Abstract
Plant phenology is manifested in the seasonal timing of vegetative and
reproductive processes, but also has ontogenetic aspects. The adaptive
basis of seasonal phenology has been considered mainly in terms of
climatic drivers. However, some biotic factors as likely evolutionary
influences on plants’ phenology appear to have been under-researched.
Several specific cases of putative biotic factors driving plant
phenology are outlined, involving both herbivores and pathogens. These
illustrate the diversity of likely interactions rather than any
systematic coverage or review. Emphasis is on woody perennials, in which
phenology is often most multi-faceted and complicated by the ontogenetic
aspect. The complete seasonal leaf fall that characterises deciduous
plants may be a very important defence against some pathogens. Whether
biotic influences drive acquisition or long-term persistence of
deciduousness is considered. In one case; of leaf rusts in poplars,
countervailing influences of the rusts and climate suggest persistence.
Often, however, biotic and environmental influences likely reinforce
each other. The timing and duration of shoot flushing may in at least
some cases contribute to defences against herbivores, largely through
brief periods of ‘predator satiation’ when plant tissues have highest
food value. Wide re-examination of plant phenology, accommodating the
roles of biotic factors and their interplays with environments as
additional adaptive drivers, is advocated, towards developing and
applying hypotheses that are observationally or experimentally testable.
Introduction
The phenology of an organism is among the key bases of evolutionary
adaptation to its habitat. It involves timing of an array of
developmental processes, with seasonal and ontogenetic aspects. With
plants at least, phenology is generally addressed in terms of its
seasonal aspect, which we mainly address. Seasonal phenology involves
seasonal timing of growth and reproductive processes. The visible
processes in plants include bud break in spring, shoot elongation, bud
set in autumn, natural foliage shedding, production of flower (or
strobilus in gymnosperms) buds, actual flowering, and development of
fruit and eventual fruit drop or seed shedding. Phenology, however, can
also include cryptic features (cf Albert et al. 2019). These include
initiation and differentiation of primordia, seed development, timing of
cambial activity, dehardening and hardening of tissues against frost,
the nature of growth rings, and seasonal patterns in root development.
However, we will not address specifically the cryptic phenomena, which
include both precursors of and flow-on from the visible ones. In any
event, the fullest, most multi-faceted expression of phenology tends to
be in woody perennials, which feature predominantly in this article.
The evolutionary drivers of phenology are of more than purely scientific
interest. They are also of increasing interest with the accentuated
adaptive pressures on plant populations imposed by climate change (e.g.
Kijowska-Oberc et al. 2020), ecosystem fragmentation and the arrival of
new pests and pathogens. Understanding both the evolutionary drivers and
the increased pressures will help in future management decisions. An
extensive literature on evolutionary drivers of phenology has focused
mainly on climates, with their seasonal cycles, the topic being
complicated by extreme diversity of adaptive strategies. Numerous
trade-offs arise between different features of strategies that may
contribute to fitness in particular environments. Adaptive strategies
for any organisms are thus highly multidimensional, being characterised
by how different features interact with each other to create ecological
fitness, and not by any single features. Even within a single habitat,
different plant species typically vary widely in their adaptive
strategies. This is obvious for co-occurring species that are evergreen
or deciduous as the case may be. Less obvious, though, are some specific
selective forces that shape individual strategies.
Ontogenetic phenology is considered briefly towards the end of this
article, to give perspective. It centres on how plants, as they get
older and larger, undergo maturation, which is manifested in widely
varying degrees (Poethig 1990; Zotz et al. 2011). It generally involves
acquisition of reproductive competence, which introduces a whole suite
of seasonal expression. Even vegetatively, there can be a transition
from a juvenile habit to a mature one, or in some species a relatively
abrupt switch (Zotz et al. 2011). Whatever the case, there can be major
changes in gross morphology and tissue anatomy.
Some consideration has been given interplays between biotic factors and
plant phenology. Both biotic and abiotic selective influences were
considered decades ago in reviews focused on plant phenology. Rathcke
and Lacey (1985), however, focused heavily on quantitative descriptors
of phenology, namely timing, duration, synchrony and statistical
distributions of phenological events. Van Schaik et al. (1993)
emphasised on seasonal climatic drivers of phenology, with the
implications for herbivores (“consumers”). Recently, in relation to
the relative importance of biotic drivers of local adaptation,
meta-analyses have been conducted ― albeit with no specific focus on
phenology. Hargreaves et al. (2020) did so for biotic effects in plants
only, and Briscoe Runquist et al. (2020) for abiotic and biotic effects
in plants and animals. Some trends were detected, notably in biotic
influences being more important in tropical than in temperate latitudes.
However, results were very heterogeneous and perennial plants were
weakly represented. One area that has been significantly researched is
seasonal phenology of leaf production in relation to herbivory within
the tropics (Lamarre et al. 2014). In some other cases, the research
focus has been on the seasonal phenology of herbivorous insects
adjusting to that of the host plant (e.g. Elzinga et al. 2007; Chuine
2010; Singer and Parmesan 2010). In a context of mammalian herbivory,
Benning et al. (2018) cite a case of a plant’s reproductive phenology
constraining its geographic range.
Despite these considerations, the possible extent and diversity of
putative biotic factors as evolutionary drivers of seasonal plant
phenology appear to remain under-researched, especially with pathogens.
Such factors represent the main focus of this paper. We consider the
evolutionary importance of biotic interactions, involving pathogens and
herbivory, with plant phenology. Main emphasis is on seasonal phenology,
with brief consideration of ontogenetic phenology. While some postulated
cases are cited from the literature, we offer others. Among postulated
cases, involving both pathogens and herbivores, we first consider
briefly the timing and synchronicity of both vegetative growth (bud
burst, shoot flushing and bud set) and flowering. We then focus strongly
on the complete seasonal leaf fall that characterises the deciduous
habit, in relation to selective pressures imposed by pathogens and
herbivores, and address the evolutionary hurdles facing shifts between
the deciduous and evergreen habits. Several other cases of putative
biotic drivers are also outlined. Coverage involves mainly woody
perennial plants, but two cases with pasture plants are considered,
along with one involving various wild herbaceous plants. As such, our
coverage serves to illustrate the diversity of likely biotic
interactions involving plant phenology, and the need for additional
investigation, rather than any attempt at comprehensive or even
systematic review. We draw heavily on close research familiarity with
certain species, hoping that the value of some detailed case histories
outweighs the sparseness of the coverage
In considering the evolutionary importance of biotic interactions,
involving pathogens and herbivory, with plant phenology our main
emphasis is on seasonal phenology. Ontogenetic phenology is considered
briefly.
Seasonal phenology
We note initially some key features of seasonal phenology, in relation
to cues and selective forces involving climate, as background for
considering interactions with pathogens and herbivory.
Traits of seasonal phenology are often both variable and heritable
within populations (e.g. Li and Adams 1993; Matziris 1994; Skrøppa and
Steffenrem 2019), giving scope for evolutionary change. Nevertheless,
limits to a species’ phenology can still govern its geographic range
(Chuine 2010), which of course may be altered by climatic change.
However, our focus is on likely drivers of the phenology of populations
wherever they are growing, considering vegetative and reproductive
aspects separately.
2.1 Vegetative aspect
In the seasonal timing of vegetative shoot phenology, there are the
obvious climatic drivers, reviewed in detail by Axelrod (1966). A key
feature is timing of bud burst, or flushing, which typically occurs in
spring in temperate climates or in some relation to wet and dry seasons
in tropical or semi-tropical climates. Also typical is a close seasonal
concentration and synchronisation of flushing. In temperate or cool
temperate climates, optimal fitness will classically represent some
balance between the advantages of flushing as soon as conditions favour
growth and the safety of delaying it until after almost all threat from
late (spring) frost. The period of shoot extension growth that follows
flushing can be very brief, certainly in many temperate tree species,
including various conifers. Often these seasons seem far shorter than
the periods when climatic conditions would permit active growth, classic
examples existing among the true firs (Abies spp). Complementing
flushing and subsequent shoot extension are bud set associated with the
cessation of elongation, and the complete shedding of foliage in
deciduous species. These processes occur in late summer or autumn in
temperate or cool temperate climates, but in variable relationships to
dry seasons at lower latitudes.