University of Groningen
Ecology of benthic microalgae Engel, Friederike Gesine
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Orbiting Earth in the spaceship, I saw how beautiful our planet is.
People, let us preserve and increase this beauty, Not destroy it!
Chapter 6
Discussion
Friederike G. Engel
Biodiversity is fundamental for the functioning of this planet (Hooper et al. 2005,
2012, Cardinale et al. 2012) and thus for the survival of humanity. Unfortunately,
we are experiencing a global biodiversity crisis that could lead to mass extinction
rate and magnitude within the next centuries (Barnosky et al. 2011, IPCC 2014).
Surprisingly, the global biodiversity crisis does not appear to lead to species loss
on the local scale (Vellend et al. 2013, Dornelas et al. 2014, Elahi et al. 2015).
This is probably due to range expansions and invasions that bring species into
novel territories (Parmesan and Yohe 2003, Wonham and Carlton 2005, Parmesan
2006, Byrnes et al. 2007, Dornelas et al. 2014). However, changes in species
composition, including dominance patterns, are observed on global and local
scales (Hillebrand et al. 2008, 2017, Magurran 2016, Jones et al. 2017). These
changes most likely influence ecosystem functions in ways comparable to the
complete loss of species. Therefore, it is important to consider both species
richness and species composition when studying the consequences of biodiversity
loss. Furthermore, today there is a general call to increase our effort to study
biodiversity effects on ecosystem functioning in more natural settings, to promote
our understanding of biodiversity effects in real-world ecosystems (Gamfeldt et
al. 2008, Duffy 2009, Brose and Hillebrand 2016). In practice this means making
experimental set-ups more complex by for example incorporating heterogeneity
and natural processes, and thus make them more ecologically relevant. A key
improvement needed to promote realism in biodiversity ecosystem function
research is to include dispersal in experimental set-ups, to be able to study both
local and regional processes. In addition, using species assemblages with natural
compositions gives more informative results for real ecosystems than using
artificially created species assemblages.
DISCUSSION
Unicellular algae are an integral part of the functioning of marine ecosystems, as
they build the base of many food webs and turn carbon dioxide into oxygen via
photosynthesis. Notably, the pelagic unicellular algae (phytoplankton) contribute
roughly 50% of global primary production (Field et al. 1998), to which the benthic
microalgae additionally contribute. In intertidal areas, such as the Wadden Sea,
benthic microalgae are dominated by diatoms and their contribution to total
primary production can exceed that of the phytoplankton in overlying waters
(Admiraal et al. 1984, Underwood and Kromkamp 1999). Thus, in these areas,
they are the main source of primary production and fuel intertidal food webs.
Benthic microalgae ecology is complex and many scientists have spent entire
careers investigating these organisms. These studies have revealed that species
composition, abundance, and biomass production of benthic microalgae on
intertidal flats is determined by a multitude of factors, including temperature,
nutrient availability, grazing, salinity, inundation, wave action, and sediment
grain size (MacIntyre et al. 1996, Underwood and Kromkamp 1999, Sahan et al.
2007, Weerman et al. 2011a, 2011b, Scholz and Liebezeit 2012). Yet, there is still
a lack of information on general ecological principals in benthic microalgae,
because few ecologists use these organisms as model systems in their
experiments. Due to their importance in coastal areas and their lifestyle
characteristics (e.g. short generation times, ability to reposition themselves
actively), however, benthic microalgae, especially diatoms, are ideal study
organisms for ecological laboratory and field experiments.
For the work in this thesis, I conducted field and laboratory experiments to
investigate the impacts of different climate change stressors on biodiversity and
ecosystem functioning of benthic microalgae. In my experiments, I considered
multiple spatial (i.e. local and regional communities via dispersal) and temporal
(i.e. multiple sampling points) scales, as well as multiple components of a
community (i.e. autotrophic microalgae and heterotrophic bacteria), used natural
community assemblages, and exposed the communities to natural stressors (i.e.
warming and mechanical disturbance). With my research, I aimed to shed light on
the following general questions: (1) Do potential climate change stressors
influence biodiversity and ecosystem functioning of benthic microalgae? (2)
Which ecological processes determine the response of microalgae to stressors
throughout community succession? (3) Does increasing the realism of ecological
experiments alter the response of benthic microalgae to simulated climate change
stressors? On the next pages, I summarize the main findings of my thesis.
CHAPTER 6
A. Ecosystem engineers promote benthic microalgae, but the strength of the
effect depends on scale.
In Chapter 2, I described results of a study that combined a field experiment with
transect measurements on the intertidal flat. I found that mussel beds increase
biomass production and primary productivity of benthic microalgae living in the
proximity of these structures (Fig. 6.1). In addition, the results showed that scale
is important for this function: large, established mussel beds that have existed for
multiple years had a greater positive effect on benthic microalgae than small-scale
plots that existed for only a few months. Thus, both spatial and temporal scales
are important for the facilitating effect of ecosystem engineers on primary
producers.
Fig. 6.1 Ecosystem engineers promote benthic microalgae biomass and productivity
(Chapter 2). A natural mussel bed promotes microalgae biomass and productivity in its vicinity. The addition of mussels to small-scale experimental plots also promotes microalgae biomass, however, the effect is smaller than that of the natural mussel bed.
These results exemplify the importance of ecosystem engineers for the
functioning of intertidal food webs and productivity of benthic microalgae. With
their physical structure and biological provisioning, ecosystem engineers strongly
influence the food-web dynamics and can greatly increase primary production in
intertidal areas.
Furthermore, the results have implications for reef restoration and protection, as
they demonstrate that reef size matters for the facilitation effect of ecosystem
engineers. In real ecosystems, this means that it may be more beneficial to restore
or protect a larger cohesive reef in one location, compared to several smaller ones
in multiple locations.
DISCUSSION
B. The relative importance of local community composition and dispersal for
biodiversity and ecosystem functioning depends on successional time.
In Chapter 3, I observed that the importance of different factors influencing
microalgae diversity, biomass, and the ratio of bacteria to microalgae change with
successional time. In a laboratory experiment, I discovered that initial local
community composition was most important in the beginning of successional
time, whereas dispersal became more important towards the end of the experiment
(Fig. 6.2).
Fig. 6.2 The effect size of initial community composition (dark dotted line) and dispersal
(light solid line) changes with successional time (Chapter 3). In the beginning of community succession, initial species composition has the strongest effect size, but by the end of community succession, dispersal has the strongest effect size.
This experiment shows that the temporal scale is important in ecological studies,
because different processes dominate at different times throughout community
succession. By only measuring the responses at one timepoint, important
information can be missed and results can be misleading. Of course, like in all
experiments, usually there is a logistic limitation for obtaining more time
replicates. If it is not possible to take measurements at multiple timepoints, we
should at least be aware that these results only capture a snap shot of this
community and should not be generalized. Creating experiments that represent
real-world ecosystems better includes being conscious about community
succession and choosing sampling times deliberately.
CHAPTER 6
C. Dispersal maintains ecosystem functioning of microalgae by preventing
bacterial dominance.
In Chapter 3, I also discovered that dispersal can maintain ecosystem functioning
in a metacommunity by preventing heterotrophic bacteria from gaining
competitive advantage over microalgae. Dispersal supplied a strong microalgae
competitor to all local patches which mitigated increasing bacterial superiority
and maintained high algae biomass. At the same time, within microalgae,
dispersal decreased diversity by spreading the superior microalgae species into all
local patches where it became dominant (Fig. 6.3).
These results exemplify the importance of connectivity (i.e. dispersal) for
community functioning. Isolated algae communities were quickly taken over by
bacteria and had reduced ecosystem functioning. Whereas with dispersal, a
superior competitor could colonize all local patches, successfully compete with
the bacteria and maintain ecosystem functioning. This has implications for
conservation: it is important to protect biodiversity and connected habitats to
ensure that species best suited to certain conditions can reach the habitat.
The results also show that to mechanistically understand community structure and
functioning, we need to look at how multiple components of communities are
affected by the community structuring drivers (in this case dispersal) and how this
in turn changes interactions among them. In this case, I had a simplified system
of only two competing groups (i.e. autotrophic microalgae and heterotrophic
bacteria), but in nature, there will be a multitude more of interactions among the
levels in a community that can influence overall ecosystem functioning, which
need to be considered in ecological experiments.
DISCUSSION
Fig. 6.3 Dispersal hinders bacteria from outcompeting the microalgae and thus
maintains ecosystem functioning of the microalgae (Chapter 3). Within microalgae, dispersal increases dominance of a superior species that got spread into all local patches. However, between microalgae and bacteria, dispersal weakens the dominance of bacteria by spreading a strong microalgae competitor and thus prevents bacterial dominance.
D. Regional warming increases species turnover, but the effect is only visible
when considering relevant scales.
In Chapter 4, I described a laboratory experiment with benthic microalgae
metacommunities, in which I found that warming increases regional species
turnover. One heat-tolerant species was promoted by warming and then spread by
dispersal, until it was dominant in all local communities within a metacommunity.
The effects on turnover on the local scale strongly depended on initial community
composition and were not uniform within the different local communities.
This experiment illustrates the need for considering multiple spatial scales and
connectivity when analyzing the responses of ecosystems to environmental
factors (here related to climate change). Due to opposing responses in different
local patches, there might not be a noticeable overall effect on smaller scales, but
when looking at patches in the metacommunity context, disturbance events such
as a heatwave might have strong effects. Analyzing both local and regional
community processes in ecological experiments creates more realistic scenarios
that are closer to real-world ecosystems compared to experiments that only
consider local patches of habitats.
CHAPTER 6
E. Decreased biodiversity in response to warming may not be reflected by
species loss.
The results of Chapter 4, also provide an example of how the response of species
diversity and species richness to changing conditions can be fundamentally
decoupled on ecological time scales. In the experiment both warming and
dispersal destabilized community composition and decreased species diversity,
although the number of species in the metacommunity was not decreased, even
after ca 15 generations (Fig. 6.4).
Fig. 6.4 Warming and dispersal lead to the loss of regional biodiversity, but this is not
reflected in species richness (Chapter 4). In the isolated, non-heated metacommunity, dispersal-limitation leads to a decrease in species richness (dark gray solid line) over time, but Shannon diversity (light gray dotted line) remains constant. With dispersal and warming, Shannon diversity in the metacommunity decreases due to spread and increasing dominance of a heat-tolerant species, but species richness remains constant.
This has important implications for experimental ecology and conservation
biology. Since negative effects on biodiversity can manifest themselves in a
multitude of ways, it is not sufficient to look at species richness when surveying
ecosystems. We have to consider both the number of species and changes in the
relative abundance of species when discussing the consequences of biodiversity
loss for ecosystems. Experiments that run only for a relatively short time might
not capture negative effects on species richness, because it usually takes much
longer to actually see changes in richness compared to changes in dominance
patterns. The solution to this problem is to analyze changes in the relative
abundance of species in addition to species richness.
DISCUSSION
F. Initial species composition determines the effect of disturbance on
ecosystem functioning.
In Chapter 5, I presented the results of a
laboratory experiment in which I exposed
locally dissimilar benthic microalgae
communities
to
different
levels
of
disturbance on the metacommunity scale.
In this experiment I discovered that the
response of ecosystem functioning in the
face of disturbance depends on initial
species composition (Fig. 6.5). Initial
species
composition
varied
due
to
differences in habitat conditions, among
them different levels of hydrodynamic
stress, organic matter content, and sediment
grain size. The results suggest that previous
exposure of a local assemblage to
hydrodynamic
stress
weakened
the
negative effect of disturbance on biomass,
mediated by the selected-for community
composition.
These results illustrate that species
identities matter and again highlight the
importance to not only focus on species
richness, but also consider other aspects of biodiversity when discussing
biodiversity loss. Communities that consist of native species adapt to local
conditions and so are, for example, accustomed to more frequent disturbances of
the sediment. With future disturbances, the community as a whole will probably
have higher resistance and resilience compared to previously sheltered
communities, because their response diversity is geared towards disturbances
already.
Fig. 6.5 Initial species composition
determines the effect of disturbance on biomass (Chapter 5).
Communities that were previously exposed to higher hydrodynamic stress have a higher biomass after repeated disturbance events compared to the previously more sheltered community.
CHAPTER 6
G. Dispersal does not mitigate negative effects of disturbance on ecosystem
functioning.
In Chapter 5, I did not find support for the
hypothesis that communities connected by
dispersal are better able to cope with
regional
disturbances
than
isolated
communities. There was no significant
difference between biomass in the dispersal
and no-dispersal communities (Fig. 6.6).
These results indicate that dispersal (i.e.
habitat connectivity) may not be a default
solution for maintaining biodiversity in the
face
of
system-wide
disturbances.
Dispersal can potentially be very beneficial
in situations where a local disturbance does
not affect all patches. However, when a
global disturbance event takes place, like in
this study, dispersal may not have a
positive effect on ecosystem functioning.
This is important for conservation efforts
that focus on connectivity or preventing
habitat fragmentation. The quality of the
different local patches connected in metacommunities is crucial. Thus, not only
do we have to make sure that we protect separate habitats that species can disperse
into, but also that after a disturbance event, there are sufficient patches that were
not affected by the disturbance so that species can migrate from undisturbed
patches into the disturbed patches. For global disturbances, such as sea-level rise
or global warming, this is nearly impossible. For more localized disturbances such
as severe storms or precipitation events, this is more attainable.
Fig. 6.6 Dispersal does not
mitigate negative impacts of disturbance in a metacommunity (Chapter 5). There is no difference in biomass of the metacommunities connected by dispersal and the isolated communities.
DISCUSSION
Concluding Remarks
In this thesis, I demonstrate that it is important to make ecological experiments
more realistic. Simplifying too much leads to skewed results that cannot be
extrapolated to real-world ecosystems. In my experiments, I saw differences in
results depending on the successional time the samples were taken, the scale that
was analyzed (local vs. regional, large vs. small, long-term vs. short-term, within
microalgae vs. microalgae-bacteria), and the measure of biodiversity considered.
Simplified set-ups are important to detect fundamental principles and confirm
theories, but they should be extrapolated to bigger scales cautiously and thus have
limited applicability for real-world problems such as the conservation of actual
habitats. As a consequence, experimental ecologists should persistently increase
the realism of their experiments. This includes turning towards natural
assemblages of species instead of single species or artificial assemblages;
studying multiple components of a community (i.e. autotrophs and heterotrophs);
considering multiple spatial scales, which can be achieved by using dispersal in
the experimental set-up; measuring multiple parts of biodiversity to capture
changes in both species richness and species composition; and measuring
responses at multiple time points throughout community succession, as the
importance of different factors might change with time. Finally, we need to a
larger extent “field-test” laboratory results by field manipulations and natural
sampling campaigns before making conclusions about generality and relevance,
and before making recommendations towards practical conservation. Trade-offs
are inevitable, but constantly striving towards re-creating realistic scenarios will
advance research in experimental ecology.
CHAPTER 6
Personal Reflection
Every experiment matters, just as every piece added to a puzzle clarifies the
finished picture. The more hands-on data we add to the continuously growing
scientific literature on ecological principals, the better we will be able to
understand, predict, and counteract changes in nature. This will be increasingly
important, as ecosystems on the planet are changing with an unprecedented speed.
Habitats are destroyed, novel habitats are created. Species need to expand their
ranges, populations need to adapt to altered conditions, and individuals will have
to survive new extremes. The evolutionary race is becoming more and more
skewed and fewer species will have a chance of winning it. Even though nature is
difficult to predict and nearly impossible to tame, with experiments we can
increase our understanding of processes and prevent some negative events from
taking place. Cooperation between different disciplines and using multiple
methodological approaches simultaneously become crucial, as all humans only
have this one planet to live on (as of yet). Conclusions derived from experimental
studies and collaborations are not going to solve all the world’s problems, but they
might just tip the scale in the right direction.
Science.
Science is survival.
Science is worth nothing without integrity.
Protect scientific integrity, and humanity has a chance to survive.
Survive.
Freedom of thought is best promoted by the gradual illumination of men’s minds which follows from the advance of science.
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