Discussion
Since the green world hypothesis proposed by Hairston et al. (1960), a
number of studies have examined effects of primary production and
predation (Carpenter et al. 1985; Power 1992; Shurin et al. 2002;
Hambright 1994; Hanley & La Pierre 2015; Ward et al. 2015;), and those
of anti-herbivory defense or edibility of producers (Coley et al. 1985;
Wolfe et al.1997; Agrawal & Fishbein 2006; Poelman et al. 2008; Mooney
et al. 2010) on herbivore abundance relative to producer abundance (theH/P ratio). Although elemental stoichiometry of primary producers
has often been considered as a factor that determines herbivore biomass
(Ceberian 1999; Sterner & Elser 2002; Ceberian et al. 2009), few
studies have experimentally examined whether nutrient contents can
regulate herbivore relative to producer abundance at a community level
(e.g., Urabe et al. 2002). Moreover, to the best of our knowledge, no
studies have determined and compared the relative importance of these
factors in natural communities, presumably because no theoretical
framework has been developed for quantitatively examining their effects
in a comparable way. This is the first study to examine simultaneously
the effects of those four factors on the H/P mass ratio in a
single natural community. By fitting our observed data to a modified
Lotka-Volterra-based model, we have shown that in addition to primary
production and predation, edibility and stoichiometry of primary
producers plays pivotal roles in regulating the H/P mass ratio.
Our model, based on Lotka-Volterra equations, is derived from the
equilibrium state of a system. In this study, both phytoplankton and
zooplankton biomass dynamically changed in all the treatments throughout
the experiment, indicating that no community in this study reached
equilibrium. However, theoretically, temporal means of herbivore and
producer abundances for at least one oscillation cycle should coincide
with the equilibrium abundances in the Lotka-Volterra model (Haberman
1977). Theoretical and experimental studies have also shown that one
oscillation cycle occurred within < 50 days in
zooplankton-phytoplankton dynamics (McCauley & Murdoch, 1990). Thus,
the present experimental run would be sufficiently long so that the
temporal mean values among samples collected biweekly were close to
equilibrium values in zooplankton-phytoplankton dynamics.
Among the factors we examined, fish abundance had the greatest effect on
changes in the H/P mass ratio. This result might be caused by the
fact that, in comparison with planktonic organisms, fish abundance was
temporally more stable due to their longer life span. In all sections
(treatments) of pond 217, where planktivorous fishes were abundant, the
density of large cladocerans in the zooplankton community was low. The
result was in accordance with the well-known fact that planktivorous
fish prey selectively on larger zooplankton species (Carpenter et al.
1985; Hambright 1994; Lampert &Sommer 2007). Other than the direct
effect of predation, several studies suggest that fish can indirectly
affect zooplankton biomass by stimulating primary productivity through
nutrient recycling (Williamson et al. 2018). However, in this study, the
specific production rate (μ ) was not related to fish abundance,
suggesting that the net impact of fish abundance on the H/P mass
ratio was largely attributable to a direct top-down force on zooplankton
biomass rather than indirect bottom-up forcing through nutrient cycling.
A number of studies have argued that the H/P mass ratio is
regulated by the efficacy of the producer’s anti-predator defense (Coley
et al. 1985; Poelman et al. 2008; Moony et al. 2010). In this study,
occurrence of algae that might have contained some toxicities for
zooplankton such as cyanobacteria (Lampert & Sommer 2007; Smith &
Schindler 2009) was limited. Therefore, we focused physical defense of
phytoplankton. Since most herbivore plankton cannot efficiently graze
phytoplankton species with a cellular or colony size larger than 30 µm
(Lampert and Sommer 2007), enlargement of cellular or colony size can be
viewed as a defense trait against herbivory (Pančić & Kiørboe 2018).
Therefore, we examined fraction of edible phytoplankton
(αedi ) on H/P mass ratio. No significant
relationship was detected between these in simple regression. However,
if we considered only the treatments in pond 218 where fish abundance
was limited, the H/P ratio tended to increase with this fraction.
Indeed, αedi was significantly related with the
mass ratio when other factors, such as fish abundance, were
simultaneously considered in the multiple regression analysis. These
results indicate that edibility or a defense trait such as enlargement
of cellular or colony sizes indeed play a role in regulating H/Pmass ratio, even in aquatic communities.
Other than the defense trait, nutritional values or nutrient contents of
producers have often been proposed as crucial factors determining the
abundance of herbivores relative to that of producers (Cebrian 1999;
Srerner & Elser 2002; Ceberian 2009; Konno, 2016). In this study
cyanobacteria biomass was less than 10%, suggesting that deficiency of
polyunsaturated fatty acids were not prime factors affecting quality of
phytoplankton food for zooplankton in this study (Urabe et al. 2018).
Cebrian (1999) argued that a lower H/P mass ratio in terrestrial
communities compared with aquatic communities is attributable to lower
nitrogen and phosphorus contents relative to carbon in terrestrial
producers. In this study, we focused on phosphorus as the main nutrient
since phosphorus limitation of herbivore growth at an individual level
has been repeatedly pointed out. Indeed, this study successfully showed
that seston carbon to phosphorus ratio was a significant factor
affecting H/P mass ratio across communities with different
taxonomic compositions of phytoplankton and zooplankton. The result
supports a theory of ecological stoichiometry which states that the
relative abundance of herbivores to producers changes depending on the
stoichiometric mismatch between them (Sterner & Elser, 2002).