Figure 2: Relative contribution of prey carbon biomass to the total
ingested biomass by Limnomysis benedeni plotted as a function of
the relative contribution of each prey to total available carbon
biomass. Prey types used are Cryptomonas sp. (dark green) andB. calyciflorus (orange). Solid dots represent samples while
error bars indicate the 95% confidence intervals. The dashed 1:1 line
represents where L. benedeni would be consuming a prey
proportional to its availability, meaning random food uptake (neither
preference, nor avoidance).
Discussion
Our results clearly showed that the diet preference of L.
benedeni depends on the relative (C) biomass concentration of prey
types, by shifting from microzooplankton to phytoplankton prey with
increasing phytoplankton prey biomass. The patterns of consumption rates
in response to relative prey biomass differed between the prey types
suggesting slightly different functional responses for the
microzooplankton and phytoplankton prey. While both resembled a
sigmoidal pattern (Fig. 1A), the ingestion rate on B.
calyciflorus followed a type III functional response more clearly,
which usually indicates either prey switching or efforts to modify
foraging behaviour in response to the prey density
(Holling, 1959;
Kiørboe et al., 2018; Thomas et al., 1996). In the case ofCryptomonas sp. after a slower increase at low densities, the
pattern was closer to linear and did not show saturation within the
tested biomass range during the experiment, overall resembling a type I
functional response
(Holling, 1959),
suggesting that consumption of Cryptomonas sp. is primarily a
function of density.
The decreasing consumption rates on rotifers with increasing algae
concentration illustrated how the presence of alternative prey items in
sufficient densities can lead to decreased predation pressure on another
type of prey. If more than one alternative food source is present,
predators can select based on prey-specific encounter rates to optimize
foraging time and energy intake
(Krebs et al., 1977).
Specifically, the relative attack rate is a function of relative density
and the switching can happen only if the likelihood of attacking the
last eaten species is higher than attacking other species
(Oaten & Murdoch,
1975). In our case, the cost-to-benefit ratio changes in favour of
algae at higher algae densities. Indeed, we found that algae consumption
increased in comparison to rotifer consumption for biomass equal to or
higher than 1 mgC L-1. This is also supported by
Ivlev’s index results which point towards the flexibility in the feeding
behaviour of L. benedeni depending on algal density. The Ivlev’s
indices indicate a preference for rotifers in the presence of low algae
biomass and avoidance of algae and vice versa with high algal biomass.
Predators typically select their diet based on size, nutritional
quality, and escape responses of the prey
(Cotonnec et al.,
2001; Frost, 1972; Viitasalo & Rautio, 1998). They would try to
increase their fitness by acquiring prey with easier access and lower
cost-to-benefit ratio
(MacArthur & Pianka,
1966; Pyke et al., 1977; Stephens & Krebs, 1986). Earlier studies
suggest that L. benedeni is not an optically-oriented predator
but selects its food based on size
(Fink et al., 2012).
Here we provided L. benedeni with two types of food with very
different sizes. Purely from a size-based perspective, feeding on the
smaller prey is only beneficial when available in sufficient densities,
which was indeed confirmed by our results, with L. benedenishowing a gradual shift to the smaller prey with its increasing
quantity.
Prey nutritional quality can also affect the development of consumers
and influence their dietary choices
(Gulati & Demott,
1997; Meunier et al., 2016). For instance, algae generally have a
higher carbon-to-nutrient ratio than animal prey
(Elser et al., 2000;
Sterner & Hessen, 1994). In the case of Cryptomonas SAG 26.80,
a C:P ratio of ~150 and a C:N ratio of
~22 were reported during the exponential growth phase
(i.e. when nutrients are not limiting growth;
Vad et al., 2020).
For B. calyciflorus , C:P ratios are relatively constant around
~92, while C:N are ~4
(Jensen & Verschoor,
2004), which is very close to the body stoichiometry of omnivorous
crustaceans such as mysids (C:P~90 and C:N
~4)
(Arbačiauskas et al.,
2013). Therefore, based on a purely elemental stoichiometric point of
view (Laspoumaderes et
al., 2010), rotifers would be the preferred prey. The higher C to
nutrient ratios of algae may explain the pattern we found in the case of
total ingested carbon biomass, which instead of steadily increasing
showed an accelerating increase at the highest Cryptomonas sp.
biomass level. This may indicate that L. benedeni needs to
increase overall food uptake when feeding on algae, to obtain sufficient
amounts of nutrients.
Other factors such as essential fatty acids
(Ahlgren et al., 1990;
Brett & Müller-Navarra, 1997; Ramlee et al., 2021; Trommer et al.,
2019), or vitamins
(Fridolfsson et al.,
2018, 2019; Hessen, 1992) can also influence food quality.Cryptomonas sp. is considered to be a high-quality algal food
source based on the high cellular content of essential fatty acids
(Von Elert & Stampfl,
2000; Weers & Gulati, 1997). Consequently, the results may differ if
the autotrophic food quality is less cost-efficient for the predator
than the heterotrophic prey. For instance, had a ‘less favourable’ algal
food source, such as green algae, been used, the preference for rotifers
might have been more pronounced. Nonetheless, a preference for green
algae (Chlamydomonas sp. ) over zooplankton has been observed
previously at an algal biomass of 0.3 mg POC L-1 as
well (Fink et al.,
2012).
Given that our study is based on a short-term experiment, there are some
aspects in which its results might differ from patterns arising in
natural communities. For instance, the container size in laboratory
studies is a factor that may influence predator behaviour
(Bergström & Englund,
2004; Toonen & Fu-Shiang, 1993). Therefore, a small-sized jar could
have increased the competition among mysids thus forcing them to choose
algae, a ‘costly prey’, to consume maximum food to maintain their energy
budget. In addition, in this grazing experiment, we did not include
predators of mysids, though in natural ecosystems optimal foraging
strategy is based on a tradeoff between nutritional needs and
simultaneously minimising the risk of predation as described in the
unified foraging theories (e.g., Mangel & Clark, 1986). Experiments
with another trophic level (e.g., small fish), carried out in larger
mesocosms, could therefore provide more specific predictions on these
tradeoffs in the future, including longer-term effects on ecosystem
stability.
Despite these limitations, our results provide important implications
for plankton community dynamics in natural ecosystems. Depending on the
relative biomasses of phyto- and zooplankton, mysid shrimps may act as
predators or competitors of zooplankton, being intraguild predators of
the latter. By always suppressing the more abundant planktonic prey,
they may reduce the amplitude of predator-prey oscillations, thereby
contributing to ecosystem stability. However, there are certainly other
possible scenarios as well, as illustrated by the effects of other
invasive omnivorous Ponto-Caspian mysids. For example, Hemimysis
anomala and Paramysis lacustris were both found to contribute to
the alteration of trophic pathways in their invaded habitats, due to
their strong predatory impact on zooplankton and benthic
macroinvertebrate communities
(Evans et al., 2018;
Ketelaars et al., 1999; Rakauskas, 2019). For a better understanding of
the potential effects of omnivorous mysids on trophic cascades and food
web stability, studying their feeding mechanisms and diet selection is
of high importance. Field observations coupled with laboratory and
mesocosms studies could contribute to understanding the mechanisms
underlying community and ecosystem-level effects of these widespread
(and still spreading) invasive species.
Acknowledgements
This study was supported by the NKFIH-138215 project. We acknowledge the
valuable suggestions given by Pavel Kratina and Peter Borza.
Author’s contributions
- Varsha Rani- Conceptualization (Equal), Methodology (Equal), Data
curation (Lead), Formal analysis (Equal), Original draft of the paper
(Lead), Revision of the paper (Equal)
- Zsófia Horváth- Conceptualization (Supporting), Formal analysis
(Equal), Revision of paper (Equal), Supervision (Supporting)
- Jens C. Nejstgaard- Conceptualization (Equal), Methodology
(Supporting), Revision of the paper (Equal)
- Ádám Fierpasz- Methodology (Supporting), Revision of the paper
(Supporting)
- Károly Pálffy- Formal analysis (Equal), Revision of the paper (Equal)
- Csaba F. Vad- Conceptualization (Equal), Methodology (Equal), Resource
(Lead), Data curation (supporting), Formal analysis (Equal), Original
draft of the paper (Lead), Revision of the paper (Equal), Supervision
(Lead), Funding acquisition (Lead)
Conflict of Interest Statement
The authors declare no conflict of interest.