ABSTRACT
Synzoochory is the dispersal of seeds by seed‐caching animals. The animal partner in this interaction plays a dual role, acting both as seed disperser and seed predator. We propose that this ...duality gives to synzoochory two distinctive features that have crucial ecological and evolutionary consequences. First, because plants attract animals that have not only positive (seed dispersal) but also negative (seed predation) impacts on their fitness, the evolution of adaptations to synzoochory is strongly constrained. Consequently, it is not easy to identify traits that define a synzoochorous dispersal syndrome. The absence of clear adaptations entails the extra difficulty of identifying synzoochorous plants by relying on dispersal traits, limiting our ability to explore the full geographic, taxonomic and phylogenetic extent of synzoochory. Second, the positive and negative outcomes of interactions with synzoochorous animals are expressed simultaneously. Consequently, synzoochorous interactions are not exclusively mutualistic or antagonistic, but are located at some point along a mutualism–antagonism continuum. What makes synzoochory interesting and unique is that the position of each partner along the continuum can be evaluated for every plant–animal interaction, and thus the continuum can be precisely described by assessing the relative frequency of positive and negative interaction events in each pairwise interaction. Herein we explore these two main features of synzoochory with a comprehensive quantitative survey of published studies on synzoochory. Synzoochory has been recorded for at least 1339 plant species differing in life forms, from annual and short‐lived herbs to long‐lived trees, belonging to 641 genera and 157 families widely distributed across the globe and across the seed plant phylogeny. Over 30 animal families belonging to five disparate taxonomic groups (rodents, marsupials, birds, insects, and land crabs) potentially act as synzoochorous dispersers. Although synzoochory appears to be fundamentally a secondary dispersal mode, many abundant and dominant trees are primarily synzoochorous. In addition, we found evidence of the existence of diplosynzoochory (caching animals acting both as primary and secondary dispersers of the same individual seed), mostly in nut‐bearing trees. Finally, we found that synzoochorous interactions are widely spread across the mutualism–antagonism continuum. Nevertheless, there were some differences among disperser species and functional groups. Corvids and some rodents (cricetids, nesomyids, sciurids) were located in the positive‐effects region of the continuum and presumably behave mostly as dispersers, whereas land crabs and insects were located in the negative‐effects extreme and behave mostly as seed predators. Our review demonstrates that synzoochory is not an anecdotal ecological interaction. Rather, it is pivotal to the functioning of many ecosystems where the natural regeneration of keystone plant species depends on the activity of granivorous animals that play a dual role. This distinctive interaction should not be ignored if we wish to have an accurate understanding of the functioning of natural systems.
Growth in seed dispersal studies has been fast-paced since the seed disperser effectiveness (SDE) framework was developed 17 yr ago. Thus, the time is ripe to revisit the framework in light of ...accumulated new insight. Here, we first present an overview of the framework, how it has been applied, and what we know and do not know. We then introduce the SDE landscape as the two-dimensional representation of the possible combinations of the quantity and the quality of dispersal and with elevational contours representing isoclines of SDE. We discuss the structure of disperser assemblages on such landscapes. Following this we discuss recent advances and ideas in seed dispersal in the context of their impacts on SDE. Finally, we highlight a number of emerging issues that provide insight into SDE. Overall, the SDE framework successfully captures the complexities of seed dispersal. We advocate an expanded use of the term dispersal encompassing the multiple recruitment stages from fruit to adult. While this entails difficulties in estimating SDE, it is a necessary expansion if we are to understand the central relevance of seed dispersal in plant ecology and evolution.
A core interest in studies of mutualistic interactions is the ‘effectiveness’ of mutualists in providing benefits to their partners. In plant‐animal mutualisms it is widely accepted that the total ...effect of a mutualist on its partner is estimated as (1) a ‘quantity’ component multiplied by (2) a ‘quality’ component, although the meanings of ‘effectiveness,’ ‘quantity,’ and ‘quality’ and which terms are applied to these metrics vary greatly across studies. In addition, a similar quantity × quality = total effect approach has not been applied to other types of mutualisms, although it could be informative. Lastly, when a total effect approach has been applied, it has invariably been from a phytocentric perspective, focussing on the effects of animal mutualists on their plant partner. This lack of a common framework of ‘effectiveness’ of mutualistic interactions limits generalisation and the development of a broader understanding of the ecology and evolution of mutualisms. In this paper, we propose a general framework and demonstrate its utility by applying it to both partners in five different types of mutualisms: pollination, seed dispersal, plant protection, rhizobial, and mycorrhizal mutualisms. We then briefly discuss the flexibility of the framework, potential limitations, and relationship to other approaches.
Mutualism effectiveness, the contribution of an interacting organism to its partner's fitness, is defined as the number of immediate outcomes of the interactions (quantity component) multiplied by ...the probability that an immediate outcome results in a new individual (quality component). These components form a two‐dimensional effectiveness landscape with each species’ location determined by its values of quantity (x‐axis) and quality (y‐axis). We propose that the evolutionary history of mutualistic interactions leaves a footprint that can be identified by three properties of the spatial structure of effectiveness values: dispersion of effectiveness values, relative contribution of each component to the effectiveness values and correlation between effectiveness components. We illustrate this approach using a large dataset on synzoochory, seed dispersal by seed‐caching animals. The synzoochory landscape was clumped, with effectiveness determined primarily by the quality component, and with quantity and quality positively correlated. We suggest this type of landscape structure is common in generalised coevolved mutualisms, where multiple functionally equivalent, high‐quality partners exert similarly strong selection. Presumably, only those organisms located in high‐quality regions will impact the evolution of their partner. Exploring properties of effectiveness landscapes in other mutualisms will provide new insight into the evolutionary and ecological consequences of mutualisms.
Mutualism effectiveness, the contribution of an interacting organism to its partner's fitness, is defined as the number of immediate outcomes of the interactions (Quantity component) multiplied by the probability that an immediate outcome results in a new individual (Quality component). These components form a two‐dimensional effectiveness landscape with each species’ location determined by its values of quantity and quality. We propose that the evolutionary history of mutualistic interactions leaves a footprint that can be identified by three properties of the spatial structure of effectiveness landscapes: dispersion of effectiveness values, relative contribution of each component to the effectiveness values and correlation between effectiveness components.
What drives seed dispersal effectiveness? Nevo, Omer; Filla, Caitlynn; Valenta, Kim ...
Ecology and evolution,
September 2023, Letnik:
13, Številka:
9
Journal Article
Recenzirano
Odprti dostop
Seed dispersal is a critical phase in plant reproduction and forest regeneration. In many systems, the vast majority of woody species rely on seed dispersal by fruit‐eating animals. Animals differ in ...their size, movement patterns, seed handling, gut physiology, and many other factors that affect the number of seeds they disperse, the quality of treatment each individual seed receives, and consequently their relative contribution to plant fitness. The seed dispersal effectiveness framework (SDE) was developed to allow systematic and standardized quantification of these processes, offering a potential for understanding the large‐scale dynamics of animal–plant interactions and the ecological and evolutionary consequences of animal behavior for plant reproductive success. Yet, despite its wide acceptance, the SDE framework has primarily been employed descriptively, almost always in the context of local systems. As such, the drivers of variation in SDE across systems and the relationship between its components remain unknown. We systematically searched studies that quantified endozoochorous SDE for multiple animal species dispersing one or more plant species in a given system and offered an integrative examination of the factors driving variation in SDE. Specifically, we addressed three main questions: (a) Is there a tradeoff between high dispersal quality and quantity? (b) Does animal body mass affect SDE or its main components? and (c) What drives more variation in SDE, seed dispersal quality, or quantity? We found that: (a) the relationship between quality and quantity is mediated by body size; (b) this is the result of differential relationships between body mass and the two components, while total SDE is unaffected by body mass; (c)neither quality nor quantity explain more variance in SDE globally. Our results also highlight the need for more standardized data to assess large‐scale patterns in SDE.
Seed dispersal effectiveness (SDE) is a quantitative framework designed to quantify the contribution of animals to plant fitness. It is widely accepted but is mostly applied locally. We analyze SDE data from dozens of publications to assess what factors drive variation in SDE across systems.
In this study we assessed the effectiveness of rodents as dispersers of Quercus ilex in a patchy landscape in southeastern Spain. We experimentally followed the fates of 3,200 marked and weighed ...acorns from dispersal through the time of seedling emergence over three years. Rodents handled about 99% of acorns, and dispersed 67% and cached 7.4% of the dispersed acorns. Most caches were recovered and consumed, and only 1.3% of the original experimental acorns were found alive in caches the following spring. Dispersal distances were short (mean = 356.2 cm, median = 157 cm) and strongly right-skewed. Heavier acorns were dispersed further and were more likely to be cached and survive than lighter acorns. All caches were in litter or soil, and each contained a single acorn. Rodents moved acorns nonrandomly, mostly to oaks and pines. Most surviving acorns were either in oaks, a poor microhabitat for oak recruitment, or shrubs, a suitable microhabitat for oak recruitment. Our results suggest that rodents, by burying a relatively high proportion of acorns singly in shrubs and pines, act as moderately effective dispersers of Q. ilex. Nonetheless, this dispersal comes at a very heavy cost.
Sagebrush ecosystems of western North America are threatened by invasive annual grasses and wildfires that can remove fire‐intolerant shrubs for decades. Fuel reduction treatments are used ostensibly ...to aid in fire suppression, conserve wildlife habitat, and restore historical fire regimes, but long‐term ecological impacts of these treatments are not clear. In 2006, we initiated fuel reduction treatments (prescribed fire, mowing, and herbicide applications tebuthiuron and imazapic) in six Artemisia tridentata ssp. wyomingensis communities. We evaluated long‐term effects of these fuel treatments on: (1) magnitude and longevity of fuel reduction; (2) Greater Sage‐grouse habitat characteristics; and (3) ecological resilience and resistance to invasive annual grasses. Responses were analyzed using repeated‐measures linear mixed models. Response variables included plant biomass, cover, density and height, distances between perennial plants, and exposed soil cover. Prescribed fire produced the greatest reduction in woody fuel over time. Mowing initially reduced woody biomass, which recovered by year 10. Tebuthiuron did not significantly reduce woody biomass compared to controls. All woody fuel treatments reduced sagebrush cover to below 15% (recommended minimum for Greater Sage‐grouse habitat), but only prescribed fire reduced cover to below controls. Median mowed sagebrush height remained above the recommended 30 cm. Cheatgrass (Bromus tectorum) cover increased to above the recommended maximum of 10% across all treatments and controls. Ecological resilience to woody fuel treatments was lowest with fire and greatest with mowing. Low resilience over the 10 posttreatment years was identified by: (1) poor perennial plant recovery posttreatment with sustained reductions in cover and density of some perennial plant species; (2) sustained reductions in lichen and moss cover; and (3) increases in cheatgrass cover. Although 10 years is insufficient to conclusively describe final ecological responses to fuel treatments, mowing woody fuels has the greatest potential to reduce woody fuel, minimize shrub mortality and soil disturbance, maintain lichens and mosses, and minimize long‐term negative impacts on Greater Sage‐grouse habitat. However, maintaining ecological resilience and resistance to invasion may be threatened by increases in cheatgrass cover, which are occurring regionally.
There is growing realization that intraspecific variation in seed dispersal can have important ecological and evolutionary consequences. However, we do not have a good understanding of the drivers or ...causes of intraspecific variation in dispersal, how strong an effect these drivers have, and how widespread they are across dispersal modes. As a first step to developing a better understanding, we present a broad, but not exhaustive, review of what is known about the drivers of intraspecific variation in seed dispersal, and what remains uncertain. We start by decomposing 'drivers of intraspecific variation in seed dispersal' into intrinsic drivers (i.e. variation in traits of individual plants) and extrinsic drivers (i.e. variation in ecological context). For intrinsic traits, we further decompose intraspecific variation into variation among individuals and variation of trait values within individuals. We then review our understanding of the major intrinsic and extrinsic drivers of intraspecific variation in seed dispersal, with an emphasis on variation among individuals. Crop size is the best-supported and best-understood intrinsic driver of variation across dispersal modes; overall, more seeds are dispersed as more seeds are produced, even in cases where per seed dispersal rates decline. Fruit/seed size is the second most widely studied intrinsic driver, and is also relevant to a broad range of seed dispersal modes. Remaining intrinsic drivers are poorly understood, and range from effects that are probably widespread, such as plant height, to drivers that are most likely sporadic, such as fruit or seed colour polymorphism. Primary extrinsic drivers of variation in seed dispersal include local environmental conditions and habitat structure. Finally, we present a selection of outstanding questions as a starting point to advance our understanding of individual variation in seed dispersal.
In sagebrush ecosystems invasion of annual exotics and expansion of piñon (Pinus monophylla Torr. and Frem.) and juniper (Juniperus occidentalis Hook., J. osteosperma Torr. Little) are altering fire ...regimes and resulting in large-scale ecosystem transformations. Management treatments aim to increase resilience to disturbance and enhance resistance to invasive species by reducing woody fuels and increasing native perennial herbaceous species. We used Sagebrush Steppe Treatment Evaluation Project data to test predictions on effects of fire vs. mechanical treatments on resilience and resistance for three site types exhibiting cheatgrass (Bromus tectorum L.) invasion and/or piñon and juniper expansion: 1) warm and dry Wyoming big sagebrush (WY shrub); 2) warm and moist Wyoming big sagebrush (WY PJ); and 3) cool and moist mountain big sagebrush (Mtn PJ). Warm and dry (mesic/aridic) WY shrub sites had lower resilience to fire (less shrub recruitment and native perennial herbaceous response) than cooler and moister (frigid/xeric) WY PJ and Mtn PJ sites. Warm (mesic) WY Shrub and WY PJ sites had lower resistance to annual exotics than cool (frigid to cool frigid) Mtn PJ sites. In WY shrub, fire and sagebrush mowing had similar effects on shrub cover and, thus, on perennial native herbaceous and exotic cover. In WY PJ and Mtn PJ, effects were greater for fire than cut-and-leave treatments and with high tree cover in general because most woody vegetation was removed increasing resources for other functional groups. In WY shrub, about 20% pretreatment perennial native herb cover was necessary to prevent increases in exotics after treatment. Cooler and moister WY PJ and especially Mtn PJ were more resistant to annual exotics, but perennial native herb cover was still required for site recovery. We use our results to develop state and transition models that illustrate how resilience and resistance influence vegetation dynamics and management options.
Some studies suggest that canopy gaps are not crucial for woody species recruitment in typhoon-disturbed forests because of frequently defoliated forest crowns and invariant high-light levels under ...the forest canopy. Here we examined this speculation focusing on seedling establishment stages and forest floor light in a forest with annual return frequencies of typhoons. We monitored light (photosynthetically active radiation; PAR) and seedling dynamics in 75 seedling quadrats (each 1 × 1 m
2
) for eight years in Nanjenshan tropical lowland forest, Taiwan (2043 newly recruited seedlings; 199 advance regeneration seedlings). Due to attenuation by the understorey vegetation, only 24% of the PAR that penetrated the forest canopy reached the forest floor. We found that PAR transmittance on the forest floor was heterogeneous temporally, ranging from 0.01 to 15.6%. Nonetheless, shade-intolerant species established at relatively high median values of light transmittance, compared to species of the moderate and tolerant groups, indicating that light is a crucial resource at the establishment stage. However, many seedlings died in relatively high-light conditions, suggesting that factors other than low light were more critical for survival. The generally low-light environment on the forest floor also resulted in similar composition and slow growth of seedlings across quadrats, except for a few in extraordinary high-light quadrats. In conclusion, the temporal light environment below the understorey layer was heterogeneous and was critical for differentiated establishment and growth patterns of newly recruited seedlings. Thus, besides canopy gaps, the light attenuation effect caused by understorey vegetation plays an essential role in the early establishment stage of seedlings in a forest frequently disturbed by typhoons.
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