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.