and complex sequence of changes in gene expression that start almost immediately after the diapause termination stimulus through the early post-diapause phase. These findings give rise to the hypothesis that these sequential changes in gene expression control a universal mechanism that fully terminates diapause before an organism can resume its developmental program. However, even after the transition is complete there is a lengthy post-diapause phase, which is necessary to complete the reproductive program. After emergence from diapause, it takes six to seven weeks before females release the first clutch of eggs.

Females die once spawning is complete, and the population is composed of newly-hatched larval copepods (?nauplii?), which depend on the spring phytoplankton bloom to grow. As hypothesized, preliminary evidence suggests that nauplii can themselves enter a state of physiological quiescence while food resources are low, resuming growth after phytoplankton (algae) levels increase. Quiescence in the nauplii bore some of the molecular signatures of diapause, giving better insight into its mechanism and ultimately to the species? resilience to environmental variability. There was evidence that during a year of very low phytoplankton abundances, although females were still able to complete diapause and the post-diapause reproductive program, overall fecundity was lower. In addition, there were significant interannual differences in gene expression profiles of females in diapause suggesting that growth conditions affected this phase. This study is closing a knowledge gap in the mechanistic understanding of how an organism restarts physiological processes after prolonged diapause to complete its life cycle. The research has furthered the long-standing goal of biological oceanographers of understanding dormancy and its role in controlling population cycles in marine copepods. It has introduced new technologies for studying dormancy in adults and nauplii.  These new insights will contribute to predictions and preparation for anticipated environmental changes impacting vulnerable fisheries in a region that currently accounts for over half of all fish produced for consumption in the United States  and a third of its economic value.

The project provided training opportunities for two post-doctoral fellows, a graduate student, four undergraduate students and two post-baccalaureate fellows from the University of Hawaiʻi at Mānoa and additional students at the University of Alaska Fairbanks. Trainees from Hawaiʻi joined research cruises in the Gulf of Alaska and participated in laboratory experiments at the University of Alaska Fairbanks. One undergraduate student was from an under-represented group and another was a former NIH Maximizing Access to Research Careers fellow. The project supported the development and implementation of a new graduate course in bioinformatics of non-model species. Outreach in Hawaiʻi and Alaska occurred through special events like the large biennial Open House in Hawaiʻi (2015, 2017, 2019) and presentations and laboratory tours in Seward and Homer, Alaska (2018, 2019).  The research was featured in a children?s book published in 2020 (Into the Deep: Science, Technology, and the Quest to Protect the Ocean by Christy Peterson, Lerner Publishing Group).


Last Modified: 12/13/2020
Modified by: Daniel K Hartline

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