Discussion
Perturbation of the pond ecosystems with nutrients evoked strong
responses in all ponds, which were dependent on the presence of
foundation species and, in some cases, their co-occurrence. As expected,
all nutrient pulses led to strong increases in phytoplankton abundances
across all treatment combination, which, at first, was mediated by the
presence of either Myriophyllum or mussels in the single species
treatment. However, when both Myriophyllum and Dreissenawere present within a pond, nutrient additions led to a contrasting
pattern: phytoplankton biomass in these ponds increased stronger than in
the presence of a single species or when none of the two species were
present. These patterns suggest strong non-additive interactions between
macrophytes and mussels that affected phytoplankton biomass during and
following the disturbance periods.
Mediation of phytoplankton blooms
under increased nutrient loading by either macrophytes or mussels alone
was expected, and is in agreement with a large body of previous
theoretical and empirical work
(van Neset al. 2007; Iacarella et al. 2018; Yamamichi et
al. 2018). Macrophytes can keep phytoplankton biomass in the water
column at lower levels compared to ecosystems that lack macrophytes.
Such control of phytoplankton biomass by macrophytes is often linked to
their competitive relationship with phytoplankton for nutrients and
light (Scheffer et
al. 1993) or the production of allelopathic substances that can
inhibit phytoplankton growth
(Korner & Nicklisch
2002; Hilt & Gross 2008), especially of some cyanobacteria
(Nakai et al.2001, 2012). However, these mechanisms are only effective below the
“critical turbidity” threshold
(Scheffer et al.1993), above which light limitation prohibits macrophytes growth and
can lead to macrophyte die off, which marks the transition to a turbid
water state
(Schefferet al. 1993; van Nes et al. 2007; Kéfi et al. 2016;
Yamamichi et al. 2018). In our experiment, macrophytes died out
and did not re-establish after the final pulse of the first nutrient
addition (October 10th 2016) until the following spring, which we
confirmed by visual inspection of all ponds in March 2017. Therefore the
observed differences between treatments with and withoutMyriophyllum can only be explained by the legacy of their prior
impact throughout the summer and fall. Macrophytes also affected the
dynamics of dissolved organic matter (Fig. 2): fDOM increased more
rapidly and to higher levels in both M and MD treatments than in ponds
without Myriophyllum (C and D). This was expected, asMyriophyllum is known to be a producer of a wide range of organic
substances, including allelopathic chemicals
(Catalán et al.2014; Reitsema et al. 2018).
The presence of Dreissena alone
lead to the expected mediation of phytoplankton biomass, relative to the
control without foundation species during parts of the first, and, by
tendency, also throughout the second period of nutrient addition. Filter
feeding organisms like Dreissena can remove large quantities of
algae and suspended materials from the water column, which can help
stabilizing aquatic ecosystems in a clear water state, even when the
nutrient input is high
(Gulati et al.2008; McLaughlan & Aldridge 2013). In this context, Dreissenahave higher persistence than Myriophyllum , because they are not
limited by increasing turbidity like macrophytes. It has been shown that
population growth of mussels can be very high in eutrophic lakes
(Karatayev et
al. 2014a; Strayer et al. 2019), if sufficient amounts of hard
substrate are available
(Ibelings et
al. 2007; Fishman et al. 2010). In such cases, Dreissenacan not only affect water clarity and nutrient cycling, but also
directly lead to shifts in the composition of the phytoplankton
community towards a higher proportion, in some cases dominance, of
cyanobacteria like Microcystis
(Vanderploeg et
al. 2001; Bierman et al. 2005; Fishman et al. 2010) . Dreissenacan selectively reject particles as pseudofeces that bypass the
digestive tract, thus releasing less palatable particles like
cyanobacteria back to the environment
(Vanderploeg et al.2001). If this loosely consolidated substrate contains viable
cyanobacteria, these cells can resuspended in the water column while
other phytoplankton species are absorbed by the mussel.
The observed non-additive antagonistic
effect of Myriophyllum and Dreissena coincided with a
dramatic shift towards cyanobacteria that occurred when both macrophytes
and mussels were present (Fig. 2). As found by Narwani et al.
(2019), who
determined phytoplankton community composition from pond water samples
taken at regular intervals in the first year of the study, the small
cyanobacterium Synechococcus was dominant when bothMyriophyllum and Dreissena were present in a pond. In a
parallel laboratory experiment, Narwani et al.
(2019) tested
how the presence of allelochemicals (“Myriophyllum -tea”) orDreissena , alone and in combination, affected the relative
concentration of two species of microalgae that were most dominant in
the pond ecosystems (Lagerheimia sp. and Synechococcussp.). Similar to the dynamics observed in the pond experiment,Synechococcus increased in abundance relative to the green algaeLagerheimia when both Dreissena and allelochemicals were
present. This suggests that a relative advantage of cyanobacteria in the
presence of both foundation species, while other taxa in the community
experienced stronger negative effects, may have contributed to the shift
of phytoplankton communities toward cyanobacteria, resulting in an
overall increase in phytoplankton biomass (Narwani et al. 2019).
Throughout the study, we found strong
effects of the nutrient disturbances on the dynamics of ecosystem
metabolism, which varied among treatment combinations of the foundation
species. In both periods of disturbance (i.e. Figure 4, Phase 1 and 3),
the dynamics of ecosystem metabolism such strong evidence of
non-additivity, whereas in the intervening period (Figure 4, Phase 2)
the differences among treatments were more subtle, and the overall
patterns were driven by seasonality. For example, all metabolic rates
increased over the spring until the middle of June, and then decreased
until the final nutrient addition at the beginning of Phase 3 in
October. Moreover, in the MD treatment the CV of GPP was often higher
than the other treatments during the period when seasonality and weather
events likely dominated the dynamics. CV is a commonly used metric for
early warning sign for shifts in ecosystem state (just like AC, GEV, and
skewness - see supplement), and the increase towards the end of Phase 2
hints that the ecosystems might respond differently to the impending
pulse disturbance in Phase 3 (Figure 4). This suggests that high
frequency time series might provide insight into how ecosystems will
respond to disturbance. Following the final nutrient addition, all
ecosystems containing foundation species (D, M and MD) showed
significantly lower GPP and NEP, but higher R. This could be because
chlorophyll concentration in the control ponds without foundation
species continued to increase throughout the winter 2017/2018, whereas
DOM concentration in all other ponds decreased (Fig. 2). As a
consequence, higher productivity from phytoplankton in the control ponds
and higher respiration from DOM breakdown in all other ponds may be
responsible for the observed divergence in metabolic patterns towards
the end of the experiment.
Multiple lines of evidence suggest that non-additive interactions
between Myriophyllum and Dreissena strongly affected
ecosystem dynamics in ponds experiencing progressive nutrient
perturbations. This was especially visible in the phytoplankton
communities: the presence of both Myriophyllum andDreissena led to a higher algae biomass relative to control,
instead of a decrease when only one species was present in the ponds.
This demonstrates how a non-additive, antagonistic interaction between
two foundation species can have dramatic effects on the ecosystem, by
providing an opportunity for a third species, in this case
cyanobacteria, to dominate the community. Ecological synergies following
ecosystem perturbation are a known, but not well researched phenomenon
(Suttle et
al. 2007; Darling & Côté 2008; Thompson et al. 2018). In some
cases it may be difficult to uncover the effects that non-additive
species interactions have on ecosystems, particularly when they are only
expressed under disturbance conditions: in our experiment, the
phytoplankton biomass decreased again after we ceased the nutrient
additions. Nevertheless, the ecological mechanisms underlying these
effects might persist over time, even though the dynamics are not
evident during times of no disturbance (e.g. Phase 2). In our study,
even after perturbing the ecosystems a year later with a single strong
pulse of nutrients, the effect was stronger than during the first
addition, indicating that the non-additive effects of species
interactions can persist over time in a repeatable way.