Nutrient scarcity as a selective pressure for mast seeding

Abstract

Mast seeding is one of the most intriguing reproductive traits in nature. Despite its potential drawbacks in terms of fitness, the widespread existence of this phenomenon suggests that it should have evolutionary advantages under certain circumstances. Using a global dataset of seed production time series for 219 plant species from all of the continents, we tested hether masting behaviour appears predominantly in species with low foliar nitrogen and phosphorus concentrations when controlling for local climate and productivity. Here, we show that masting intensity is higher in species with low foliar N and P concentrations, and especially in those with imbalanced N/P ratios, and that the evolutionary history of masting behaviour has been linked to that of nutrient economy. Our results support the hypothesis that masting is stronger in species growing under limiting conditions and suggest that this reproductive behaviour might have evolved as an adaptation to nutrient limitations and imbalances.

Full text

Articles
https://doi.org/10.1038/s41477-019-0549-y
1PLECO (Plants and Ecosystems), Department of Biology, University of Antwerp, Antwerp, Belgium. 2Global Ecology Unit, CREAF–CSIC–UAB,
Barcelona, Spain. 3US Geological Survey, Fort Collins Science Center, Fort Collins, CO, USA. 4CREAF, Barcelona, Spain. 5Department of Biological and
Environmental Sciences, University of Gothenburg, Gothenburg, Sweden. 6Gothenburg Global Biodiversity Centre, Gothenburg, Sweden. 7Cornell
Lab of Ornithology, Cornell University, Ithaca, NY, USA. 8Department of Biological Sciences, DePaul University, Chicago, IL, USA. 9Department of
Systematic Zoology, Faculty of Biology, Adam Mickiewicz University in Poznań, Poznań, Poland. 10Institute for Agriculture and Forestry Systems in
the Mediterranean, National Research Council of Italy (CNR-ISAFOM), Rende, Italy. 11Department of Innovation in Biological, Agro-food and Forest
Systems, University of Tuscia, Viterbo, Italy. 12Department of Geography and Planning, School of Environmental Sciences, University of Liverpool,
Liverpool, UK. 13DISAA, Università di Milano, Milan, Italy. *e-mail: marcos.fernandez-martinez@uantwerpen.be
Mast seeding—often called masting—has long intrigued
biologists as one of the most bizarre reproductive behav-
iours found in nature1,2. This behaviour consists of the
synchronous production of highly variable seed crops over time3.
Masting has often been considered an evolutionary paradox because
organisms that skip reproductive attempts should have lower fitness
than those that reproduce at every opportunity4. Nonetheless, the
fact that this reproductive behaviour is found in different lineages
suggests that masting behaviour should be beneficial, at least under
certain scenarios.
The most widely accepted hypotheses explaining the selective
advantages of masting are all related to economies of scale5,6. Briefly,
these hypotheses state that, in terms of fitness, it is more efficient
for plants to produce a large number of seeds every few to several
years than to produce a constant number every year. This general
mechanism includes the predator satiation hypothesis2,7–9, where
predators are starved during years of null or low reproduction and
satiated during high reproduction mast years, leaving large num-
bers of seeds intact. Another example is the pollination efficiency
hypothesis5,10,11, which states that, particularly for wind-pollinated
plants, saturating the atmosphere with pollen in a given year is
more efficient than producing regular amounts of pollen each year
to ensure pollination. Given that masting is present in only a mod-
est percentage of plant species12, such economies of scale are appar-
ently advantageous only under certain circumstances. What those
circumstances are remains, so far, under debate.
The environmental stress hypothesis13 suggests that masting
behaviour should be stronger under unfavourable growing condi-
tions or limitation of resources—conditions under which econo-
mies of scale should be more beneficial3,11,14. This is because plants
growing in unfavourable environments presumably experience
more difficulties in acquiring the required resources to reproduce,
as suggested by the resource accumulation hypothesis15,16. According
to this hypothesis, plants growing under favourable conditions will
be able to accumulate the required amount of resources every year
and, therefore, present a regular pattern in seed production, without
exhibiting any underlying negative temporal autocorrelation that
could indicate resource depletion after reproduction15. The opposite
is true for plants growing in unfavourable conditions, which will
exhibit high interannual variability and negative temporal autocor-
relation in seed production due to potential resource depletion after
seeding. However, there is no current empirical evidence suggesting
that species with higher interannual variability in fruit production
are more likely to exhibit negative temporal autocorrelation than
species that produce seeds more regularly. In contrast, weather
variability has been found to be a key factor driving interan-
nual variability in fruit production in many plant species11,17–20.
Therefore, temporal patterns in weather events (that is, temporal
variability and autocorrelation) could potentially shape the temporal
patterns of fruit production21.
Foliar nutrient concentrations play a key role in plant ecophysi-
ology and ecosystem functioning: photosynthetic rates are linked
to foliar nitrogen (N) and phosphorus (P) concentrations22–24.
Together with carbon, they are the basis of ecological stoichiom-
etry25,26 and are fundamental parts of the elementome or the bio-
geochemical niche27, useful for inferring ecological traits from the
elemental composition of organisms28. N and P, as well as carbon
(C), have been suggested to be potential resources determining
seed production and masting behaviour14,29–31, because seeds and
fruits are enriched with N and P compared with vegetative tissues32.
Nutrient scarcity as a selective pressure for
mast seeding
M. Fernández-Martínez 1,2*, I. Pearse3, J. Sardans2,4, F. Sayol 5,6, W. D. Koenig7, J. M. LaMontagne 8,
M. Bogdziewicz 9, A. Collalti 10,11, A. Hacket-Pain 12, G. Vacchiano 13, J. M. Espelta4, J. Peñuelas 2,4
and I. A. Janssens 1
Mast seeding is one of the most intriguing reproductive traits in nature. Despite its potential drawbacks in terms of fitness, the
widespread existence of this phenomenon suggests that it should have evolutionary advantages under certain circumstances.
Using a global dataset of seed production time series for 219 plant species from all of the continents, we tested whether mast-
ing behaviour appears predominantly in species with low foliar nitrogen and phosphorus concentrations when controlling for
local climate and productivity. Here, we show that masting intensity is higher in species with low foliar N and P concentrations,
and especially in those with imbalanced N/P ratios, and that the evolutionary history of masting behaviour has been linked to
that of nutrient economy. Our results support the hypothesis that masting is stronger in species growing under limiting condi-
tions and suggest that this reproductive behaviour might have evolved as an adaptation to nutrient limitations and imbalances.
NATURE PLANTS | VOL 5 | DECEMBER 2019 | 1222–1228 | www.nature.com/natureplants
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