Long read: Plankton in Peril!

3 May 2018

Plankton, in the popular imagination, are dull but worthy creatures. Dull because, amorphous and passive, they drift around helplessly on ocean currents, awaiting death by ingestion. Worthy because, in providing an All-You-Can-Eat buffet for predators from sardines to blue whales, they are the foundation of the oceans’ food-web. Not content with this contribution, plankton perform further services: their massive photosynthesis produces up to 50% of the world’s oxygen. Even after death, their contribution to human life continues, as their corpses “suffer a sea change”, into our fossil fuels. Ironically, all these services to the Earth and humanity are now under growing threat, from human-driven global environment change.

‘Plankton’ is the collective name for a wide variety of marine creatures, grouped not by species, but by behaviour. Or rather lack of it. The word ‘plankton’ derives from the Greek word planktos which means ‘drifting’: these are, by definition, animals that float along on the prevailing current. “So,” says Chan, “It might sound counterintuitive that we work on their behaviours, but we do. We look at how plankton behave and the implications of their behaviour; how their behaviour affects environment and vice versa. And it’s unique work.”

Plankton-busters, Tools of the Trade

The Chan Lab employs state-of-the-art technologies for their research, in particular two related techniques: Micro Particle Tracking Velocimetry and Micro Particle Image Velocimetry. These technologies were originally developed by engineers to trace complex flow patterns in liquids, by tracking the paths of individual fluid particles. Plankton researchers like Chan are now adapting these techniques to trace the complex fluid flow around free-swimming larvae, like slippersnail veligers, and thereby to identify and analyze their locomotion. Although other researchers have applied micro PTV/PIV to larger, ‘tethered’, individual organisms, Chan is among the first to use it at this small scale, on groups of free-swimming larvae. Chan’s technique involves observing groups of about 80 larvae housed in small flasks of seawater. Polystyrene ‘trace’ micro-particles are introduced to cloud the water, and the set-up is illuminated with batteries of super bright white LED’s. Throughout the duration of the study, high-speed, high resolution micro-videography recordings are made and analysed to produce visualizations of water flow around individual veliger. Chan’s lab sift the recordings to select those ‘bullseye’ video sequences where veligers clearly intersect the focal plane. This footage is then processed and analyzed using a battery of complex statistical and computational techniques, including Gaussian blur, MTrack2 tracking routine, Fast Fourier Transform, and ANOVA variance analysis. The unique combination of technologies and techniques allows detailed resolution of the swimming motion of the larval body, including the position of the velar, and even the beating of cilia on an individual velum. Larval body speed is easily calculated as length of path divided by duration of observation, and shell and velar lobe areas are measured from the central frame of the relevant image-sequence. To compare swimming speed and vela orientation, the Lab identifies the center of the shell and each velum, and computes the varying distances between them. To compare swimming speed and cilia motion, they quantify the ciliary beat frequencies of all individuals.

Dr Tessa Hill, a fellow high-profile researcher who, like Chan, runs her own eponymous institute - the Hill Biogeochemistry Lab at University College Davis California – describes this unique work thus:

“Karen Chan’s research, focusing on the nearshore waters along the coast of Hong Kong is both exciting and relevant. The more we learn, the more we understand how organisms might be ‘locally adapted’ to their neighborhood right along the coast. Karen is looking at big questions - evolution, adaptation, environmental stress, human impacts - and bringing them right home to the coastline. It is very exciting to see this work.”

To address these big questions, Chan employs an assortment of cutting-edge tools and techniques - including state-of-the-art engineering technologies such as Particle Image Velocimetry, and complex numerical simulations - to track the behaviours of her elusive subjects.

“Our species do ‘behave’,” observes Chan. “For one thing, they all swim. Not horizontally, against the current, but vertically, up and down the water column. And they seem to do so for a variety of ‘motives’, including foraging for food and avoiding predators.”

The ocean-drifting larval stage is vital for these species’ dispersal. Unfortunately, that dispersal is at the whim of the currents, a limitation that the plankton’s vertical mobility would seem unable to challenge. However, as Chan explains, her species can take advantage of the fact that current is not uniform throughout the water column.

“The analogy I use is that if you can move up and down, you can go onto different On and Off ramps on a highway. It’s about driving your car to the right entrance, and getting off at the right exit. So when, at different levels in the water column, currents are moving in different directions, plankton can move up and down, catching and riding a current which is going in a preferred direction.”

Such behaviour implies capacities for information-gathering and decision-making not naturally associated with mindless drifters. “These species don’t have brains,” Chan admits, “But they do have neuron clusters, and so can respond to various environmental cues.” Different plankton species, in fact, possess sensory mechanisms which can detect variations in a range of stimuli, including sunlight, temperature, gravity, water pressure, and sound. They are also able to gauge salinity, and to detect other chemical signatures, such as those associated with food sources, helping them to forage, and those associated with predators, helping them to avoid becoming forage. “Some coral-associated animals, like sea slugs,” notes Chan, “Even respond to a specific ‘time to come home’ chemical signal given off by the coral.”

At the current state of knowledge, Chan and her colleagues understand the mechanics of how the plankton neurons are triggered, but when asked how the organisms integrate these sensory inputs to generate behaviour, she throws up her hands. “No-one knows! If I could choose one superpower, it would be the ability to communicate with my animals, so that I could ask them. ‘Why are you doing this?’ I’m actually glad people can’t see me in our dark room here, cos I talk to my plankton a lot.”

Chan believes that the key to the mystery of plankton behaviour is how they resolve three conflicting basic survival needs: efficient swimming, efficient foraging, and efficient predator evasion. Chan cites the example of purple sea urchin larva.

As with many plankton species, the ‘cilia’ – the thousands of tiny hairs on their many arms – which urchins use to generate the motion for swimming, are the same ones used to feed. This implies a conflict of interests, since a body design which is perfect for fast swimming might be one which is inefficient at catching food. Further, in generating the movement to capture food, urchins disturb the surrounding fluid, producing a motion signature that nearby predators might sense. “Urchins have to balance these three elements in order to stay alive, and evolutionarily they’ve been selected to do this well”, says Chan.

A critical aspect of Chan’s research is how the planktonic larvae of keystone species are affected by global marine climate change. In the Lab, her team systematically manipulate environmental variables such as temperature, salinity, and pH levels, to mimic the effects of climate change factors. The results make for disturbing reading.

Chan identifies two ways in which the ‘stressors’ associated with climate change – increased heat, salt, acidity – can affect plankton. The first is by direct physiological impact. “If organisms find themselves in a stressful environment, then they have to perform more metabolic functions – such as the up-regulation of proteins – just to handle the unpleasant stuff. This means that less energy is available for other things, and in some species, animals simply run out of fuel and die.”

Other plankton species seem more resilient: they survive, but not unchanged. In these species, the ‘sub-lethal’ impacts of stressors act over a longer time-frame, affecting how the planktonic larvae grow. This often results in smaller larvae possessing different morphologies, or body shapes. The new morphology in turn generate a different swimming motions, so that climate change stressors cause both physical and behavioural alterations in the plankton.

Intriguingly, these alterations do not seem, at least on first examination, to be necessarily harmful. In recently published research papers, Chan’s lab reports that the urchin species raised in stressor environments can swim as fast, or even faster, than their normal counterparts. “This is super counter-intuitive,” Chan observes, “Because they are smaller, but they can swim just as well, so what is going on?”

One theory that Chan is working on is that the smaller, more vulnerable, stressed organisms prioritize swimming speed over feeding efficiency because of the increased risk of predation.

Chan’s experimental work is also revealing that climate change stressors produce different effects, not just between different species, but between different populations of the same species. When isolated populations of an organism breed over several generations, some emerge as more resistant than others to stressors. This is a crucial, and encouraging finding, since it offers a possible mechanism for the selection of climate-change survivors among plankton.

Sam Dupont, a close colleague of Chan from the Department of Biological and Environmental Sciences, University of Gothenburg, puts her work into the global perspective of differential species survival:

“Karen Chan has an unusual expertise in the field. She focuses on traits such as larval swimming behavior that are often overlooked despite their critical importance for species dispersal and population sustainability. Different populations of the same species can be adapted to different environments, and so can be more or less sensitive to the changes to come. Karen’s work in understanding how larval behaviors differ in these populations, and how they might be differently impacted by future global changes, is then critical.”

Support for Chan’s conclusions comes from large-scale real-world investigations. One species of purple sea urchin, endemic along the entire Californian coast, experiences significant variations in water acidity. Some locations undergo frequent ‘deep upwellings’, which bring up high concentrations of waste, and therefore CO2, causing lower local water pH. Research by Gretchen Hoffman and colleagues at UC Santa Barbara has shown that local populations exposed to these acidic environments over generations do better under acidic conditions, so that resistance seems to be inherited.

The obvious weakness with evolution over many generations is slowness: climate change, like time and tide, waits for no-one. But various plankton species also demonstrate the shorter-term mechanism of developmental plasticity, whereby organisms adapt to specific local environments within their own lifetimes. In one study, Dawn Vaughn of California State University demonstrated that veliger snail larvae reared in the presence of predators developed smaller shell openings and rounder shells than non-predated populations, and subsequently showed higher survival rates. Ben Miner of Western Washington University has shown that sea urchin larvae reared under conditions of food scarcity develop longer ‘arms’ and smaller stomachs than populations given abundant food: the first group ‘choosing’ a morphology that prioritizes food-gathering over digestion. Such developmental flexibility could be a key plankton survival resource, as Richard Strathmann of the University of Washington confirms: “With climate change, much changes, and plasticity in responses should help.”

Chan is particularly interested in examining species’ adaptation in the local waters of Hong Kong. While most plankton research projects and predictions focus on populations in the open ocean, Chan feels that Hong Kong’s island geography offers a unique study opportunity: “Estuary and coastal locations are in general extraordinarily dynamic, and if you want to look at a super-stressful environment, then Hong Kong is perfect.”

Hong Kong has the usual tidal fluctuations of a coastal environment, and mineral leakage from coastal rocks, together with chemical and temperature fluctuations caused by heavy rainstorms. In addition, its position on the Pearl River estuary means an inflow of fresh water combined with various human pollutants, all of which combine to produce an unstable, multi-stressor environment.

Sam Dupont emphatically supports Chan’s claims for the special character of her research location:

“Hong Kong is a unique place to study global changes. In a way, it can be seen as an extreme environment facing a unique set of local challenges, including pollution. Marine species in Hong Kong waters are already facing several stressors and future warming and acidification may be the last punch leading to extinction of key local species.”

Ironically, one of the organisms which Chan’s lab has chosen for this study happens to appear on many people’s ‘I Wish They Were an Endangered Species’ List. They are bryozoan – a plant-like estuarine/coastal animal which is officially classified as a major nuisance (or ‘marine biofouling’) species. Bryozoan are aggressively invasive creatures, hated by fishermen as they clogs nets, and by sailors as they smother ship hulls. Chan’s key question is whether Hong Kong bryozoan they have become acclimated through enduring the extreme multi-stressor environment, and results currently being written up indicate that they have. Whereas ‘normal’ populations thrive at an open-ocean pH of about 8.1, the Hong Kong-hardened types make nothing of a pH as low as 6.5. “In this much more acidic environment, Hong Kong bryozoan babies grow as well, if not faster, than their open-ocean counterparts do at normal acidity.”

Asked how her research might help preserve species which we do want to save, and which might become endangered, Chan describes a current project in which her lab is investigating the potential of artificial selection to produce commercial edible larvae of two organisms: snails, and local purple urchins, selecting those that survive in low pH environment and raising them through subsequent generations to see if that resilience is inheritable.” The results so far confirm the implications from the California coast urchin data, that resistance to acidity – and probably to other stressors – is inheritable, and can be ‘bred’ in the lab, producing what Chan refers to as ‘pre-exposed’ or ‘pre-adapted’ stressor-resistant populations.

For the future, Chan’s Lab will focus on improving our understanding of local plankton species endemic to Hong Kong. In particular, they wish to investigate the exact mechanisms which underlie variations in resistance between different plankton populations. “We are looking at their physiological and biochemical tools, as well as genetic ones.”

Chan’s final message is mixed. “Yes, climate change and anthropogenic stressors can affect these marine organisms at a critical life-stage: their larvae, their babies. So yes, we can mess up our environment.” However, the future is not all doom and gloom: “These organisms have variability; some are going to be winners, some losers; so we are expecting change, but it’s not like the sea will be empty, just different.”

Dr Karen Chan is the Assistant Professor of Division of Life Science at Hong Kong University of Science and Technology. She received her BSc with first class honors from the University of Hong Kong in Environmental Life Science in 2006. She then moved to Seattle to pursue her MSc and PhD in Oceanography at the University of Washington under the supervision of Dr. Daniel Grunbaum. Her dissertation research focus on the consequences of ocean changes for ecological functions of marine invertebrate larvae. After her PhD, she was funded by the Croucher Foundation and worked at the Woods Hole Oceanographic Institution. Her postdoctoral research focus on fluid-organisms interactions under climate change conditions. 

To view Dr Chan's Croucher profile, please click here.