Application to specific questions

The second section of this book looks to addressing specific questions with the analytical tools of temporal processes. Temporal processes take on a wider framework here than in the previous section, including consideration of internally driven fluctuations. The extent to which species aggregated within a landscape are experiencing temporal variation is likely to become an important topic in the future, and we can look forward to fruitful development of these explorations as and when they are challenged by real data from real communities.

Yoh Iwasa and colleagues and Akiko Satake and colleagues provide a tandem approach to masting, the periodic synchrony of reproduction in forest trees. Iwasa et al. first deal with masting within species, after which Satake et al. address multispecies masting. These chapters depend upon elaboration of a very simple biological model for resource reserves, the idea being that if a tree depletes its resources severely in an episode of fruiting it will have no resources to spare for reproduction for several years thereafter. The studies offer a fascinating review of complicated time-dependent phenomena emerging from a model that is very simple, both biologically and mathematically. Although not directly related to the role of environmental fluctuation in promoting coexistence, there is an indirect link: the phenomenon of masting generates a fluctuating environment for seed predators, and fluctuating levels of infestation constitute a fluctuating environment for the species of insect which prey upon the larvae that feed upon the seeds.

Introduction

This chapter differs from the main current of this volume – the identification and quantification of coexistence mechanisms associated with temporal niche dynamics – in exploring the ramifications of these processes for ecosystem ecology. The intimate link between niches and ecosystem function has long been recognised, at least in the general sense that more species, representing a greater diversity of ‘life-styles’, make more complete use of available resources and thus achieve higher levels of productivity (e.g. Preston 1948, Odum 1953, MacArthur 1955, May 1975). This broadly stated principle has been unpacked in numerous models that are more specific, for example in resource-ratio niche theory (Tilman 1982) and various forms of spatial niche theories (Loreau 1998). However, the role of temporal niches in the ecosystem context is somewhat less well developed, but critical to understanding ecological responses to climate change.

Two main features characterise worldwide, anthropogenic climate change: a general warming trend that is strongest at low latitudes and weakest at high latitudes, and complex changes in precipitation patterns, currently predicted to include reductions in precipitation at the poleward fringe of the subtropical dry belt at midlatitudes (IPCC 2007, Scheff and Frierson 2012). Both temperature and precipitation shifts, as well as their interactions, have the potential to alter environmental heterogeneity. For example, the onset of spring/summer growing seasons could be advanced (Menzel et al. 2006) and the frequency and amplitude of extreme hydrological events such as drought and flooding increased (Huntington 2006). Both temperature trends and precipitation variability are important factors in structuring temporal niches, for example by functioning as triggers of life-history events (Kelly et al., this volume, Venable and Kimball, this volume) or by controlling competitive interactions through their effects on primary production (Haxeltine and Prentice 1996). Simultaneous changes in seasonal temperature and precipitation patterns may have complex effects on populations and their interactions. Predicting such effects, and their feedbacks on climate, is one of the premiere challenges of earth system science and, in our opinion, cannot be adequately tackled without a more complete understanding of temporal niche dynamics and its role in ecosystem function.

Introduction

Masting, or mast seeding, is the synchronous seed production in certain years by a population of plants (Kelly 1994). The reproductive activity of plants in forests often fluctuates considerably between years, and flowering and fruit production are synchronised over long distances (Koenig and Knops 1998, 2000, Koenig et al. 1999).

Mast seeding has clear disadvantages such as higher density-dependent mortality of seedlings and lost opportunities for reproduction (Waller 1979). In addition, field observations suggest that seed production fluctuates more than the level that can be explained by climate-mediated variation in resource availability (Büsgen and Münch 1929). Two major questions arise from ecological studies on masting: Why is masting evolutionarily favoured regardless of apparent disadvantages? How do plants allocate resources to realise variable flowering efforts in a way synchronised over different individuals?

A family of resource budget models that have recently been studied provides answers to both questions: on the physiological mechanism by which plants may successfully generate such intermittent and synchronous reproduction (Isagi et al. 1997, Satake and Iwasa 2000, 2002a, b) and on the conditions for which masting is adaptive (Rees et al. 2002, Tachiki and Iwasa 2008). Resource budget models assume that plants accumulate resources every year and set flowers and fruits at a rate limited by pollen availability when the stored resources exceed a reproductive threshold level. The model predicts that individual plants flower intermittently when their resources are depleted after heavy flowering and fruiting, and that synchrony emerges in self-organised fashion by coupling through the need to receive outcross pollen from other plants (Satake and Iwasa 2000).

Introduction

Plant communities are structured in time as well as space. Their component species may differ in the timing of establishment, growth and reproduction both within and between years, creating temporal differences in relative abundances. Under appropriate conditions, temporal differences among co-occurring species can allow their coexistence (Grubb 1977, Chesson and Huntly 1997, Higgins et al. 2000, Kelly and Bowler 2002, 2005, Chesson et al. 2004, Schwinning et al. 2004, Adler et al. 2006). Whether or not temporal differences are responsible for the coexistence of any given pair or set of species, temporal niches are a fundamental part of community structure. Understanding this aspect of community structure is becoming even more important as we are called upon to interpret and to predict responses of communities to climate change (Dukes and Mooney 1999, Walther et al. 2002, Fischlin et al. 2007).

In this study we examine temporal variation in population dynamics in a set of eight co-occurring herbaceous perennials. In addition to examining temporal variation in population sizes (densities), we use simple population dynamic models to provide estimates of temporal variation in equilibrium population density. Because actual densities lagged equilibrium population densities, the latter were more useful for comparing the temporal niches of different species and for relating temporal variation in precipitation to population dynamics. The degree of lag itself can be interpreted as a measure of the intensity of density-dependent population regulation, and variation in the degree of lag as another aspect of a species’ temporal niche.

Introduction

Over 50 years ago, Hutchinson (1941) noted that variation in environmental conditions could alter the outcome of competition. One implication of his observation was that environmental fluctuations could promote coexistence, allowing many species to persist in a habitat where all but one would be excluded under constant conditions. By the end of the 1980s, Chesson and colleagues had clearly described the theoretical requirements for coexistence via the storage effect (Chesson and Warner 1981, Warner and Chesson 1985, Chesson and Huntly 1989). Yet despite the long history of these ideas, relatively few direct empirical tests of the storage effect exist. Studies from a variety of natural ecosystems provide partial evidence for the storage effect (Pake and Venable 1995, 1996, Kelly and Bowler 2002, Descamps-Julien and Gonzalez 2005, Facelli et al. 2005, Kelly et al. 2008), but tests of all the required conditions or quantification of the strength of the effect are much rarer (Cáceres 1997, Adler et al. 2006, 2009, Angert et al. 2009).

The lack of rigorous case studies limits our ability to generalise about the role of the temporal storage effect in maintaining diversity. We know that multiple coexistence mechanisms will operate in different communities, but currently we cannot say where the storage effect makes an especially important contribution. This information will be essential for understanding the consequences of expected increases in climate variability (Karl and Trenberth 2003, Jain et al. 2005, Salinger 2005, Allan and Soden 2008), which could impact species diversity in systems where the storage effect is important (Adler and Drake 2008). Understanding the influence of the storage effect on coexistence across a variety of ecosystems is therefore a prerequisite for anticipating future changes in species diversity.

Introduction

Nature is pervaded by variation: the physical environment is ever changing in time and in space, populations fluctuate, and no two organisms are the same. To explore natural environments is to be confronted by variation, and the science of ecology is challenged by the persistent question: is this variation more than variation itself? Environmental variation can cause population fluctuations (Ripa et al. 1998), but can it do more than this? Does it affect how organisms interact with one another? Does it shape populations and communities? How and in what ways? Biologists firmly accept that variation shapes the organisms. Heritable variation is the engine of evolution, which is fuelled by environmental change. In life-history theory, it is widely accepted that organisms show adaptations to variation in the physical environment, exemplified by evolutionary theories of iteroparity and seed dormancy (Cohen 1966, Bulmer 1985, Ellner 1985a, Real and Ellner 1992). Fundamentally, these adaptations allow species to take advantage of favourable environmental conditions without being too vulnerable to unfavourable environmental conditions.

Community ecologists have had a variety of attitudes to variation, especially variation in the physical environment (Chesson and Case 1986). Successional change after disturbance had a prominent role in the early development of plant and ecosystem ecology (Clements 1916) and now has an important role in diversity maintenance theory relying on competition–colonisation tradeoffs (Hastings 1980). Spatial variation is often assumed to provide for, and should therefore promote, species diversity (Pacala and Tilman 1994, Amarasekare and Nisbet 2001, Snyder and Chesson 2004). Although it is often assumed that regular temporal variation, such as seasonal and diurnal variation, provides for temporal niches (Armstrong and McGehee 1976, Levins 1979, Brown 1989a, b, Chesson et al. 2001), there is also much unpredictable temporal variation, such as deviations of weather and climate from seasonal averages (Davis 1986) and disturbances such as fire (Connell 1978, Bond and Keeley 2005). Should we think of this unpredictable temporal variation as disruptive to ecological processes (May 1974)? Do organisms fail to adapt to unpredictable temporal variation? Are they merely jerked around by it? Life-history theory suggests otherwise (Bulmer 1985, Real and Ellner 1992), yet conclusions are often drawn from models that reflect no such adaptations, for example Lotka–Volterra models with unpredictable environmental variation added arbitrarily (Turelli 1981, Kilpatrick and Ives 2003).

Niche dynamics

The chapters in this volume convey several important messages. Perhaps the most obvious of these is that there is mounting – and compelling – empirical evidence for the importance of temporal niche differentiation in natural communities. The contributions by Adler, Chesson et al., Fowler and Pease, Hanley and Sykes, Kelly et al. and Venable and Kimball provide strong evidence that temporal niche differentiation occurs, that it can be documented and that in at least some cases we can understand many of its mechanistic underpinnings. While there is still much to be learned, these contributions – together with earlier published work (see citations in chapters) – have established the temporal niche as a vital area of research and built a foundation for the study of temporal processes in nature.

It is essential to the better understanding of temporal process that empirical evidence continues to be developed, and with a variety of approaches. For many ecologists, temporal niches (and differentiation between them among competing species) represent something new to the way we have been accustomed to think and to conduct research. Persuading ecologists that this is an important area of research (and that temporal niche differentiation is an important part of species coexistence) is likely to require more than a single book or critical experiment, but here we present a considerable body of evidence developed in a variety of communities, using multiple approaches to make inferences.

Introduction

Desert annual plants are frequently used to illustrate the principles of adaptation to variable environments, the population dynamic functions of dispersal and dormancy, and how temporal variation may promote species coexistence (Cohen 1966, Venable and Lawlor 1980, Shmida and Ellner 1984, Chesson and Huntly 1988, 1989, Philippi and Seger 1989, Venable et al. 1993, Chesson 2000). All of these topics involve ecological and evolutionary responses to environmental variability. High levels of environmental variation driven by rainfall are a signature characteristic of hot deserts (Frank and Inouye 1994, Davidowitz 2002). Desert annuals have provided useful conceptual models because they have very simple life cycles and respond on a rapid time scale to such environmental variation (Patten 1975, Venable and Pake 1999, Venable 2007). ‘Good wildflower years’, when showy-flowered annuals blanket the desert, often occur in association with abrupt desert annual population increases. Such years are correlated with greater than average germination season rainfall and global climatic cycles, such as El Niño and Pacific Decadal Oscillations, in the case of US southwestern deserts (Cayan et al. 1999, Venable and Pake 1999, Bowers 2005). Desert annuals spend most of their lives as seeds and may even go unnoticed during their normal flowering season in years of little germination or high mortality. Persistent seedbanks play an important role in population and community dynamics, and it is not uncommon for species to reappear following years of absence.

While desert annuals are small and short lived, they occur as members of mature, persistent communities. This means that it is relatively easy to monitor multiple generations during the course of a single long-term project. Thus, in addition to being good conceptual models, desert annuals make good empirical models for exploring ecological and evolutionary dynamics in variable environments. Here, we present the results of our work combining the collection of long-term population dynamic data with several short-term focused approaches to understanding the ecology of Sonoran Desert winter annuals. We begin by introducing our study system and long-term data set, demonstrating how our data provide evidence for bet hedging and coexistence via the storage effect. Next, we describe a fundamental functional tradeoff that structures the dominant members of our community and determines the degree of interannual variation in fecundity. Finally, we explain long-term trends in response to climate change.

Introduction

The variable and synchronous production of seeds by plant populations is called masting or mast seeding and is observed in diverse forests (Kelly 1994). Many flowers and fruits are produced one year (called a mast year) but little reproductive activity occurs during the several subsequent years until the next mast year (Herrera et al. 1998, Koening and Knops 1998, 2000, Koening et al. 1999). The variance in the reproductive activity of trees between years is large. It cannot be simply a result of environmental fluctuation in annual productivity (Tamura and Hiura 1998).

Many studies on masting have focused on adaptive significance (Kelly and Sork 2002). A popular hypothesis is the predator satiation theory – that is, seed predators starve during non-mast years, while they are unable to consume all the seeds during mast years (Janzen 1971, Silvertown 1980, Nilsson and Wästljung 1987, van Schaik et al. 1993). An alternative but not mutually exclusive hypothesis is pollination efficiency: in mast years, trees receive a lot of outcross pollen, which may improve fruiting success compared with reproduction in non-mast years (Nilsson and Wästljung 1987, Smith et al. 1990, van Schaik et al. 1993, Shibata et al. 1998, Kelly et al. 2001, Rees et al. 2002, Satake and Bjørnstad 2004).

Introduction

This chapter reviews evidence concerning the vital role that temporal dynamics can have in the ecology of trees and other long-lived species in the assembly and maintenance of natural communities. The research synthesised here was stimulated by a desire to determine the action of temporal dynamics in nature, and its implications for the nature of competition, community structure and assembly on multiple scales and across a range of climatic conditions. For the most part, the results discussed concern tropical forests, but we think they provide strong support for a more general view that can be applied across biomes. Finally, we ask if there may be a potential role for temporal dynamics in speciation, in light of what we have learned from the tropical trees.

A field programme begun in the late ’90s in the tropical dry forest of México was consciously designed to study the coexistence of closely related species in a very speciose community, but the role of temporal dynamics had not been suspected and its finding was serendipitous. With centuries-long lifespans, decades-long juvenile stages and low population turnover rates, trees are problematic candidates for demographic analyses, either observational or experimental. Unless instant death is involved, the particular hurdle with trees, as with any long-lived organism, is directly connecting any specific response in the early life of the individual with the long-term individual persistence or character of the standing population. However, trees differ from many long-lived organisms in carrying their history in their structure at both the individual and population levels. Thus, a tree population itself documents individual success over the history of the population (Parker et al. 1997, Cole et al. 2011). The distribution of a population with regard to physical conditions, size and age structure and relative to other woody species all contain information on the ecology and interactions of species (e.g. Veblen 1989, 1992, Villalba and Veblen 1998, Kelly et al. 2001) and it was the age structure of populations that revealed the action of temporal dynamics at Chamela Biological Station.

Temporal fluctuations in populations can have significant consequences for the stable coexistence of competing species, as well as for the evolution of life-history traits in a number of ways. In this volume, we examine two specific products of temporal processes: reproductive scheduling and the stable coexistence of similar species. The studies contained here principally use plants to extract general principles, with the added benefit that the observed temporal processes may also be applied to a better understanding of the resource base on which depends the larger community. The range of topics dealt with here present, as a whole, a foundation of the workings of temporal processes in nature.

Temporal cycling of plant dynamics and their role in ecosystem processes and services have potential impacts up and down the foodweb (Chesson and Kuang 2008). Taken together, these studies indicate deep ties between temporal niche dynamics (sometimes just temporal dynamics, or TND for short) and a number of fundamental ecological issues. In order to make the jump to those fundamental issues we need a better handle on what drives temporal processes in nature, and the studies included here point the way to doing so. The first section of this book addresses population persistence and species coexistence regulated by environmentally generated fluctuations. The second section of this book examines plant reproduction driven by internal processes leading to synchronised, oscillating behaviour at the population and community levels – masting in forest trees.

Observing temporal processes in nature

The chapters in the first section of this book are aimed at documenting the action of temporal dynamics in natural systems. We include here an assortment of life-history types as well as both experimental and observational evidence of temporal processes.

The desert annual community of the American southwest was and is a continuing resource for investigating temporal dynamics, and two of our chapters make use of it. One advantage to this community is the short generation times of the component species – up to a year aboveground, and a few years to (at most) a few decades in the seed bank. Peter Chesson is best known for his theoretical work on the ecology of diversity, in particular the mechanism known as the storage effect, dating from Chesson and Warner (1981; citation in most chapters). Here, he and his colleagues use desert annuals and clonal perennials to apply two different approaches to testing the storage hypothesis; each is drawn largely from field observations but also includes experimental elements. Larry Venable and Sarah Kimball provide an exhaustive yet concise summary of the studies carried out by the Venable group, also in the desert annual system, over a period of some 28 years. These studies are not limited to demography but include a strong ecophysiological component, which, among other things, has allowed them to extract the effects of climate change over this period.