Reply to: Nutrient scarcity cannot cause mast seeding

Abstract

In his recent communication on our original paper 1,2 , D. Kelly, claiming that nutrient scarcity cannot select for masting behaviour in plants, initiated a fruitful discussion on traditionally settled hypotheses about the evolution of reproductive behaviour in plants. In his commentary, Kelly raises support for a contrasting hypothesis explaining our observation that temporally variable seed production is more pronounced under nutrient scarcity, namely that nutrient scarcity does not directly cause seed production variability but instead increases variability induced by economies of scale (EOS). The commentary hinges mainly on the argument that an EOS is necessary to select for highly variable seed production. It also points out that there are no mechanisms by which nutrient scarcity would select for that particular trait over generations. In reply to the stimulating comment, we (1) propose a mechanism by which nutrient scarcity may select for highly variable seed production, with weather patterns inducing masting synchrony across populations; and (2) further discuss why wind pollination and predator satiation, the EOS suggested by Kelly, cannot be the only selective pressures that select for highly variable reproduction. There is robust empirical evidence 3,4 showing that nutrient scarcity and climate, are long-existing evolutionary forces that have selected for multiple plant traits and have constrained the physiology of plants since their early development. Limiting resources, such as water and nutrients, thus trigger the evolution of conservative traits for those limiting factors 4. Logically, nutrient availability is a direct determinant of the mean fruit production in agriculture and in the wild 5. In our paper 1 , we hypothesized that low nutrient availability is also an important factor selecting for highly variable and synchronized seed production, the latter in combination with adaptation to variability in long-term climate patterns. Our hypothesis as to why nutrient scarcity may have selected for highly variable seed production in nutrient-poor plants, probably not entirely explained in our original paper, was based on a mechanism linking highly variable seed production in nutrient-poor plant species to increased interspecific and intraspecific competitiveness. Because fruits are nutrient-enriched tissues 6 , their production under low fertility implies a reduced allocation of nutrients to growth and defence 7 , and therefore lower competitiveness and survival for the parent plants. Reductions in plant nutrient concentrations after reproduction have been described for several species 8 , in addition to growth and defence-reproductive trade-offs 7. Therefore, when nutrients are scarce, losing large amounts of nutrients year after year might jeopardize plant growth through reduced photosynthesis, a highly nutrient-dependent process 9. Constant yearly reproduction would also imply a constant lowering of the availability of nutrients for other processes. In contrast, nutrient accumulation in years with suitable weather conditions for soil organic matter decomposition and mineralization may provide sufficient nutrients to allow a high fruit crop in the following year, which would not come at the expense of reduced competitiveness or increased mortality risk (Fig. 1). Under these conditions, high temporal variability would thus be beneficial and likely to be selected for. In contrast, under nutrient-rich conditions, plants can potentially reproduce regularly without jeopardizing their competitiveness ; this is actually one of the reasons for fertilizer addition as a long-existing agricultural practice. This mechanism, which could have originated during the early evolution of plants, may explain why, under low nutrient availability, nutrient-conservative plants with highly variable reproduction may have been preferentially selected in comparison to nutrient-spending plants (with more constant reproduction). Further research, including long-term datasets of reproduction, growth and defence allocation, however, is needed to validate our hypotheses. For a population to exhibit highly variable reproduction over time, a strong synchrony among individuals is required 10. Synchronous seed production is another important feature of masting behaviour that has been traditionally associated with the benefits of EOS, as it has been suggested to be an adaptive response to improve pollination efficiency or escape seed preda-tion 8. Synchrony among individuals in a plant population is the rule rather than the exception, as for example in leaf flushing, flower blooming, die-back episodes or simply growth as shown by dendrochronology studies. The most likely mechanism driving the synchrony in phenology, growth or reproduction is the similar response of a population to changing weather patterns, by affecting metabolism and plant resources.

Full text

Matters arising
https://doi.org/10.1038/s41477-020-0703-6
1Research Group PLECO (Plants and Ecosystems), Department of Biology, University of Antwerp, Antwerp, Belgium. 2Global Ecology Unit, CREAF-CSIC-UAB,
Barcelona, Spain. 3CREAF, Barcelona, Spain. 4Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.
5Gothenburg Global Biodiversity Centre, Gothenburg, Sweden. 6Department of Biological Sciences, DePaul University, Chicago, IL, USA. 7Department of
Systematic Zoology, Faculty of Biology, Adam Mickiewicz University, Poznań, Poland. 8Institute for Agriculture and Forestry Systems in the Mediterranean,
National Research Council of Italy (CNR-ISAFOM), Perugia, Italy. 9Department of Innovation in Biological, Agro-food and Forest Systems, University of
Tuscia, Viterbo, Italy. 10Department of Geography and Planning, School of Environmental Sciences, University of Liverpool, Liverpool, UK. 11DISAA, Università
di Milano, Milan, Italy. ✉e-mail: marcos.fernandez-martinez@uantwerpen.be
In his recent communication on our original paper1,2, D. Kelly,
claiming that nutrient scarcity cannot select for masting behav-
iour in plants, initiated a fruitful discussion on traditionally settled
hypotheses about the evolution of reproductive behaviour in plants.
In his commentary, Kelly raises support for a contrasting hypoth-
esis explaining our observation that temporally variable seed pro-
duction is more pronounced under nutrient scarcity, namely that
nutrient scarcity does not directly cause seed production variabil-
ity but instead increases variability induced by economies of scale
(EOS). The commentary hinges mainly on the argument that an
EOS is necessary to select for highly variable seed production. It also
points out that there are no mechanisms by which nutrient scarcity
would select for that particular trait over generations. In reply to the
stimulating comment, we (1) propose a mechanism by which nutri-
ent scarcity may select for highly variable seed production, with
weather patterns inducing masting synchrony across populations;
and (2) further discuss why wind pollination and predator satiation,
the EOS suggested by Kelly, cannot be the only selective pressures
that select for highly variable reproduction.
There is robust empirical evidence3,4 showing that nutrient scar-
city and climate, are long-existing evolutionary forces that have
selected for multiple plant traits and have constrained the physi-
ology of plants since their early development. Limiting resources,
such as water and nutrients, thus trigger the evolution of conserva-
tive traits for those limiting factors4. Logically, nutrient availability
is a direct determinant of the mean fruit production in agriculture
and in the wild5. In our paper1, we hypothesized that low nutrient
availability is also an important factor selecting for highly variable
and synchronized seed production, the latter in combination with
adaptation to variability in long-term climate patterns. Our hypoth-
esis as to why nutrient scarcity may have selected for highly vari-
able seed production in nutrient-poor plants, probably not entirely
explained in our original paper, was based on a mechanism linking
highly variable seed production in nutrient-poor plant species to
increased interspecific and intraspecific competitiveness.
Because fruits are nutrient-enriched tissues6, their produc-
tion under low fertility implies a reduced allocation of nutrients
to growth and defence7, and therefore lower competitiveness and
survival for the parent plants. Reductions in plant nutrient con-
centrations after reproduction have been described for several spe-
cies8, in addition to growth and defence–reproductive trade-offs7.
Therefore, when nutrients are scarce, losing large amounts of
nutrients year after year might jeopardize plant growth through
reduced photosynthesis, a highly nutrient-dependent process9.
Constant yearly reproduction would also imply a constant lower-
ing of the availability of nutrients for other processes. In contrast,
nutrient accumulation in years with suitable weather conditions for
soil organic matter decomposition and mineralization may provide
sufficient nutrients to allow a high fruit crop in the following year,
which would not come at the expense of reduced competitiveness or
increased mortality risk (Fig. 1). Under these conditions, high tem-
poral variability would thus be beneficial and likely to be selected
for. In contrast, under nutrient-rich conditions, plants can poten-
tially reproduce regularly without jeopardizing their competitive-
ness; this is actually one of the reasons for fertilizer addition as a
long-existing agricultural practice. This mechanism, which could
have originated during the early evolution of plants, may explain
why, under low nutrient availability, nutrient-conservative plants
with highly variable reproduction may have been preferentially
selected in comparison to nutrient-spending plants (with more con-
stant reproduction). Further research, including long-term datasets
of reproduction, growth and defence allocation, however, is needed
to validate our hypotheses.
For a population to exhibit highly variable reproduction
over time, a strong synchrony among individuals is required10.
Synchronous seed production is another important feature of
masting behaviour that has been traditionally associated with
the benefits of EOS, as it has been suggested to be an adaptive
response to improve pollination efficiency or escape seed preda-
tion8. Synchrony among individuals in a plant population is the
rule rather than the exception, as for example in leaf flushing,
flower blooming, die-back episodes or simply growth as shown
by dendrochronology studies. The most likely mechanism driving
the synchrony in phenology, growth or reproduction is the similar
response of a population to changing weather patterns, by affecting
metabolism and plant resources.
Reply to: Nutrient scarcity cannot cause mast
seeding
M. Fernández-Martínez 1 ✉ , J. Sardans2,3, F. Sayol4,5, J. M. LaMontagne 6, M. Bogdziewicz 7,
A. Collalti 8,9, A. Hacket-Pain 10, G. Vacchiano 11, J. M. Espelta3, J. Peñuelas 2,3 and
I. A. Janssens 1
replying to D. Kelly Nature Plants https://doi.org/10.1038/s41477-020-0702-7 (2020)
NATURE PLANTS | VOL 6 | JULY 2020 | 763–765 | www.nature.com/natureplants 763
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