Research Interests

Ecophysiology • EcoDevo • Conservation Biology • Malacology • Crustacean Biology

I’m interested in understanding how changes in the abiotic environment (especially alterations in temperature and pH) influence physiological processes in marine invertebrates, both across taxa, and across life history stages within a single species. I am also interested in biological questions related to organism-environment interactions and scale - how do a species' physiological tolerances influence its performance and distribution and what effect do these variations have on whole ecosystem features and processes? I’ve taken a broadly integrative approach to investigate these types of questions, utilizing both whole organism and functional genomics tools to address physiological hypotheses in a diverse array of taxa (porcelain crabs, giant clams, and sea hares).

 

Current Projects

Physiology of Tropical Giant Clams

A juvenile Tridacna crocea.

A juvenile Tridacna crocea.

Giant clams (genus Tridacna) are among the most charismatic of coral reef inhabitants and are important both culturally and economically in many developing island nations where their annual export production values can exceed $90 million USD (~5% of total GDP). Giant clams also host symbiotic algae (genus Symbiodinium), a characteristic shared by many reef-building corals. However, unlike corals, whose temperature induced symbiotic breakdown (bleaching) has been intensively studied, there is currently very little known about the effects of increased temperature and low pH on tridacnid clams and their symbionts.

*** More Information Coming Soon ***


Susceptibility of Early-Life Stages to Multiple Stressors

Ocean warming and acidification are both products of increased atmospheric pCO2, and have been shown in many taxa to lead to altered developmental timelines, inhibition of growth, malformations in calcitic exoskeletons, and reduced fitness. However, the magnitude of these effects can vary significantly across taxa and across life history stages within a single taxon. Early life history stages are often more susceptible to acute changes in the environment than adults and frequently require a narrower range of optimal conditions to successfully complete their development. Mortality among early recruits can be extremely high (>90%) even under ambient natural conditions and thus sensitive early life history stages may represent important population bottlenecks.  Thus understanding early life history responses to stress are of paramount importance for improving predictions about species persistence under a changing climate.

 

I'm particularly interested in investigating the sensitivity of early larval stages of marine calcifiers to multiple climate change stressors and have examined these effects in several systems including crustaceans (Petrolisthes crabs), gastropods (sea hares), and bivalves (Tridacna clams).  Recently, I've shown that in the tropical sea hare Stylocheilus striatus, hatching success was reduced by ~20 and 55% under high pCO2 and warming, respectively, while simultaneous exposure to both conditions resulted in a nearly additive 70% reduction in hatching.  Exposure of embryos to climate change stressors also resulted in significant morphological effects with larval exhibiting a 53% reduction in size under multi-stressor conditions relative to modern ambient controls (Armstrong et al. 2017).

 

I'm also interested in understanding how the timing of exposure to "extreme" events (e.g. heat waves, high pCO2 upwelling) may alter developmental trajectories in marine invertebrates.  To address this question, I worked in collaboration with the Calosi Lab at the University of Plymouth to assess developmental effects of exposure to acute heat stress in an intertidal porcelain crab, Porcellana platycheles.  Embryos exposed to an acute heat shock in early development (Early and Double Heat Shock treatments) showed significantly higher levels of mortality mid-way through the development.  However, exposure to heat shock in later development had no (or only slightly negative) effect on embryonic survival.  This suggests that even within early life history stages, there are windows of increased vulnerability to stress exposure.

Exposure to multistressor conditions has a nearly additive, negative, effect on hatching success in the tropical sea hare Stylocheilus striatus.  From (Armstrong et al. 2017)

Exposure to multistressor conditions has a nearly additive, negative, effect on hatching success in the tropical sea hare Stylocheilus striatus.  From (Armstrong et al. 2017)

Porcellana platycheles embryos exposed to 1-h heat shock early in development (orange), or both early and late (red) showed higher levels of mortality mid-way through the experiment (black arrow) than those exposed to heat shock later in development or not at all (green and blue lines).

Porcellana platycheles embryos exposed to 1-h heat shock early in development (orange), or both early and late (red) showed higher levels of mortality mid-way through the experiment (black arrow) than those exposed to heat shock later in development or not at all (green and blue lines).


Using nExt-generation sequencing to assess Mechanisms Underlying Differential Sensitivity

The intertidal zone is a highly dynamic environment where species zonate as a consequence of their relative tolerances to abiotic stress. In order to assess regulation of stress responsiveness among intertidal species, I utilized comparative next-generation sequencing to investigate the transcriptomic responses of two, differentially sensitive, intertidal species of porcelain crab (genus Petrolisthes) to natural variability in temperature and pH.

 

Congeners were exposed to either a low-variability, ambient control or a high-variability stress treatment where temperature spiked +15 °C and pH dropped 0.5 units mimicking natural diel fluctuations. Gill tissue was collected from crabs exposed to a single temperature/pH cycle (naïve response) and from those exposed to several cycles over two-weeks (acclimated response). Among the most strongly differentially expressed genes were those involved in acid-base regulation (e.g. VHAs) and stress recovery (e.g. HSPs), and patterns of expression differed significantly between species in potentially ecologically relevant ways. Although P. manimaculcus exhibited a greater degree of expression change, nearly five times more genes were differentially expressed in P. cinctipes. In addition, for P. manimaculis, expression changes at a given exposure time did not differ significantly between stress and ambient treatments whereas both naïve and acclimated individuals of P. cinctipes showed strong, stress-specific alteration in expression of putative acid-base regulatory genes.

 

These results suggest that P. manimaculis’ sensitivity to abiotic stress may be a result of a reduced molecular stress response generally, and a limited capacity to alter expression of acid-base regulatory proteins in particular. This reduced responsiveness may be a consistent feature among species susceptible to environmental stress, setting modern habitat limits and potentially acting as a primary determinant of “winners and losers” under future climate change.

Transcriptomic responses of the congeneric species Petrolisthes cinctipes and P. manimacuis.  In the more heat-sensitive species, P. manimaculus, fewer genes are differentially expressed in response to heat shock and acidification, but those genes respond more strongly than in the heat tolerant P. cinctipes.

Transcriptomic responses of the congeneric species Petrolisthes cinctipes and P. manimacuis.  In the more heat-sensitive species, P. manimaculus, fewer genes are differentially expressed in response to heat shock and acidification, but those genes respond more strongly than in the heat tolerant P. cinctipes.


Past Projects

Phytoplankton Community Structure and Carbon Export in the North Pacific

TokyoCruiseTrack2.png

As a graduate student in the Quay Lab at the University of Washington, I participated in two trans-Pacific research cruises (summer and fall 2011, see image) on the OOCL container ship Tokyo to gather baseline data on the temporal and spatial variability in rates of primary production, phytoplankton community structure (in collaboration with the Armbrust Lab), and carbon export in the subtropical and subarctic North Pacific.

SeaFlow.png

Results from this work can be found here:

Palevsky HI, Quay PD, Lockwood DE, & Nicholson DP. (2016) The annual cycle of gross primary production, net community production and export efficiency across the North Pacific Ocean. Global Biogeochemical Cycles 29
Online

 


Targeted Metabolomics in Giant Clams and Reef-Building Corals

Glycine betaine.  One of the most abundant betaines in marine organisms.

Glycine betaine.  One of the most abundant betaines in marine organisms.

When organisms are faced with osmotic stress they often produce compounds known as osmolytes to help reduce osmotic pressures and thereby protect cells from damage from dessication or over-hydration. One class of purported osmolytes are betaines and in particular, the compound glycine betaine (see image).

Interestingly, glycine betaine has also been implicated in plants to play a role in stabilizing chloroplast photosytem II complexes leading to reduced oxidative damage during periods of intense photosynthesis. Glycine betaine (and other related compounds) have been recently reported in corals and are associated with both the zooxanthellae and cnidarian hosts. Although more reserach needs to be done to ascertain the exact functional role of betaines in corals, their presence suggests that corals may be using betaines in a dual capacity - both as osmolytes and as photoprotectants

BetainePlot_New.png

As an undergraduate, I worked in the Hill Lab using a targeted metabolomics approach to identify and quantify betaine compounds within samples of giant clam mantle (siphonal and byssal), adductor mussel, and gill. Several betaines were found to be present in extremely high abundance in giant clam tissues. As in corals, this suggests that betaines may be playing a functional role in tridacnid clams - either as osmolytes, or perhaps as stabilizing agents for the photosystem II complex of symbiotic zooxanthellae.

Results from this work can be found here:

Hill RW, Armstrong EJ, Florn AM, Li Chao, Walquist RW, Edward A. (2017) Abundant betaines in giant clams (Tridacnidae) and western Pacific reef corals, including study of coral betaine acclimatization.
Marine Ecology Progress Series. 56
Online


Gulf of Maine CyanoHAB Monitoring Project

As an undergraduate student, I interned in the Anderson Lab at Woods Hole Oceanographic Institute(WHOI) where we used a Fluorescent-In-Situ-Hybridization (FISH) technique to identify cyanobacterial species which secrete potent toxins that are harmful to humans and other organisms.

Conceptual cartoon of fluorescent in-situ hybridization technique on the left.  On the right, examples of labelled and unlabelled cyanobacterial cells.  The goal is to develop fluorescent probes with are specific to some species (e.g. toxic Microcystis spp.) while non-reactive to others (e.g. non-toxic Anabaena spp.) as shown here.

Conceptual cartoon of fluorescent in-situ hybridization technique on the left.  On the right, examples of labelled and unlabelled cyanobacterial cells.  The goal is to develop fluorescent probes with are specific to some species (e.g. toxic Microcystis spp.) while non-reactive to others (e.g. non-toxic Anabaena spp.) as shown here.

FISH is a staining technique that allows for labelling of cells containing a specific sequence of either DNA or RNA. A fluroescent molecule is attached to a small nucleotide primer which is complementary to the sequence of DNA or RNA of interest in the cell (see image below). When the primer encounters this target sequence it binds, bringing the fluroescent molecule along with it and thereby "labelling" the cell. If enough primer binds inside a cell, that cell can be identified under a fluorescent imaging microscope (see below).

The goal of this project was to design RNA-binding probes from available 16s-rRNA data for three most important toxic cyanobacteria species in the Gulf of Maine (Microcystis aeruginosa, Anabaena flos-aquae, and Cylindrospermopsis raciborskii). Using FISH, we were able to clearly label potentially toxic cells, thereby allowing for quick and sure identification of dangerous cyanobacteria. As part of this research, I successfully developed two species-specific rRNA probes. Work on this project continues in the Anderson lab with the ultimate goal being the development of a cyanobacteria-sensing instrument that can be permanently moored in the Gulf of Maine, alerting coastal managers to the presence and abundance of toxic cyanobacterial blooms in real-time.