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\begin{document}

\title{Putative biotic drivers of plant phenology: with special reference to
pathogens and deciduousness}



\author[1]{Rowland Burdon}%
\affil[1]{Scion (New Zealand Forest Research Institute Ltd)}%


\vspace{-1em}



  
  \date{May 24, 2024}


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\selectlanguage{english}
\begin{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.%
\end{abstract}%



\sloppy


\textbf{Title:} Putative biotic drivers of plant phenology: with special
reference to pathogens and deciduousness

\textbf{Authors:} Rowland D. Burdon (corresponding); ORCID number
0000-0002-7815-2739;\textbf{E-mail:}\textless{}rowland.burdon@scionresearch.com\textgreater{}

Michael J. Bartlett; ORCID number 0000-0002-4253-6589

\textbf{Address:} Scion (New Zealand Forest Research Institute Ltd),
Private Bag 3020, Rotorua 3046, New Zealand

\textbf{Keywords:} biotic interactions, evolution, deciduous, herbivory,
pathogens, plant phenology

\textbf{Manuscript category:} Hypotheses

\textbf{Words (total):} 12,104; (Main text -- 9,161; References list --
2,747; Tables file -- 135; Fig. captions -- 196)

\textbf{List of elements:} manuscript; Tables; Figure 1; Figure 2;
Figure 3

\textbf{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.

\textbf{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.

\textbf{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; Skr\selectlanguage{ngerman}øppa 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.

\textbf{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 (\emph{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.

\textbf{2.2 Reproductive aspect}

Seasonal synchronisation of flowering is often closely linked to
vegetative phenology. This has several obvious benefits, apart from
those incidental to optimal timing with respect to climatic factors.
Among the benefits, close synchronisation helps assure adequate pollen
when the female structures are receptive. Also, by all occurring early
enough, this assures sufficient time for fruits and seeds to develop and
mature before either summer drought or autumn cold disrupt such
processes. Moreover, brief but differentiated flowering seasons can also
provide reproductive barriers between species that are interfertile but
whose hybrids may not be ecologically fit; however, such barriers have
broken down in some eucalypt species grown as exotics where their
flowering seasons differ from those in native habitats (Eldridge et al.
1993). This synchrony can mean very seasonal food supplies for animal
pollinators, but very short seasons can be made good by other, sympatric
species having differentiated flowering seasons \selectlanguage{english}- as with various
eucalypt species (Eldridge et al. 1993). A further but probably very
incidental benefit of flowering synchrony may be creating a brief
superabundance for herbivores, which we will consider later.

Masting, namely heavy flowering and seed production in some years, with
little or none in between (e.g. Kelly 1994; Kelly and Sork 2002), is a
phenomenon involving the timing of flowering. Its postulated biotic
significance is as a means of alternating between occasional predator
satiation and more frequent predator avoidance. However, it is not
actually a seasonal phenomenon, nor really ontogenetic, so it is not
considered further.

Timing of flowering has been reported as a minor factor in complex
interactions involving transmission of pathogens by pollinators (Biere
and Antonovics 1996; McArt et al. 2014), but is not considered further
in this connection.

\textbf{Pathogens as putative drivers}

The role of pathogens as potential evolutionary drivers of seasonal
phenology appears to have been especially under-researched. Cases we
consider involve: potential roles of pathogens in governing the
deciduous growth habit; the seasonal timing of spring flushing in a
widely distributed conifer; two closely related \emph{Pinus} species
with overlapping distributions but markedly different seasonal timing of
vegetative and reproductive processes; and an oak species in what is
effectively an altitudinal transect. Briefly considered also is how
pathogens can modify phenotypically some processes that are normally
parts of seasonal phenology.

\textbf{2.3.1 Deciduous versus evergreen habit}

Of special note in phenology is the seasonal complete shedding of
foliage that characterises the deciduous habit, versus the evergreen
habit. This was reviewed by Holttum (1953) for tropical forests and
Axelrod (1966) for temperate forests. These important papers pointed to
factors of the abiotic environment as the evolutionary drivers of
deciduousness. This focus on abiotic factors appears to have dominated
subsequent enquiry into the topic. Both authors postulated that seasonal
drought was the original driver. Specifically, Axelrod postulated that
this habit, having originated during the Cretaceous, was a preadaptation
to cold winters that subsequently characterised high-latitude
environments along with their widely fluctuating daylengths. Yet, in
many harsh, high-latitude climates, with very severe winters, both
deciduous and evergreen tree species co-occur. Moreover, even within
some genera, notably \emph{Nothofagus} in South America, both deciduous
and evergreen species can grow adjacently. In adaptation to climates
with severe winters there are some obvious trade-offs. The deciduous
habit entails heavy seasonal turnover of biomass, but the leaves do not
require investment in anatomical features needed for overwintering. This
habit also allows the leaves to be photosynthetically very efficient
relative to their dry matter (Reich et al. 1992). Apart from
co-occurring species, sometimes close relatives, including both
evergreens and deciduous ones, there are other obstacles to facile
climatic interpretation. For instance, deciduousness exists among many
species without severe winters (e.g. Suc 1984; Li et al. 2013). Also,
there are deciduous tropical tree species that produce new foliage well
before dry seasons end, which we will revisit.

For the evergreen habit, the anatomical requirements for leaves
surviving winters or other seasonal stresses will also tend to make them
less attractive or rewarding to herbivores in general. Such protection
against herbivory is very often complemented by toxin production. All
these defences, along with defences against abiotic factors, require
additional investments (Loehle \& Namkoong 1987; Strauss et al. 2002;
Kursar \& Coley 2003; Villar et al. 2006), or ``higher construction
costs'' (Smith et al. 2019). However, such investments can obviate the
cost of the complete seasonal turnover of foliage in deciduous plants.
Also, early flushing is not crucial for evergreens to resume
photosynthesis in the spring (cf Panchen et al. 2014). Osada (2020),
comparing sympatric evergreen and deciduous species, found the former to
have later and longer periods of leaf expansion. One might expect
foliage toxicity to be more prevalent and more severe in evergreen
species than in deciduous ones, but we have found no published survey on
this question. Anecdotally, however, yews (\emph{Taxus} spp) which are
evergreen are both notoriously toxic and often associates of deciduous
species. Within a deciduous example (\emph{Populus deltoides x P. nigra
`Robusta'} ) a subtle, seasonal effect of seasonal decline in phenolic
compounds being associated with increasing susceptibility to the leaf
rust \emph{Melampsora} \emph{larici-populina} Kleb. was observed by
Maupetit et al. (2018). This suggests that, if phenolic compounds
represent a defence mechanism, that decline reflects an energetic cost
of their production and decreasing value of the protection that they
confer.

While much attention given to the energetic costs and associated
trade-offs in alternative strategies of deciduous or evergreen habit,
little seems to have been given to the possible roles of pathogens and
herbivores in generating or maintaining the deciduous habit. In relation
to the evolutionary pressures imposed by both biotic and abiotic
factors, we will consider also the evolutionary hurdles to be overcome
in shifting from one habit to the other. Regarding deciduousness, the
presence and life cycles of pathogens may play a role, and we now
consider a probable example.

\textbf{2.3.1.1 The poplar rust case}

A clue came when two poplar (\emph{Populus} ) leaf rusts, caused by
\emph{Melampsora medusae} Thum. and \emph{M. larici-populina} , reached
Australia and thence New Zealand in 1973 (Van Krayenoord et al. 1974;
Wilkinson and Spiers 1976; Spiers 1998). These fungal pathogens, between
them, severely affected most of the planted poplar clones in both
countries. While \emph{M. medusae} can only affect poplar, \emph{M.
larici-populina} has a potentially complex life cycle, which in its most
complex form is illustrated in Figure 1. While the poplar hosts are in
leaf, both these rusts spread by urediniospores (asexual spore stage) ,
this spread being polycyclic with repeated cycles of infection within
the season. At the start of the autumn, thick-walled, dikaryotic
teliospores are produced by \emph{M. larici-populina,} which overwinter
on fallen poplar leaves and begin the sexual stage of the life cycle.
Teliospores germinate in spring, producing basidiospores that infect the
alternate, conifer host, generally larch (\emph{Larix} sp.). Infection
of poplar from mid-spring begins from aeciospores, produced on the
conifer. This completes the sexual stage of the life cycle, starting
afresh the polycyclic seasonal build-up of infection. Where the conifer
host is not present, however, some overwintering of the uredinial stage,
either on persisting poplar leaves in mild climates or possibly as
mycelia within dormant leaf buds, can start the build-up (Walker et al.
1974; Wilkinson and Spiers 1976; Barres et al. 2012; Albornoz et al.
2018). In a co-evolved host/pathogen relationship involving such leaf
rusts, there should be a comparatively slow build-up of infection during
the growing season. However, overwintering cycles of urediniospore
production would accelerate the new seasonal build-up. In New Zealand, a
semi-evergreen mutant clone (cv. Sempervirens) of the Lombardy poplar
(\emph{Populus nigra} L. cv. Italica) had been widely planted, being
often favoured for orchard shelterbelts. This had originated in Chile as
a somatic mutation. Its widespread presence, with the semi-evergreen
habit and the inherent susceptibility to \emph{M. larici-populina} (but
not to \emph{M. medusae} ), exacerbated the initial rust epidemic. Where
winter conditions are suitably mild to allow retention of leaves, the
all-year presence of infected leaves assured a continuing supply of
urediniospores, favouring a far quicker build-up of infection in the new
season than would be expected from deciduous material. Aided by this
quick build-up, \emph{M. larici-populina} spread rapidly and widely,
defoliating poplars susceptible to both rusts, while\emph{M. medusae}
unable to build up inoculum in the winter was outcompeted and remained
restricted in distribution (Wilkinson and Spiers 1976). The
semi-evergreen clone was very severely affected, and was soon almost
eradicated, which presumably contributed to the rusts becoming less
serious a few years after arriving. Other contributing factors would
have included felling of trees of other severely affected cultivars, and
a spontaneous proliferation of hyperparasitic and otherwise antagonistic
microorganisms in phyllosphere communities on the leaf surfaces (Heather
and Chandrashekar 1982)\textbf{.}

The semi-evergreen cultivar shared the inherent susceptibility to
infection with the original deciduous cultivar. That susceptibility,
however, has exposed a potential danger of an evergreen habit in
reducing protection from natural delays in the seasonal build-up of
infection. Such a reduction can be expected to increase the level of
resistance required for field fitness. That would increase selection
pressures imposed by rusts, which operate alongside all the other
selection pressures. Since increased selection pressure on any trait
tends to reduce the possible selection intensity for other traits, that
means a potential for 'selection overload'. Moreover, the poplar rust
pathosystems are very complex (e.g. Barres et al. 2012; Persoons et al.
2014; Albornoz et al. 2018), with a potential to be very dynamic and
readily destabilised. Table 1 summarises the expected impacts of rust on
the poplar host, in scenarios varying according to: severity of winter,
presence of absence of alternate (conifer) hosts, and decidousness or
evergreenness. Figure 2 outlines expected functional interplays, under a
mild climate, between evergreen/semi-evergreen habit, growth potential,
infection level and host performance,

Co-adaptation between rusts and poplars has tended to arise in climates
that have severe or moderately severe winters. Thus, the mild climates
of New Zealand and Chile are not the norm for the natural pathosystems.
Yet these novel conditions outside climatic norms that provide an
opportunity to examine the action of pathogens as evolutionary drivers
influencing the persistence of deciduousness. Testing our hypothesis,
and whether an evergreen poplar could ever be ecologically fit, however,
faces major practical obstacles. Ideally, a population of evergreen
genotypes, rather than just one, should be used for comparison with
deciduous genotypes. However, there is no easy pathway to obtaining such
a population. Even using the existing semi-evergreen clone would be
suspect, because it might not match young seedlings, from which native
poplars grow, for susceptibility to the pathogen within the growing
season. Indeed, any matching of comparison material for inherent
susceptibility would be challenging. Field testing would be wanted,
where natural pathogens would be present. The impact of the pathogen(s)
would need to be evaluated, most likely over several years as most
impacts from rusts occur after repeated seasons of infection. Evaluating
impact is likely to be complicated by the fact that presence of a
susceptible evergreen host will likely influence disease development and
impact on deciduous genotypes. Pathogen dispersal between stands could
similarly complicate the picture. To manage these challenges, chemical
control (or some effective but targeted biocontrol) of the pathogen(s)
would need to be used to exclude rust impacts from a subset of trees.
Support for our hypothesis would be obtained from the persistence of
susceptible evergreen genotypes, and the relative success compared to
susceptible deciduous genotypes, where the pathogen impacts are excluded
from both, and the decline and eventual extinction of evergreen
genotypes where pathogen impacts are not prevented.

\textbf{2.3.1.2 Some deciduous tropical trees}

Some deciduous tropical tree species behave very counterintuitively in
producing fresh foliage before a dry season ends (e.g. Frankie et al.
1974; Borchert and Rivera 2001; Kushwaha et al. 2015). A specific case
is \emph{Faidherbia albida} A. Chev. (apple-ring acacia), a widely
distributed, deep-rooting tropical tree species of Africa, found with
annual rainfall of 200\selectlanguage{english}-500 mm. It flushes vegetatively during the dry
season, but sheds its leaves during the rains (Huxley 2001), yet it
flowers at the end of the wet season. Accounting for such
counterintuitive behaviour is a challenge, but it is hard to see a
convincing alternative to the postulate of pathogens driving a shift to
deciduousness. Actual support for the postulate would come if, when such
species are grown with no dry season, the new foliage suffered from
pathogens. The success of such a study, however, would depend on both
the presence of the appropriate pathogens and the nature of the triggers
for shedding old leaves and producing new ones. An alternative driver,
namely increased herbivory pressure during the wet season, seems very
unlikely in these cases\textbf{.}

Suggesting a similar explanation are some results of Frankie et al.
(1974), for ``Wet'' forests in Costa Rica, where dry seasons would not
be severe and not generally associated with actual deciduousness. They
noted ``Most Wet forest species flushed large quantities of new leaves
during the first dry season.''

\textbf{2.3.1.3 Evolutionary barriers to switches of habit}

The \emph{Melampsora} story raises two questions: (1) whether the
influence of pathogens serves to maintain a habit, or drives switches
from one to the other; and (2) if the latter, in what direction? It was
long ago proposed (e.g. Holttum 1953; Axelrod 1966) that the deciduous
habit arose as a defence against seasonal stresses. But, once
established, it may persist, in a state of `biotic lock-in', due to
factors like the behaviour of \emph{Melampsora} rusts. Answers to both
questions, however, depend on the evolutionary hurdles facing the
respective switches.

The evolutionary hurdles for a shift in habit will differ between the
directions of switch. A related question is what factors, in what
combinations, may either drive a switch or prevent one? Another question
involves relationships between individual fitness and population
fitness. An evolutionary switch from a deciduous to an evergreen habit
might be expected to be favoured by a mild climate, imposing no
stringent requirements for anatomical and physiological adjustments to
abiotic factors. However, it would likely require adjustment to biotic
factors. These might include enhanced morphological, anatomical or
chemical defences against herbivores, or evolution of greater pathogen
resistance. A mild climate, if humid, tends to favour various fungal or
oomycete pathogens, creating a need for greater resistance. Thus, an
evolutionary inertia may work against a switch to an evergreen habit. A
potential corollary to that is restriction of the host's geographic
range to where deciduousness does not incur a decisive competitive
disadvantage.

In a co-adapted relationship between a temperate-zone evergreen host and
a pathogen, the likely gains from becoming deciduous in avoiding
infection pressure appear minor, especially compared with the selective
and energetic costs of acquiring the habit. With a new pathogen
arriving, the comparative fitness advantages and selective costs can
change radically, as with \emph{Melampsora} . This risk is much elevated
by increasing human influences, from long-distance trade and travel.

\textbf{2.3.1.4 Discussion}

We are not postulating that pathogens have necessarily created a biotic
lock-in of deciduousness, but rather that the evolutionary inertia may
have been decisive in some cases but not others. The evolutionary
outcome could likely be influenced by various factors, including details
of the pathogen life cycle. Possibly relevant details include: longevity
of fungal fruiting bodies, level of host specificity, and absence or
presence of alternate hosts. If alternate hosts exist, whether they are
obligate, and what phases of the pathogen life occur in which host, are
also likely to be relevant. A useful framework to examine these complex
co-evolutionary dynamics that includes the context of abiotic factors is
the `disease triangle' (Stevens 1960), which illustrates the interplay
between host, pathogen and environment, and their respective interaction
and influence on disease and impact upon the host (Figure 3).

The story for tropical tree species does appear to be different. The
production of foliage during the dry season in some species suggests
strongly that, if pathogens are a selective force, they would have
sometimes driven a switch to deciduousness.

The picture concerning the general incidence of deciduousness among
woody perennial taxa is mixed. Conifers, which represent the ancient
taxon, are very predominantly evergreen, suggesting profound
evolutionary inertia against a shift to deciduousness. One exception is
the entire genus \emph{Larix} , within the Pinaceae, being deciduous.
The remaining exceptions are all Taxodiaceae members of the
Cupressaeae/Taxodiaceae complex, namely the genera \emph{Taxodium}
,\emph{Glyptostrobus} and \emph{Metasequoia} , although \emph{T.
mucronatum} Ten. is semi-deciduous. They also tend to have few
pathogens, along with some other taxonomically isolated species. Among
angiosperms, which are evolutionarily more recent, deciduousness is far
more common, in numbers of species if not in percent of total species.
Even with genera, sympatric species can include both deciduous and
evergreen members. This is so with \emph{Nothofagus} in South America
(as already mentioned), and \emph{Quercus} in North America (where some
species are semi-evergreen/deciduous) and the Mediterranean basin.
Overall, the general incidence of deciduousness among taxa argues
against any completely overriding influence of abiotic environment or
taxonomic lineage \emph{per se} .

\textbf{2.3.2 Swiss needle cast and Douglas-fir}

With native populations of Douglas-fir (\emph{Pseudotsuga
menziesii}(Mirb.) Franco in western north America, dates of spring bud
burst show a coast-to-inland gradient from the Pacific coast. At a given
elevation bud burst comes earlier the further from the coast (Campbell
and Sugano 1979). This has been observed not only \emph{in situ} but
also in common-garden experiments, ruling out a simple effect of cooler
coastal temperatures caused by the cold ocean current. One possible
reason is that coastal populations have a longer humid season in which
to complete vegetative growth and cone ripening, especially compared
with more easterly populations where summer drought starts earlier (cf
Campbell and Sorensen 1978). Another possible factor may be less
insolation early in spring. Both factors might reduce the advantages of
early bud burst in coastal populations. Yet another possibility, not
mutually exclusive, is that later bud burst there escapes the worst of
the seasonal hazard, created by humidity, of infection by foliage
pathogens. Of such pathogens the most prominent is \emph{Phaeocryptopus
gaeumannii}(T.Rohde) Petrak, cause of Swiss needle cast (Boyce 1940;
Mulvey et al. 2013), which is most aggressive in the humid coastal
climates. Given the postulated selection pressure imposed by the
pathogen, one might expect fog-belt Douglas-fir grown in very mild
climates without the pathogen to show a genetic shift to earlier bud
burst. However, any such study would both be long-term and face the
difficulty of finding anywhere that will remain free of the pathogen.
Chemical control of the pathogen would need to be long-term and is
expensive, and could be complicated by the pathogen evolving resistance.

\textbf{2.3.3 Two \emph{Pinus}species}

Two closely related coastal California pine species appear to be another
case in point. They are \emph{Pinus radiat} a D.Don (either Monterey
pine or radiata pine) and \emph{P. muricata} D.Don (bishop pine or
muricata pine). They have overlapping (but almost entirely allopatric)
geographic distributions. \emph{Pinus radiata} ranges discontinuously
from 28\selectlanguage{english}-37degN, and \emph{P. muricata} discontinuously from
31\textsuperscript{1}/\textsubscript{2}\selectlanguage{english}-41degN. \emph{Pinus radiata} has a
very long, opportunistic growing season, being able to make growth all
year if temperatures permit, which evidently accounts for a very fast
growth potential (e.g. Burdon 2001; Burdon et al. 2017). By
comparison.\emph{P. muricata} makes minimal shoot elongation during
winter, with apical buds remaining sealed, and is slower growing.
Correspondingly, it has a later pollination season. These species are
naturally challenged by strongly overlapping sets of pathogens, notably
ones causing needle casts and shoot galls.

\textbf{2.3.3.1 Needle casts}

\emph{Pinus radiata} , when grown in the British Isles, is very subject
to a foliage disorder called ``yellows'' (Lally and Thompson 2000;
Fennessy et al. 2012). This is very severe needle cast, which was
eventually linked to the fungus \emph{Cyclaneusma minus} (Butin) DiCosmo
after problems with false negative isolations. The disease occurs after
long spells of mild, cloudy weather in winter and early spring which
mean very low insolation at such latitudes. Similar needle casts have
occurred in New Zealand, associated with prolonged very wet and mild
winter weather. One of these has been attributed to \emph{C.
minus}emerging from latent pathogen status to cause ``spring needle
cast''. Another, called ``physiological needle blight'', has been
unexplained but is now suspected to have been caused by the
oomycete\emph{Phytophthora} \emph{kernoviae} Brasier, Beales \& S.A.
Kirk (McDougal and Ganley 2021). Yet another, ``red needle cast'', has
been associated mainly with \emph{Phytophthora pluvialis} Reeser, Sutton
\& Hansen and to a lesser extent with \emph{P. kernoviae} (Fraser et al.
2020). Such weather, with temperatures allowing growth but with low
insolation restricting photosynthesis, is likely to deplete the
carbohydrate reserves that would help the host resist pathogens. By
comparison, the more winter-dormant Guadalupe Island provenance
of\emph{Pinus radiata} is less prone to yellows (Fennessy et al. 2012)
than cultivated \emph{P. radiata} stocks of mainland California origin.
Also, northern populations (Lat. \textgreater{}38degN in California)
of\emph{P. muricata} , which is much more winter-dormant, are far less
subject to such needle casts. While this comparison involves both
species as exotics, rather than in natural habitats, it suggests that
pathogen pressure can favour winter quiescence despite winter
temperatures that permit active growth. That said, \emph{P. radiata}must
suffer very severe needle cast before it is outgrown by \emph{P.
muricata} (Ades et al. 1992; Burdon and Low 2020). In the northern
populations of \emph{P. muricata} , however, selective pressures imposed
by such foliage pathogens may have favoured winter dormancy. Winter cold
in their coastal environments seems unlikely to be a strong selective
force, especially as \emph{P. radiata} (of origin
36\textsuperscript{1}/\textsubscript{2}\selectlanguage{english}-37degN) is notable for
growing-season frost tolerance (ca - 6degC). This tolerance exceeds that
of material derived from one such \emph{P. muricata} population (Lat.
39\selectlanguage{english}-39\textsuperscript{1}/\textsubscript{2}degN) (Menzies \& Holden 1981).

\emph{2}\textbf{.3.3.2 Western gall rust}

A prominent shoot pathogen affecting pines within and beyond the natural
ranges of \emph{P. radiata} and \emph{P. muricata}
is\emph{Endocronartium harknessii} (J.P. Moore) Hirats. which causes
western gall rust (Old 1981; Ramsfield et al. 2007). It infects soft,
elongating shoots during spring to early summer. In certain years, when
cool, moist conditions persist during the infection season, abundant
`wave year' infection can occur. We suggest that the late flushing in
the northern populations of \emph{P. muricata} , while it may reduce
growth potential, reduces exposure to infection hazard, in a trade-off.
By comparison \emph{P. radiata} , with its earlier shoot flushing, is
vulnerable to infection over a longer season, although its dryer
habitats, all south of San Francisco Bay, mean that infection hazard is
lower. The fitness advantage of the greater growth potential of \emph{P.
radiata} resulting from the longer growing season, maybe with some
enhanced genetic resistance, evidently outweighs the fitness cost of the
associated extension of the infection season in its habitat. The fitness
cost of susceptibility is likely mitigated by susceptibility being
largely confined to young trees (Old et al. 1986) which often arise at
high density from stand-replacing fires. Selection for resistance, with
gall rust infections affecting competitive ability, thereby contributing
to the natural self-thinning, would represent essentially `soft'
(density-dependent) selection.

2\textbf{.3.3.3 Discussion}

There is thus reason to suspect that both foliage pathogens and western
gall rust have imposed selective pressures contributing to the
comparative seasonal phenology of \emph{P. radiata} and northern
populations of \emph{P. muricata} . Problematically, however, this
interpretation does not account for the flushing and pollination dates
of the southern populations of \emph{P. muricata} (\textless{}37degN).
Brown (1966), recording pollination dates, which are also a reliable
proxy for flushing dates, observed later pollination than in these
populations than in \emph{P. radiata} , although those populations flush
earlier than the northern populations. These populations are also
acutely susceptible to foliage disease (Ades et al. 1992; Burdon and Low
2020) but are naturally exposed to low disease hazard. Brown's
observations were made in an essentially common-garden situation near
Canberra, Australia. There is only one location, Monterey, where the two
species naturally co-occur, and different pollination dates are
putatively an adaptive crossing barrier there. Later pollination than
in\emph{P. radiata} in other southern populations of \emph{P. muricata}
, however, is not so readily explained, although it did not closely fit
a clinal pattern. Moreover, the coolness of the trial site, near
Canberra, may have distorted the comparative phenology of the southern
populations.

\textbf{2.3.4}

Quercus petraea

Flushing date can also involve a trade-off in defences between climatic
and biotic factors. An example has been documented for sessile oak
(\emph{Quercus petraea} (Matt.) Liebl.) in the Pyrenees mountains
(Desprez-Loustau 2010; Dantec et al. 2015). The abiotic factor is late
spring frosts, and the biotic factor is oak powdery mildew (caused
by\emph{Erysiphe quercicola} Takam. et al.). Late flushing is a defence
against the frosts, whereas early flushing helps protect against the
mildew. At higher altitudes, where late frost represents the main
adaptive hazard, late-flushing genotypes are favoured. At lower
altitudes, which are more conducive to the powdery mildew but less
subject to late frosts, early-flushing genotypes are favoured. Indeed,
the greatest incidence and severity of disease occur at intermediate
altitudes. With the trade-off meaning no closely defined or
geographically broad optimum for flushing date, the large tree-to-tree
variability in flushing date, especially at lower altitudes (Alberto et
al. 2011), is not surprising. Some validation of the interpretation
could in principle be obtained by studying the impact of chemical
control of the pathogen, but such a measure faces prohibitive practical
difficulties.

\textbf{2.3.5} \textbf{Pathogen-induced perturbations of phenology}

In addition to putative cases of pathogens operating as selective
influences on natural seasonal phenology, pathogens can exert more
direct phenotypic effects on features of the underlying seasonal
phenology of the hosts. Classically, foliage infection is a widespread
cause of premature leaf fall. Such cases generally entail hosts
responding to infection by abscission of foliage or foliage structures.
The responses can be adaptively significant, as defence mechanisms for
the hosts (Fraser et al. 2016). In some cases, shedding infected foliage
may remove inoculum, as well as possibly denying a pathogen further
sustenance. This appears to be so in the case (already mentioned) of
needle cast associated with \emph{Cyclaneusma minus} in pine species. In
some other cases, prompt shedding of foliage can prevent dangerous
spread of the pathogen within the host. With white pine blister rust,
caused by \emph{Cronartium ribicola} J.C.Fisch., prompt abscission of
infected fascicles can serve as an effective resistance mechanism in
both \emph{Pinus monticola} Douglas \emph{ex} D.Don (Hoff and McDonald
1971) and \emph{P. armandii} Franch (Hoff and McDonald 1975). The effect
of a plant-pathogen interaction at the level of a plant may differ from
the impact on individual infected tissues; for example, powdery mildew
infection of pedunculate oak (\emph{Q. robur} ) leaves resulted in
earlier senescence, but higher average infection promoted later autumn
phenology in those seedlings overall (Mutz et al. 2021). While
infection-related foliage abscission typically shows seasonality
governed by infection and/or sporulation cycles of the pathogens, along
with seasonal fluctuations in the host's carbon economy, this does not
mean that the abscission is intrinsic to the host's seasonal phenology.

In contrast to infection-triggered foliage abscission, infection of
larch (\emph{Larix} ) foliage by \emph{Hypodermella laricis} Tuboef can
stop natural abscission, thereby keeping the foliage as a continuing
source of inoculum (Cohen 1987).

\textbf{2.4 Herbivory as a putative driver}

\textbf{2.4.1 Woody perennials}

It has been noted that the timing synchronisation of seasonal flushing
can represent a balance between the advantages of flushing as soon as
conditions favour growth and the safety of delaying it until after
almost all threat from climatic damage. In temperate zones, where
seasons are defined primarily by temperatures, the classic danger is
late (spring) frost. However, it is unclear whether close
synchronisation of flushing is necessarily an adaptive consequence of
meeting that balance. An alternative interpretation is that close
synchronisation of bud burst and shoot and leaf extension means a brief
period of `predator satiation' or `predator swamping' (cf Emlen 1966;
Molles 2002) This would represent the period of maximum food value for
browsers or other herbivores, after which the food value declines
sharply. That decline, if it helps to limit the herbivore carrying
capacity of an ecosystem, also represents a feedback mechanism to reduce
browsing pressure. That, in turn may reduce the ecological importance of
other defences against herbivory. A question arising with deciduous
woody perennials, is whether, or how much, any such predator-satiation
defence may be incidental to the advantage of quick and complete
seasonal restoration of photosynthetic capacity The \emph{Quercus
petraea} /powdery mildew case, with tree-to-tree variation in flushing
date, suggests that it is not entirely so.

With evergreens, in which complete seasonal restoration of
photosynthetic capacity is not an issue, the expected premium for
earliness of flushing is less. In this connection, while apparently not
documented, the very brief flushing periods of some conifers, notably
some firs (\emph{Abies} spp\} in very mesic habitats, strongly suggests
a predator satiation strategy. Proving the postulate, however, is far
more difficult than proposing. But there would be scope for documenting
the phenology in relation to climate and moisture status, which could
provide evidence against a simple climatic explanation.

Synchronisation of flowering has its own advantages, for efficiency of
pollination, but it can also create a brief superabundance for
herbivores. This could be another `predator satiation' situation (cf
Emlen 1966; Molles 2002), but Ims (1990) concluded that for this to
operate the reproductive synchrony needs to spread across subpopulation
units. Similarly, synchrony may militate against a build-up of pathogens
that specialise on reproductive structures.

For the tropics, where seasonal effects are often dominated by wet or
dry seasons rather than temperatures, the flushing behaviour can be more
complicated than in temperate regions. There, the likely role of
herbivory as a phenotypic driver has attracted more attention. Lamarre
et al. (2014) report a study, and cite a number of others, of
``synchrony of leaf production'' in relation to herbivory. The situation
represents widespread operation of predator satiation within the
tropics. The story, however, can be more complicated. Aide (1992)
documents a case of a woody shrub flushing outside the wet season, at a
time when herbivore density is low, in `herbivore escape'. But that
species also has brief and intensive flushing and flowering, which is
consistent with an element of predator satiation. One may suggest that
in herbivore escape the species benefits from an outlier status. Such a
status can occur among the typically numerous woody species of tropical
forests. In this connection, Bagchi et al. (2014) have documented how
``negative density dependent'' selection pressures from pathogens can
tend to favour high species diversity.

Table 2 summarises, very broadly, inferred levels of alignment between
predator satiation and optimisation of growth/competitive ability in
temperate and tropical zones.

\textbf{2.4.2 Non-woody plants}

Outside woody perennials trees, three cases are adduced for herbaceous
plants, two for pasture plants, and one for a collection of species in a
Mediterranean climate. In one pasture-plant case, the seasonal
phenology, seemingly driven by climate, may actually be driven largely
by biotic factors in conjunction with climate. Key aspects of
pasture-plant phenology are seasonality of forage growth and flowering.
An extended growing season, meaning extended forage production, is
widely sought by plant breeders. However, there is classically a
trade-off between a long growing season and the persistence that avoids
a need for frequent sowings to ensure sward renewal.

\textbf{2.4.2.1 \emph{Medicago}}

Cold tolerance is typically associated, among populations, with level of
winter dormancy, suggesting that active winter growth is physiologically
incompatible with cold tolerance. Yet Daday (1964) observed otherwise.
He studied geographic races of \emph{Medicago sativa} L. (lucerne or
alfalfa). Among the races, he found the expected picture of a close
association between level of winter dormancy and cold tolerance,
admittedly not with severe winters. But, in the F2 and F3 generations of
an interpopulation diallel cross that association broke down. This
independence of inheritance of the two traits conflicted strongly with
accepted doctrine, yet no attempt to ascertain its underlying
evolutionary significance appears to have been published. We postulate
that the observed winter dormancy was in large measure a defence against
browsing pressure, rather than being a directly climatic adaptation.
Grazing pressure would be intense in winter, and very depleting of the
plants' resources if they were making active growth, presumably leading
to selection for winter dormancy. With severe winters, however, dormancy
would likely be physiologically obligate, but that would not preclude
breeding to extend autumn growth (Castonguay et al. 2006). Our
hypothesis could be experimentally probed by studying the effect of
winter grazing pressure on persistence of plants that maintained varying
levels of winter growth. With suitable material available that should be
readily feasible. Assembling suitable material might be a challenge, and
an area of ground would need to be available. Actual grazing would
require livestock, but grazing might be simulated.

\textbf{2.4.2.2 Pasture grasses}

In the other case involving pasture plants, namely forage grasses, a
biotic driver of phenology has been long recognized, at least
implicitly. A key phenological trait is the heading season, involving
the seasonal timing and duration of seed-head development.

Late and brief heading and a semi-prostrate habit are features of
persistent `pasture type' cultivar strains, bred from material with an
ancestral history of adaptation to intense grazing (e.g. Charles 1961).
By contrast, `hay type' strains do not have the same history of
adaptation to grazing. They have earlier and longer heading seasons and
a more erect habit, and much less sward persistence.

\textbf{2.4.2.3 Other plants}

Much more recently, Waterton and Cleland (2016) studied six local and
six non-local plant species grown in a common Californian Mediterranean
climate where two species of rabbit applied herbivory pressure. In the
absence of the herbivores early seasonal commencement of growth (shown
by the non-local species) conferred a productivity advantage, but with
herbivory delayed commencement was associated with an advantage. Thus, a
delay was evidently a defence against herbivory, in a classic trade-off
between defences and growth potential (cf Loehle \& Namkoong 1987;
Strauss et al. 2002).

\textbf{3. Ontogenetic phenology}

Apart from the progression with size and/or age to reproductive
competence, the process of maturation can entail radical differences
between juvenile and adult habits, in a phenomenon called heteroblasty.
This is common and often very pronounced in the New Zealand flora
(Greenwood and Atkinson 1977). Elsewhere, less extreme differences
between juvenile and adult habits are generally the norm for woody
perennials. Even vegetatively, maturation can bring some changes in
seasonal phenology, very often in a progressively stronger expression of
the seasonal phenology (e.g. Wareing 1958; Norskov-Lauritsen 1963;
Burdon 1994).

\textbf{3.1} \textbf{New Zealand flora}

The heteroblasty in various New Zealand trees and shrubs has been
postulated as a defence against vertebrate herbivory (Greenwood and
Atkinson 1977). Specifically, various such plant species have a juvenile
habit with a tangle of thin, wiry stems bearing very small leaves. This
habit is seen as being unrewarding for the large, flightless birds that
were the ground-dwelling browsers, or else resilient to browsing damage.
Despite controversy, and difficulty of proof because those browsers are
extinct, definite support for the postulate has been obtained. In a
neighbouring island flora, with closely related taxa but historically
lacking those birds, there is not the same heteroblasty (Greenwood 1992;
Burns and Dawson 2009). Other, if less striking cases of heteroblasty
conferring defences or resilience against ground-dwelling herbivores
include the production of sharp spines on foliage or stems during a
juvenile phase. Seedlings of the apple tree are a well-known example of
spines being confined to the juvenile phase.

\textbf{3.2 Two pines}

In the main landmasses mammals are typically the main ground-dwelling
browsers. While extreme heteroblasty is seldom evident as it is in New
Zealand, there are cases where ontogenetic phenology can be interpreted
in terms of changes in both palatability and browse
resilience.\emph{Pinus radiata} is an example. In it, the juvenile to
adolescent habit is bushier and more intensively branched than the adult
habit (Burdon et al. 2017), and resilience to browsing is high. The
adult habit, however, is associated with greater palatability to
ground-dwelling browsers and less resilience. This is notoriously
evident in adult-phase scions grafted for seed orchards onto small
seedlings, the scions attracting far more deer browsing than seedlings.
There is evidently a trade-off of resistance or resilience to browsing
against pathogen tolerance. Juvenile material is more susceptible to
some pathogens, notably \emph{Endocronartium harknessii} (Moore)
Hirats.) which causes western gall rust (Old et al. 1986),
and\emph{Dothistroma septosporum} (Dorog.) M. Morelet (syn. \emph{D.
pini}Hulbary) (Burdon et al. 2017). Losses of some individual seedlings
to pathogens, directly or through impaired competitive ability in the
case of western gall rust, as part of density-dependent selection, may
not impair population fitness in the thickets of regeneration that often
occur naturally. However, another advantage of a juvenile phase can lie
in how strongly a longer growing season (cf Norskov-Lauritsen 1963) can
contribute to growth potential while tree growth is still partly
exponential. At least one other pine, \emph{P. taeda} L., shares the
feature of being susceptible to an important gall rust
pathogen,\emph{Cronartium fusiforme} Hedgcock et Hunt ex Cummins, in
young trees rather than later (Powers et al. 1981).

\textbf{3.3} Eucalyptus nitens

While only incidentally reported as such, \emph{Eucalyptus
nitens}(H.Deane et Maiden) Maiden is a case involving a combination of
strong ontogenetic phenology and both herbivory and pathogen attack.
This species has major geographic (provenance) variation in the duration
of juvenile foliage production (Pederick 1979). The adult phase is
subject to insect herbivory, while the juvenile phase is very subject to
a foliage disease (Johnson and Wilcox 1989). Provenance variation
evidently reflects the comparative selective pressures imposed by insect
pests and pathogens in respective habitats. Thus, provenances with
persistent juvenile characteristics, while enjoying longer protection
against insect herbivory, are vulnerable to foliage disease with warm,
humid summers. Conversely, those provenances with a brief juvenile
phase, while less vulnerable to foliage disease are more so to insect
herbivory.

\textbf{4. Individual and population fitness and some ramifications}

Relationships between individual and population fitness in this
connection can be problematic. Population fitness depends not just on
the metric values for the fitness traits in its habitat which determine
individual fitness, but also on the amount of heritable variation for
those traits. In the poplar case, key adaptive traits in the wild would
include pathogen resistance, timing of seasonal growth, and the sexual
reproductive potential that allows genetic selection to operate. Thus,
the impact of some ill-adapted segregants can be outweighed by a
concurrent incidence of segregants that excel their parents' fitness,
since the latter contribute most to the parentage of the next
generation. However, with pathogens involved, population fitness can be
complicated by the nature of infection processes. With a `polycylic'
pathogen, there can be both reinfection from within the host individual
and cross-infection between individuals. For instance, where pathogens
impair fitness, an individual becoming deciduous gains little or no
protection if the population remains evergreen and can thereby provide a
continuous supply of inoculum. In this way, becoming deciduous is
unlikely to be advantageous, unless either this results in asynchrony
between the window of host susceptibility and presence of inoculum or
individuals are too sparse to favour cross-infection. An individual
becoming evergreen, however, might impair the fitness of the rest of the
population through producing a continuous supply of inoculum, unless it
suffers so badly from internal reinfection as to incur selective
elimination. To meet that condition, internal reinfection would
presumably need to predominate strongly over cross-infection between
individuals, which may be common with polycyclic infection.

Becoming evergreen could require evolution of enhanced pathogen
resistance and/or some more direct fitness advantage of the habit.
Natural selection for resistance may be limited by `selective
opportunity cost' whereby the fitness gains from additional resistance
are in trade-off with the fitness gains from responses to other
selective pressures. Some of those gains, it may be noted, will be
needed to make good the decay of non-additive genetic components of
fitness that occurs upon sexual reproduction. Given the dynamic nature
of biotic interactions, along with pathogen mutations, natural selection
for ecological fitness can be expected to entail a ``red queen'' model
(Van Valen 1973) requiring endless genetic shifts to maintain fitness.
With long-lived perennials, however, such shifts may occur most readily
within generational cohorts, during lifespans. With the complex and
highly dynamic poplar rust pathosystem, poplar plantations have proved
notoriously vulnerable to pathotype mutations (e.g. Persoons et al.
2014). Such plantations are typically monoclonal, which makes them
convenient to produce and manage. Present understanding of pathosystems
suggests that natural populations of poplars, reproducing by seed, might
be expected to be more resilient towards the rusts. However, fully
functioning natural populations, which would provide a good basis for
comparison, are becoming increasingly scarce.

It must be noted that the biotic vulnerability of poplar plantations,
based on species that are \emph{Melampsora} hosts, contrasts with the
biotic resilience of natural stands of American (or trembling) aspen
(\emph{Popiulus tremuloides} Michaux) which are typically monoclonal
(Latutrie et al. 2015). The aspen, with different pathogens, is
evidently involved in very different pathosystems.

5. \textbf{Pre-adaptive relationships} \emph{?}

As indicated above, seasonal timing of phenological events may serve as
defence against pathogens through avoidance of infection seasons while
the plant is vulnerable. Alternatively, the timing may be a source of
vulnerability. This seems evident in some cases of freshly introduced
pathogens, rather than in historically co-evolved cases. With Dutch elm
disease, caused by ascomycete fungi \emph{Ophiostoma} spp, early bud
burst and flushing, while possibly incurring climatic vulnerability, can
evidently avoid the height of the infection season (Ghelardini \&
Santini 2009). With sudden oak death, caused by \emph{Phytophthora
ramorum} Werres et al., host vulnerability has been linked to timing of
bud burst and onset of cambial activity in the hosts (Dodd et al. 2008).
Similarly, the pathogen \emph{Austropuccinia psidii} (G. Winter)
Beenken, a rust affecting a wide range of hosts in the Myrtaceae that
has invaded parts of Asia and the Pacific, can only infect actively
flushing host tissues (Beresford et al. 2020). In each case, invasive
pathogens appear likely to place strong selective pressures on the
phenology of native host populations, and understanding the potential
for adaptive responses appears to be worth further study.

\textbf{6. Concluding}

We propose that pathogens can be strong evolutionary drivers of seasonal
phenology, especially in respect of deciduousness. This appears to be
largely novel. Some evidence is given for our proposal for deciduousness
in a temperate zone. In the tropics, the proposal is made for want of
any other satisfactory explanation. Other examples are given of how
pathogens may influence seasonality of shoot flushing, where simple
climatic explanations seem inadequate. We suggest that evolutionary
barriers can operate against a shift from a deciduous to an evergreen
habit in some temperate-zone cases.

For herbivory we have proposed that predator satiation may operate as an
evolutionary driver in addition to purely climatic adaptation to the
occurrence of winters. Herbivory is also proposed as an evolutionary
constraint on growing or flowering seasons. For the tropics, where
climates are largely characterised by wet and dry seasons, predator
satiation has already been implicitly identified as a quite common
evolutionary driver of seasonal phenology.

Ontogenetic phenology appears strongly influenced evolutionarily by
biotic factors, including both herbivory and pathogens.

How a particular situation plays out will depend on many factors,
notably the general climatic context and the constraints it imposes
(along with other environmental factors), and the nature of biotic
pressures, viz pathogens and/or herbivory. More specifically, the
factors for pathogens involve the reproductive biology of pathogens
including seasonality; the host plant ecology, in the scale from highly
gregarious to essentially solitary; and the genetic systems of both host
and pathogens. For herbivory, they include the life cycles and seasonal
abundance of insects, along with the nature and abundance of vertebrate
browsers. Not to be ignored are interactions with other plants in the
ecosystem and among herbivores.

Influences of climate are both direct and indirect, the latter category
involving how much climate favours pathogens and herbivores. With
pathogens, there is the classic `triangle' of interactions involving
host, pathogen and the environment, so the direct and indirect
evolutionary influences are in some degree interdependent. With the
poplar/\emph{Melampsora} pathosystem, a direct influence of a climate
that is milder than the native one may favour an evergreen habit. But
the indirect influence, through the effect of the same climate on the
pathogen, is likely to militate against that shift. Often, however, the
evolutionary pressures from climatic and biotic factors would be
mutually reinforcing, as in the \emph{Medicago} case.

In calling for a broad evaluation of biotic factors as evolutionary
drivers (or co-drivers) of plant phenology, the coverage is preliminary
and selective, representing an alert to the topic. Even a more
systematic literature review would still require interpretation of
individual cases. Challenges certainly exist in such evaluation. To
identify likely cases of biotic drivers, we consider it appropriate to
look largely to those who are closely familiar with individual plant
species and their ecology. Then detailed review and analysis of
available evidence is needed, but interpretation in individual cases may
still be problematic. From there, the general postulate of biotic
influences will need to be carried forward into hypotheses that are
observationally or experimentally testable. While woody perennials have
provided tantalising case histories, they can also pose major logistical
challenges in testing hypotheses.

\textbf{Data accessibility}

Not applicable, no fresh or hitherto unpublished data being involved.

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\textbf{Tables, Figures} and \textbf{Data Accessibility Statement} :

None applicable

\textbf{Competing Interests Statement}

None

\textbf{Author contributions}

RDB drafted the manuscript and made revisions, and MJB contributed
expansion and revision. Both are agreed on final content.

\textbf{Acknowledgments}

We thank Gancho Slavov for encouragement to produce this article, Alvin
Yanchuk and Dave Kelly for comments on early drafts and suggestions,
Richard Primack for providing some references, and Stuart Fraser,
Jennifer Lau and anonymous reviewers for helpful comments and
suggestions. RDB was in receipt of office facilities from Scion, and
MJB.'s contribution was covered by the New Zealand Ministry for Business
Innovation and Employment through the Science Strategic Investment Fund
(administered by Scion, the New Zealand Forest Research Institute Ltd).



\textbf{Figure captions}

\textbf{Figure 1:~} Life cycle of\textbf{~} poplar rusts in New
Zealand\emph{.~} The smaller inner circle represents polycyclic
infection of poplars by urediniospores, with the potential epidemic
period represented by the bold line, and potential for facultative
overwintering on poplar~is represented by the dashed line. Continued
cycling by~\emph{Melampsora larici-populina} ~during mild winters on
semi-evergreen poplars facilitates earlier build-up of
epidemics.~\emph{Melampsora medusea~} can only infect poplar and must
overwinter in the uredinial stage, possibly via mycelia surviving in
leaf buds.\emph{~} The larger outer circle illustrates the full
macrocyclic life cycle of~\emph{M.~larici-populina} ~involving four
additional spore stages in which the pathogen must infect the alternate
host (conifers, primarily larch (\emph{Larix~} sp.)) before the
aeciospore stage can infect poplar and resume the cyclic urediniospore
stage. This figure is based on figures presented in~Spiers (1990) and
Vialle et al. (2011). Images of hosts were sourced from the National
Forestry Herbarium, Scion. 2020. NZFRI online dataset.
nzfri.scionresearch.com, accessed in March 2022.

\textbf{Figure 2} . Flow chart showing expected countervailing
influences of mild climate with semi-evergreen habit in poplar rust
pathosystem,

\textbf{Figure 3.} Diagram outlining interplays between factors in the
`triangle' involving host plant, pathogen and environment.

Table 1. Expected impacts of alternative poplar rust scenarios on poplar
host {[}Section 2.3.1.1{]}\selectlanguage{english}
\begin{longtable}[]{@{}llllll@{}}
\toprule
\begin{minipage}[b]{0.16\columnwidth}\raggedright\strut
\textbf{Nature of winters,} \textbf{Poplar habit}\strut
\end{minipage} & \begin{minipage}[b]{0.16\columnwidth}\raggedright\strut
\textbf{Alternate (conifer) host}\strut
\end{minipage} & \begin{minipage}[b]{0.16\columnwidth}\raggedright\strut
\textbf{Overwintering mode for rust}\strut
\end{minipage} & \begin{minipage}[b]{0.16\columnwidth}\raggedright\strut
\textbf{Spring base level of inoculum}\strut
\end{minipage} & \begin{minipage}[b]{0.16\columnwidth}\raggedright\strut
\textbf{Rate of seasonal build-up of inoculum}\strut
\end{minipage} & \begin{minipage}[b]{0.16\columnwidth}\raggedright\strut
\textbf{Impact on host}\strut
\end{minipage}\tabularnewline
\midrule
\endhead
\begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Cool to cold Poplar deciduous\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Present\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Teliospores\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Very low\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Very slow\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Mild\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Cool to cold Poplar deciduous\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Absent\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Urediniospore survival (facultative)\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Very low\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Slow to very slow\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Mild\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Mild Poplar deciduous\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Present or absent\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Urediniospores or teliospores\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Low\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Slow\strut
\end{minipage} & \begin{minipage}[t]{0.16\columnwidth}\raggedright\strut
Mild\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Mild, poplar deciduous or semi-deciduous\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Immaterial\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Continued production of urediniospores\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
High\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Very rapid\strut
\end{minipage} & \begin{minipage}[t]{0.14\columnwidth}\raggedright\strut
Very adverse\strut
\end{minipage}\tabularnewline
\bottomrule
\end{longtable}

Table 2. Inferred levels of alignment between predator satiation and
optimisation of growth potential or competitive ability {[}Section
2.4.1{]}\selectlanguage{english}
\begin{longtable}[]{@{}lll@{}}
\toprule
\textbf{Factor/Plant category} & \textbf{Temperate zone} &
\textbf{Tropics}\tabularnewline
\midrule
\endhead
Main determinant of seasons & Temperature & Rainfall\tabularnewline
Plant category & &\tabularnewline
Deciduous & Very close & Limited\tabularnewline
Evergreens & Less close & Limited\tabularnewline
\bottomrule
\end{longtable}

\textbf{Hosted file}

\verb`Putative biotic drivers Fig 1.pdf.msg`  available at \url{https://authorea.com/users/407420/articles/564019-putative-biotic-drivers-of-plant-phenology-with-special-reference-to-pathogens-and-deciduousness}

\textbf{Hosted file}

\verb`Putative biotic drivers Fig 2.pdf.msg`  available at \url{https://authorea.com/users/407420/articles/564019-putative-biotic-drivers-of-plant-phenology-with-special-reference-to-pathogens-and-deciduousness}

\textbf{Hosted file}

\verb`Putative biotic drivers Fig 3.pdf.msg`  available at \url{https://authorea.com/users/407420/articles/564019-putative-biotic-drivers-of-plant-phenology-with-special-reference-to-pathogens-and-deciduousness}

\selectlanguage{english}
\FloatBarrier
\end{document}

