Herbivores compensate for nutrient pollution

Photo courtesy of the NOAA photo library (www.photolib.noaa.gov)
Photographer: Paige Gill.

This post is a guest blog by one of my (now ex-) Ph.D. students, Dr Chloe McSkimming. Chloe has been working on what drives decline in seagrass systems and how we may be able to help stop the decline. The work described below is from one of her recent papers in the Journal of Experimental Marine Biology and Ecology.

Human activities continue to challenge the capability of ecosystems to absorb disturbances, yet many systems that face substantial human pressure remain stable, resisting change. Over the past several decades, ecologists have extensively studied resilience – the ability of an ecosystem to bounce-back – but we really don’t understand resistance, or the ability to not change. There is recent evidence that in marine systems this resistance may be in part due to biological compensatory mechanisms – basically processes that can counter disturbances which cause change. Therefore, understanding how these mechanisms allow systems to resist change to a degraded state is essential for improving our current knowledge of habitat stability.

In coastal systems, change in resource availability, particularly the increase in available nutrients via land-based runoff, favours the growth of weedy species which can displace highly productive, slower-growing species. In seagrass systems, nutrient inputs increase the growth of algae that overgrow seagrass, significantly reducing the amount of light available to the seagrass themselves, and ultimately leading to seagrass death. Small herbivores are important consumers which may provide a compensatory mechanism in these systems by eating these fast-growing algae, potentially increasing the survival of seagrass under nutrient pollution (also demonstrated for other benthic systems by myself and one of my colleagues Laura Falkenberg).

In this present study, we increased nutrient concentrations and altered herbivore abundance in a seagrass meadow to test whether this compensation does exist; that is, does nutrient pollution stimulate herbivores to increase feeding to counter the increased growth of algae?

As expected, nutrients increased the growth of algae so that they started to smother the seagrass. However, this effect was only present when herbivore abundance was reduced. When the herbivores were present, however, they reduced the effects of nutrient pollution by reducing the amount of algae on seagrass leaves. Interestingly, the abundance of herbivores did not increase, meaning that the increased consumption of algae was due to an increase in how much individuals were eating.

We still have a long way to go to understand compensatory effects in ecosystems. However, these results suggest that in some situations natural populations of herbivores may help to reduce the effects of nutrient pollution in seagrass systems by consuming the additional growth of weedy species. Herbivores are therefore an important component in the management of nutrient addition in coastal systems. BUT, it is also essential to remember that there is still a global decline of seagrasses driven by nutrient pollution, meaning that such compensatory mechanisms do have limits and ultimately the only way to stop the negative effects of nutrient pollution is to stop nutrient pollution!

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Can nature compensate for human impacts?

Algal turfs dominating under acidified conditions at cold-water (temperate) CO2 vents, which we use at “natural experiments” to try and understand the effects of carbon emissions on our oceans. You can just see the fronds of a solitary kelp plant in the right of the photo, otherwise they are rare at the site (when they should be 8 – 10 plants per metre!). This is a system that has been pushed past its ability to resist or compensate for human activities.

One thing that humans are really good at is having an impact on the environment through their activities. The problem is that we generally don’t realise that we’re having an impact until something changes in a drastic way. We talk about things called phase-shifts, where the environment changes from one “phase” to another. Good (and unfortunately common) examples are the loss of kelp forests for bare reef, seagrass meadows for bare sand, or coral reefs for algal habitats. In all of these cases, the environment has been degraded to the point where it no longer functions as it should, meaning that biodiversity and productivity are massively reduced.

There are two questions to ask here, (1) why don’t we see these phase-shifts coming, and (2) does nature have any resistance to them? A new paper by one of my PhD students, Giulia Ghedini, shows that nature may actually try to resist human-caused stressors (such as increased nutrient pollution, ocean acidification, warming) by increasing the strength of compensation. In this case, Giulia found that the compounding effects of multiple disturbances increasingly promoted the expansion of weedy algal turfs (which replace kelp forests), but that this response was countered by a proportional increase in grazing of those same turfs by gastropods. This is a natural compensatory mechanism, but it has limits.

What does this mean for our understanding of phase-shifts? First, it means that nature is stronger at resisting than we realised. BUT, because it is extremely difficult to either see or quantify this resistance we generally don’t realise it is happening…. until it stops. Then, once we push the systems past their ability to compensate for the increased pressure we place on them we see a sudden shift. It’s like watching a duck on a river – it may look extremely calm on the surface, seemingly stationary, but underneath it is paddling extremely hard. At some point the current strengthens too much and it can’t paddle harder and so, seemingly suddenly, the duck begins to float down the river.

Unfortunately, when put together, this means that more systems may be more stressed than we realise, and the only way to stop detrimental phase-shifts is to take the conservative approach and start to reduce our impacts on these systems. For example, we know that nutrient pollution, carbon emissions, overfishing and many other activities have damaged marine ecosystems, why not begin to reduce our impacts before we add more systems to the list of those we didn’t realise were at breaking point?

Declining productivity

We’ve all heard about productivity, but I suspect that the only context most people have heard the term used in is about the productivity of the workplace, or perhaps the economy.

Phytoplankton may be tiny but they are the base for much of what we see and use in the ocean!

Economists and governments are certainly concerned with productivity. But, we should all be concerned with productivity – of the oceans.
As we burn more fossil fuels and pump carbon dioxide into the atmosphere we are making astonishing changes to the global climate systems. Not the least of these is the addition of billions of tons of CO2 to the surface waters of the ocean. What does this mean for productivity of the oceans? A cursory analysis would lead you to believe that because many photosynthetic plants and algae can use in photosynthesis that productivity would increase. As the oceans produce about 50% of the oxygen we breathe and provide us with a substantial amount of food and other resources you may think that this would be a good thing. Unfortunately, the evidence is stacking up that productivity won’t increase, and in fact it is likely to decrease.
I have previously posted on work by my research group where we experimentally project that ecosystem productivity in temperate waters is likely to decrease because of an indirect effect whereby highly productive kelp forests will be replaced by lower productivity systems dominated by algal mats. Of potentially greater concern, however, is the emerging data from open-ocean pelagic systems. Recent work by Professor Kunshan Gao from the State Key Laboratory of Marine Environmental Science, Xiamen University, has demonstrated that the projected concentrations of CO2 in our oceans by 2050 (assuming we don’t suddenly decide to stop burning carbon!) will actually cause a decrease in the productivity of phytoplankton. And, the situation was even worse when the phytoplankton were exposed to increased light intensity, which will happen as the upper ocean that they live in shoals towards the surface. This result was initially surprising given that both light and CO2 are required for photosynthesis. In combination and high enough concentrations, however, they inhibit photosynthesis, leading to a decline in productivity.

What does all this mean? The changes that are happening in the ocean because of changes to our climatic systems, including (but not limited to) increased availability of CO2, ocean acidification and warming are going to be with for a very long time. The resources that we currently expect from the oceans will change, many declining. How do we stop this? By being a little smart – let’s stop burning carbon for fuel!

Don’t forget to remember the past

I have recently returned from the 10^th International Temperate Reefs Symposium in Perth. It was great to spend a week talking good science

Seagrass may increase their productivity in the future as they use CO2 for photosynthesis.
Photo: Owen Burnell

with a vibrant group of great scientists. There was an array of talks from classical marine ecology (which is great to see!) to novel modelling approaches and plenty of discussion of human impacts in marine systems. In the rare moments of quiet since my return I’ve been thinking about the main message that I took away from the meeting, and it’s this: anthropogenic climate change may be new to the planet, but we were studying the effects of human activities on ecosystems for several decades before we even realised that climate change was happening. So why is it that we seem to have abandoned ecology in our race to understand climate change?

While I was writing my talk for the conference I realised that, in general, research into the effects of climate change in marine ecosystems has been hampered by not looking at the literature on other human impacts. For example, there is a rich and abundant literature on how excess nutrient loads degrade ecosystems and change their structure and function. Yet, it is only recently that we have realised that CO₂ is a “nutrient” or resource in marine systems. This seems logical; after all, plants use inorganic carbon for photosynthesis.  However, the story isn’t that simple, with different algae and seagrasses using different forms of carbon for photosynthesis. Even more confusing is that it looks like the “weedy” species will benefit by switching to the most abundant source of carbon and start to dominate ecosystems (see some of my papers and Harley et al. for the ecosystem effects and Raven & Hurd for the physiological aspects)! But I digress….

The point is that for some reason we don’t seem to draw on this older literature for the general principles of what we may expect to see as CO₂ concentrations increase in the oceans. We’re starting to catch up, but the lost time is frustrating – let’s not make the mistakes of past generations but rather learn by them.

Digital library links for: Connell & Russell 2010

Mediation of global change by local biotic and abiotic interactions

This post is basically a short synopsis of the work done by one of my (now ex-) Ph.D. students, Dr Laura Falkenberg. Laura’s work has turned much of what we thought we knew about the effect of increased CO₂ and nutrients on its head; we found synergies where we didn’t expect them (reviewed in a book chapter) and system resilience and resistance to change beyond what we hoped (via strong competitive interaction and trophic links; published in Oecologia, PLoS One and Marine Ecology Progress Series). Laura has certainly helped us look at things in new ways and given us hope that in marine systems where synergies between stressors exist that management of local conditions could potentially buy us some time in mitigating climate change (e.g. reducing nutrient flows into the marine environment, in Journal of Applied Ecology).

Ph.D. thesis: Mediation of global change by local biotic and abiotic interactions
by Dr Laura Falkenberg.

Throughout my Ph.D., I assessed the conceptual model that while cross-scale abiotic stressors can combine to synergistically favour shifts in marine habitats from kelp forests to mats of turfing algae, management of local conditions can counter this change. My experimental manipulations found broad support for the hypotheses that; 1) cross-scale factors (i.e. local and global) can have interactive effects which increase the probability of expansion of turfs but not kelp and, 2) management of local conditions (e.g. maintaining intact forests, limiting nutrient enrichment) can dampen the effects of global change (e.g. forecasted carbon dioxide). I published the results from my thesis in four papers. In the first, I showed that experimental enrichment of CO₂ and nutrients influence the biomass accumulation of turf and kelp differently, with turf responding positively to enrichment of both resources while kelp responded to enrichment of nutrients but not CO₂. Given that such direct responses could be mediated by interactions with other taxa, in the second paper I considered a key competitive interaction and revealed that the presence of kelp can inhibit the synergistic positive effect of resource enrichment (i.e. CO₂ and nutrients) on their turf competitors. Similarly, in the third paper I highlighted the importance of herbivory by showing that under enriched CO₂ conditions rates of this process were increased to counter the expansion of turfs. Finally, in the fourth paper, I considered a scenario in which these biotic controls were absent and identified that where multiple resources had been enriched and prompted a synergistic response (i.e. the expansion of turf where CO₂ and nutrients are modified), subsequent reduction of the locally-determined factor alone (i.e. nutrients) substantially slowed further expansion of turf algae, but that the legacy of nutrient enrichment was not entirely eradicated. Together, these results represent progress in ecological tests of hypotheses regarding global climate change as they incorporate comprehensive sets of abiotic and biotic community drivers.

You can access all of Laura’s publications from the University of Adelaide’s digital library, or email her for a copy.

Recovery of seagrass from overgrazing depends on species morphology.

Above: A meadow of seagrass (Amphibolis antarctica) that has been heavily grazed by sea-urchins to the point where only dead shoots and detritus remain. Below: A moderately dense meadow of Posidonia sp. with aggregations of sea-urchins (Amblypneustes pallidus). This genus of seagrass appears to have a much greater capacity to recover from grazing than Amphibolis antarctica. Photo credits: Andrew Irving (Above), Owen Burnell (Below)

Following on from my last post on how sea-urchins alter how much they eat in response to nutrients and CO₂, here Owen Burnell describes his latest paper (in as many months!) that shows why Amphibolis antarctica and other morphologically similar species of seagrass may be so susceptible to grazing.

Sea urchins are important marine invertebrates, which in many parts of the world can shape sub-tidal habitats via their grazing. In South Australian seagrass meadows the short-spined sea urchin Amblypneustes pallidus generally occurs in low densities, however, population increases of the species have recently been documented by researchers at The University of Adelaide.

It was observed that the grazing activity of these urchins was impacting seagrass meadows, in particular the species Amphibolis antarctica, when compared with adjacent Posidonia spp.  By manipulating urchin density to measure seagrass loss and then simulating urchin grazing to study seagrass recovery, we found that while urchins grazed equally upon both seagrass species, Posidonia sinuosa recovered much faster from simulated grazing than Amphibolis antarctica. It appears the different morphology of these two seagrass species, in particular the meristem location (or centre of growth) of Amphibolis spp., which is elevated within the canopy and thus exposed to grazers, is likely to be the cause of these asymmetric grazing impacts. In essence, if the urchins eat the meristem that seagrasses grow from they don’t recover as quickly!

While sea-urchins are by no means a rampant force destroying local seagrass meadows, population expansions such as these are important to document, particularly if they have deep seated connections with changing trophic interactions or urchin fecundity. In many marine systems worldwide population expansion of macro-grazers such as urchins can be linked to over-exploitation of their predators (e.g. fish or crustaceans, or before their protection, sea otters!) or changes to temperature that affect their reproduction and metabolism.

For more information, check out the abstract (below), journal website (subscription required), or link to the full manuscript

The persistence of seagrass meadows reflects variation in factors that influence their productivity and consumption. Sea urchins (Amblypneustes pallidus) can over-graze seagrass (Amphibolis antarctica) to create sparse meadows in South Australia, but this effect is not observed in adjacent Posidonia sinuosa meadows despite greater densities of inhabiting urchins. To test the effect of urchin grazing on seagrass biomass, we elevated the density of urchins in meadows of A. antarctica and P. sinuosa and quantified seagrass decline. Urchins removed similar amounts of biomass from both seagrass species, but the loss of leaf meristems was 11-times greater in A. antarctica than P. sinuosa. In a second experiment to assess the recovery of seagrass, we simulated urchin grazing by clipping seagrass to mimic impacts measured in the first experiment, as well as completely removing all above ground biomass in one treatment. Following simulated grazing, P. sinuosa showed a rapid trajectory toward recovery, while A. antarctica meadows continued to decline relative to control treatments. While both A. antarctica and P. sinuosa were susceptible to heavy grazing loss, consumption of the exposed meristems of A. antarctica appears to reduce its capacity to recover, which may increase its vulnerability to long-term habitat phase-shifts and associated cascading ecosystem changes.

Eutrophication offsets sea urchin grazing on seagrass caused by warming and OA

Amblypneustes pallidus in a Posodonia seagrass meadow.
Photo: Owen Burnell

The title to this blog seems a bit counterintuitive, almost like eutrophication is a good thing. Don’t believe that for a second! In a recently published paper, Owen Burnell of the University of Adelaide presents some interesting data on the interactions between eutrophication (an all too common local stressor), ocean acidification and warming (both increasingly alarming stressors of global origin). As I keep discovering, interactions between these stressors never seem to turn out the way we expect:

The accumulation of atmospheric [CO₂] continues to warm and acidify oceans concomitant with local disturbances, such as eutrophication. These changes can modify plant– herbivore grazing interactions by affecting the physiology of grazers and by altering the nutritional value of plants. However, such environmental changes are often studied in isolation, providing little understanding of their combined effects. We tested how ocean warming and acidification affect the per capita grazing by the sea urchin Amblypneustes pallidus on the seagrass Amphibolis antarctica and how such effects may differ between ambient and eutrophic nutrient conditions. Consistent with metabolic theory, grazing increased with warming, but in contrast to our expectations, acidification also increased grazing. While nutrient enrichment reduced grazing, it did not fully counterbalance the increase associated with warming and acidification. Collectively, these results suggest that ocean warming and acidification may combine to strengthen top-down pressure by herbivores. Localised nutrient enrichment could ameliorate some of the increased per capita grazing effect caused by warming and acidification, provided other common negative effects of eutrophication on seagrass, including overgrowth by epiphytes and herbivore aggregation, are not overwhelming. There is value in assessing how global and local environmental change will combine, often in non-intuitive ways, to modify biological interactions that shape habitats.

Digital library

Disrupting synergies – making things not so bad.

I’ve posted on synergies between environmental stressors (what most people think of as pollution) before. Basically, a synergy is when the impact of the two stressors, say increased CO2 nd nutrients, is greater than the sum of their individual impacts. Once you recognise that synergies can occur, and are often much worse than we predict, the next question is can we do anything to stop them? The short answer is in most cases yes.

The way that synergies work means that, theoretically, if you remove one of the stressors then the “extra” impact should also be removed. In essence, if a synergy is 1 + 1 = 5, then removing 1 means that 1 + 0 = 1. When you’re talking about impacts to ecosystems that are essential to our GDP and way of life (not to mention that they have intrinsic value anyway) that is a really big consideration.

One of my Ph.D. students has just published a rather elegant study demonstrating it is possible to disrupt a synergy between CO2 and nutrients that has the potential to cause the loss of our kelp forest ecosystems. Basically, where CO2 and nutrients cause the synergistic growth of “weedy” species of algae you can remove the nutrients and remove the synergy. There is, however, a caveat. If you wait to remove the nutrients from the system then a large part of the impact will remain – things won’t go back to normal.

The thing that I like most about this outcome is that it provides useful information to the people who manage our coastal waters. If you are concerned that increasing concentrations of CO2 will have a negative impact in areas around major population centres then recycling and redirecting treated waste water away from the ocean, such as into industry or agriculture, can increase the resilience of marine systems. But, timing matters. Sooner is better.

A systems perspective of the future

Experiments show that some clownfish may not be able to smell their predators in the future

To understand how complex ecosystems function, and how things will change if we push them too hard (and we’re constantly pushing!), we humans need to break them down into simple parts. I’m not going to tell you that we shouldn’t do this, because we need to start somewhere, and I’ve certainly done it myself. Where we go wrong, however, is by not putting the parts back together again to try and understand how the entire system may work, ultimately giving us a very simple view of how the world works. But, every now and then we are reminded in stunning detail how failing to build up again will provide us with the wrong information.

My research group recently had one of these stunning moments when we were visited by Prof. Phil Munday from James Cook University. His research is primarily concerned with how ocean acidification will impact on fish and their various roles in the functioning of ecosystems. Basically, he shattered our thoughts about ocean acidification by teaching us that 1 + 1 does not equal 2!

In an elegant series of experiments, Phil’s research group has shown that if you look at the separate responses of predatory fish and their prey to ocean acidification you may not accurately predict the outcomes. For example, under near-future ocean acidification, clownfish (Amphiprion percula) are unable to recognise the smell of their predators. Even worse, some species of fish became almost suicidal, being attracted to the smell of their predator!

If you were to take this on face value you would think that these results mean that small fish are going to have increased mortality under future ocean conditions. However, Phil has shown that it’s not that straight forward because when predatory fish are also exposed to ocean acidification their prey preference can change; preferred prey under current conditions are the less preferred prey under future conditions.

What does this tell us? Apart from the fact that some fish are going to get lucky, I think the big point here is that we cannot simply add up the results of a number of simple experiments looking at individual system components and identify what will happen to systems overall. Just like unexpected synergies among different stressors, we can’t assume that adding up the components will be enough. It’s time to take a more system-oriented approach where we can!

Common synergies

Algal turfs (brown fuzzy stuff) are overgrowing the hard corals at high CO2 concentrations near volcanic vents – a good “natural” experiment. Note also that the seagrass (green, long leaves) are also doing well – a subject for another post.

We frequently hear about “climate change” in the media these days. How could you avoid it? If you do a search of the scientific literature there are thousands of publications a year on the topic. When thinking about the worlds oceans, the most common things that we hear about are ocean warming or ocean acidification (aka. the “evil twin” of warming). Do you notice somthing about this statement? We hear about warming OR acidification. But is this a realistic scenario?

We as scientists commonly break things down into their components and try to understand them one at a time. This is understandable, because the best way to comprehend the functioning of amazingly complex systems is to break them down their component parts and then put them back together again. In this case, however, we are just starting to understand that by breaking things down to individual conditions, either temperature or acidification, we may be missing the most important part of the study. My research group started to realise this in 2009 when we discovered that, when increased in combination, carbon dioxide and nutrients had a massive effect on the growth of “weedy” species of algae which can help to maintain the loss of kelp forests (download the paper here). In hindsight, this result should not be so surprising – both carbon and nitrogen are resources which the algae use to grow. Isn’t hindsight a wonderful thing?

What was surprising is that when carbon dioxide was elevated in the absence of nutrients these algae didn’t respond by grow faster. In fact, they didn’t respond at all to the increased availability of carbon. This means that CO2 and nutrients cause a synergistic response in these algae – where the response to the combined conditions is greater than the sum of responses to the individual conditions (see here for a good review on the topic).

What now worries us is that increasing availability of carbon in the oceans will happen with ocean warming – these are not either/or conditions. Indeed, the first warning shots were fired when we discovered that these same “weedy” turf algae showed the same synergistic growth in response to combined CO2 and warming (see our results published here). We can do something about nutrient pollution (something I will post on in the near future), but CO2 and warming are inherently linked. I think it is time to not talk about warming or acidification but rather to discuss them in tandem.