Seed-dispersal Mutualisms Research Articles

Underpinning Plant Intelligence-A New Arena in Plant Cognition

Like other organisms plants also face crucial challenges for survival and better fitness in a wide range of ecological niches. Complex behaviors like learning, memory, information acquisition, communication, resolving problems and decision making abilities for their own benefits in an ever changing environment are also common in plants like humans and other animals. Plants sense and respond to biotic and abiotic factors of the environment to assess resources. Plants are good timekeepers as well. Without having proper brain and nervous system plants are able to interact with themselves and other organisms via chemical talking. In some plant species emissions of certain volatile chemicals during herbivore attacks are indications of social interactions. These are evidences regarding the occurrence of kin recognitions and responses in plant growth and development in complex environmental conditions. Certain species of plants show the act of mimicry. By adopting different dispersal mechanisms plant reduces parent-offspring and offspring-offspring competition. Seed-dispersal mutualism is a complex physiological interaction between plants and animals. For the last few years the relevance of plant cognition and behavioral ecology has received much attention. Collecting various sensory inputs from the surrounding environment (perception), transducing the signals within the body (cognition) and adapting various strategies plant ensures an output for better survival and reproductive fitness. All these mechanisms explore the domain of plant intelligence.

Global insights into seed dispersal mutualism with cooperative efforts and environmental variability

Seed dispersal mutualisms assume a crucial role in sustaining overall ecosystem functionality. This study extends the foundational framework of seed dispersal mutualism by incorporating animal cooperation and environmental variability. Through the integration of stability theory and phase analysis, we investigate the global dynamics of seed dispersal mutualism in deterministic environments. Theoretical findings reveal that the deterministic system exclusively exhibits equilibrium dynamics, ruling out periodic solutions and chaotic phenomena. Notably, in cases of multiple coexisting equilibria, adjacent equilibria display distinct stability properties. Furthermore, employing stochastic analysis and Lyapunov exponents, we ascertain the uniqueness of global positive solutions in the stochastic model, along with stochastic ultimate boundedness, and precise thresholds for the stochastic persistence and extinction. These results illuminate the theoretical mechanisms governing transitions in seed dispersal mutualism across various stable population levels and underscore the insights into how essential biological factors, including animal cooperation efforts and environmental variability, impact the long-term dynamics of seed dispersal mutualism.

Tipping Points in Seed Dispersal Mutualism Driven by Environmental Stochasticity

Tipping Points in Seed Dispersal Mutualism Driven by Environmental Stochasticity

Urbanisation shapes phenotypic selection of fruit traits in a seed-dispersal mutualism.

Urbanisation is currently one of the trademarks of the Anthropocene, accelerating evolutionary processes and reshaping ecological interactions over short time scales. Species interactions represent a fundamental pillar of diversity that is being altered globally by anthropogenic change. Urban environments, despite their potential impact, have seldom been studied in relation to how they shape natural selection of phenotypic traits in multispecies interactions. Using a seed-dispersal mutualism as a study system, we estimated the regime and magnitude of phenotypic selection exerted by frugivores on fruit and seed traits across three plant populations with different degrees of urbanisation (urban, semi-urban and rural). Urbanisation weakened phenotypic selection via an indirect, positive impact on fruit production and fitness and, to a lesser extent, through a direct positive effect on species visitation rates. Our results show that urban ecosystems may impact multifarious selection of traits in the short term, and highlight the role of humans in shaping eco-evolutionary dynamics of multispecies interactions.

Bearing Fruit: Miocene Apes and Rosaceous Fruit Evolution

Extinct megafaunal mammals in the Americas are often linked to seed-dispersal mutualisms with large-fruiting tree species, but large-fruiting species in Europe and Asia have received far less attention. Several species of arboreal Maloideae (apples and pears) and Prunoideae (plums and peaches) evolved large fruits starting around nine million years ago, primarily in Eurasia. As evolutionary adaptations for seed dispersal by animals, the size, high sugar content, and bright colorful visual displays of ripeness suggest that mutualism with megafaunal mammals facilitated the evolutionary change. There has been little discussion as to which animals were likely candidate(s) on the late Miocene landscape of Eurasia. We argue that several possible dispersers could have consumed the large fruits, with endozoochoric dispersal usually relying on guilds of species. During the Pleistocene and Holocene, the dispersal guild likely included ursids, equids, and elephantids. During the late Miocene, large primates were likely also among the members of this guild, and the potential of a long-held mutualism between the ape and apple clades merits further discussion. If primates were a driving factor in the evolution of this large-fruit seed-dispersal system, it would represent an example of seed-dispersal-based mutualism with hominids millions of years prior to crop domestication or the development of cultural practices, such as farming.

Invasive Drosophila suzukii outnumbers native controphics and causes substantial damage to fruits of forest plants

Impacts of biological invasions are diverse and can have far-reaching consequences for ecosystems. The spotted wing drosophila, Drosophila suzukii, is a major invasive pest of fruits, which negatively affects fruit and wine production. However, little is known about the ecological impact of this fly species on more natural ecosystems it has invaded, such as forests. In this study, we investigated the use of potential host plants by D. suzukii at 64 sites in different forest communities in Switzerland from mid-June to mid-October 2020. We examined more than 12,000 fruits for egg deposits of D. suzukii to assess its direct impact on the plants. We recorded symptoms of fruit decay after egg deposition to determine if D. suzukii attacks trigger fruit decay. In addition, we monitored the drosophilid fauna with cup traps baited with apple cider vinegar, as we expected that D. suzukii would outnumber and potentially outcompete native controphics, especially other drosophilids. Egg deposits of D. suzukii were found on the fruits of 31 of the 39 potential host plant species studied, with 18 species showing an attack rate > 50%. Overall, fruits of Cotoneaster divaricatus (96%), Atropa bella-donna (91%), Rubus fruticosus corylifolius aggr. (91%), Frangula alnus (85%) and Sambucus nigra (83%) were attacked particularly frequently, resulting also in high predicted attack probabilities that varied among forest communities. Later and longer fruiting, black fruit colour, larger fruit size and higher pulp pH all positively affected attack rates. More than 50% of the plant species showed severe symptoms of decay after egg deposition, with higher pulp sugar content leading to more severe symptoms. The high fruit attack rate observed was reflected in a high abundance and dominance of D. suzukii in trap catches, independent of forest community and elevation. Drosophila suzukii was by far the most abundant species, accounting for 86% (81,395 individuals) of all drosophilids. The abundance of D. suzukii was negatively associated with the abundance of the native drosophilids. Our results indicate that the invasive D. suzukii competes strongly with other frugivorous species and that its presence might have far-reaching ecosystem-level consequences. The rapid decay of fruits attacked by D. suzukii leads to a loss of resources and may disrupt seed-dispersal mutualisms through the reduced consumption of fruits by dispersers such as birds.

Simple Mechanisms of Plant Reproductive Benefits Yield Different Dynamics in Pollination and Seed Dispersal Mutualisms.

AbstractPollination and seed dispersal mutualisms are critical for biodiversity and ecosystem services yet face mounting threats from anthropogenic perturbations that cause their populations to decline. Characterizing the dynamics of these mutualisms when populations are at low density is important to anticipate consequences of these perturbations. We developed simple population dynamic models detailed enough to distinguish different mechanisms by which plant populations benefit from animal pollination or seed dispersal. We modeled benefits as functions of foraging rate by animals on plant rewards and specified whether they affected plant seed set, germination, or negative density dependence during recruitment. We found that pollination and seed dispersal mutualisms are stable at high density but exhibit different dynamics at low density, depending on plant carrying capacity, animal foraging efficiency, and whether populations are obligate on their partners for persistence. Under certain conditions, all mutualisms experience destabilizing thresholds in which one population declines because its partner is too rare. Plants additionally experience Allee effects when obligate on pollinators. Finally, pollination mutualisms can exhibit bistable coexistence at low or high density when plants are facultative on pollinators. Insights from our models can inform conservation efforts, as mutualist populations continue to decline globally.

Interaction between a threatened endemic plant (Anchusa crispa) and the invasive Argentine ant (Linepithema humile)

Seed dispersal mutualisms are essential to ensure the survival of diverse plant species and communities worldwide. Here, we investigated whether the invasive Argentine ant can replace native ants by fulfilling their functional role in the seed dispersal of the rare and threatened endemic myrmecochorous plant, Anchusa crispa, in Corsica (France). Our study addressed the potential of Linepithema humile to disperse elaiosome-bearing seeds of A. crispa, examining L. humile’s effects on (1) the composition of communities of ants removing seeds, (2) the number of seed removals, (3) seed preference, (4) the distance of seed dispersion, and (5) seed germination. We caught seven native species at the control site, but only the Argentine ant at invaded sites. L humile removed A. crispa seeds in greater numbers than did native ants, respectively 66 and 23%, probably due to their higher worker density. The invader was similar to native ants with respect to distance of seed transport. Finally, rates of seed germination were not significantly different between seeds previously in contact with either Argentine ants or not. Taken all together, these results suggest that the Argentine ant is unlikely to pose a threat to A. crispa population. These results have important implications for the management of this rare and threatened endemic plant and provide an example of non-negative interactions between invasive and native species.

The Strength and Drivers of Bird-Mediated Selection on Fruit Crop Size: A Meta-Analysis

Fil: Palacio, Facundo Xavier. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo. Division Zoologia de Vertebrados. Seccion Ornitologia; Argentina. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico - Tucuman. Unidad Ejecutora Lillo; Argentina

Geographic variation of fruit scents in a dispersion mutualism, the case of Ficus lutea

Chemical mediation is often involved in interactions between plants and animals, as in pollination and in seed dispersion mutualisms. Extensive investigation has been done in floral scents and on their interspecific and intraspecific variations, but similar research on fruit scent remains poorly explored and only focused on interspecific variations. We investigated in this study the intraspecific variations of volatile bouquet emitted by mature fruits of Ficus lutea, in two sites within its wide distribution range, i.e. in South Africa and in Madagascar. We demonstrated a clear geographic variation in the volatile bouquet emitted by ripe figs in these two study sites, especially due to the presence of sesquiterpenes in Madagascan bouquets, while scents present at both sites high amounts of fatty acid derivatives. We discuss here different possible explanations for such variations in fruit scents, potentially resulting from insular and/or geographic isolation. This novel result of an intraspecific variation linked to fig seed dispersion serves to increase our knowledge of the role of scents in seed dispersal mutualisms.

The geographic distribution of seed-dispersal mutualisms in North America

It is often difficult to determine the relative importance of different sorts of species interactions in shaping community structure or how communities function because we lack basic information on patterns of occurrence of biotic interactions. Here we determine the geographic distribution of seed-dispersal mutualisms across North America, and then test the hypotheses that those patterns are correlated with mean annual precipitation and latitude. We analyze the floras of 197 sites across North America to identify which species of native seed plants are dispersed by animals in one of three types of plant-animal mutualisms: frugivory, scatter hoarding, and ants. We identified 1655 plant species that are involved in these seed-dispersal mutualisms. 16.5 ± 6.5% of all seed plants across North America are dispersed by animals; 10.0 ± 4.2% by frugivores, 3.7 ± 1.7% by scatter hoarders, and 3.9 ± 2.2% by ants. Secondary dispersal by a different mode and vector (e.g., wind dispersal followed by scatter hoarding, or ballistic dispersal followed by myrmecochory) occurred in 16.8% of all plant mutualist records. Although each mode of dispersal showed a different pattern, the prevalence of seed-dispersal mutualisms increased with mean annual precipitation. The prevalence of seed dispersal by frugivory and scatter-hoarding decreased with increasing latitude. The prevalence of seed-dispersal interactions varies dramatically across North America. The center of greatest diversity for all three types of seed-dispersal mutualisms is the eastern United States, roughly coincident with the eastern deciduous forest. Knowing the distribution of species interactions improves our understanding of how the structure and functioning of communities varies across environmental gradients.

Scatter-hoarding corvids as seed dispersers for oaks and pines: A review of a widely distributed mutualism and its utility to habitat restoration

ABSTRACT Seed dispersal mutualisms with scatter-hoarders play a crucial role in population dynamics of temperate large-seeded trees. These behaviors shape seed dispersal patterns, which can be applied to conservation of populations, communities, and even ecosystems dominated by large-seeded trees. We draw on a growing body of literature to describe the ecological context and consequences of scatter-hoarding as a seed dispersal mechanism. We synthesize the quantitative literature on the interaction between members of the avian family Corvidae (crows, ravens, jays, magpies, and nutcrackers) and nut-bearing trees such as pines (Pinus spp.) and oaks (Quercus spp.) to examine unique aspects of avian scatter-hoarders as seed dispersers. During the scatter-hoarding process, seed selectivity, transportation distance, hoarding frequency, and cache placement affect seed dispersal effectiveness, a measure of the quantity and quality of dispersal. Case studies from around the world highlight the role of corvid seed d...

Parrots as overlooked seed dispersers

Parrots as overlooked seed dispersers

Fruit advertisement strategies in two Neotropical plant–seed disperser markets

Mutualisms can be seen as biological markets in which participating species exchange resources and services. Advertisements like the colors fleshy fruits are commonly used to attract mutualistic partners such seed dispersers. Although advertisements are common, the strategies employed in partner attraction and shaping the diversity of advertisements such as fruit colors remain largely unknown. Here, we adopt a market perspective on fruit color advertisement in multi-specific ensembles of fleshy-fruited plants and their avian seed dispersers. We develop and test the following non-exclusive hypotheses about fruit advertisement strategies in two Neotropical plant ensembles: (1) some low-rewarding plants offering low-energy fruits have fruit advertisements indistinguishable from those of some highly rewarding ones offering high-energy fruits thus forming possible mimicry pairs; (2) highly rewarding plants advertise their fruits with distinctive colors; and (3) fruit colors indicate the type of nutrient offered. We find support for two of the advertisement strategies. Further, we discuss how constraints on signal diversity may affect the evolution of advertisement strategies and we provide a perspective on which processes could characterize plant advertisement strategies in the biological market of seed-dispersal mutualisms.

Ant-mediated seed dispersal in a warmed world

Climate change affects communities both directly and indirectly via changes in interspecific interactions. One such interaction that may be altered under climate change is the ant-plant seed dispersal mutualism common in deciduous forests of eastern North America. As climatic warming alters the abundance and activity levels of ants, the potential exists for shifts in rates of ant-mediated seed dispersal. We used an experimental temperature manipulation at two sites in the eastern US (Harvard Forest in Massachusetts and Duke Forest in North Carolina) to examine the potential impacts of climatic warming on overall rates of seed dispersal (using Asarum canadense seeds) as well as species-specific rates of seed dispersal at the Duke Forest site. We also examined the relationship between ant critical thermal maxima (CTmax) and the mean seed removal temperature for each ant species. We found that seed removal rates did not change as a result of experimental warming at either study site, nor were there any changes in species-specific rates of seed dispersal. There was, however, a positive relationship between CTmax and mean seed removal temperature, whereby species with higher CTmax removed more seeds at hotter temperatures. The temperature at which seeds were removed was influenced by experimental warming as well as diurnal and day-to-day fluctuations in temperature. Taken together, our results suggest that while temperature may play a role in regulating seed removal by ants, ant plant seed-dispersal mutualisms may be more robust to climate change than currently assumed.

The conservation physiology of seed dispersal.

At a time when plant species are experiencing increasing challenges from climate change, land-use change, harvesting and invasive species, dispersal has become a very important aspect of plant conservation. Seed dispersal by animals is particularly important because some animals disperse seeds to suitable sites in a directed fashion. Our review has two aims: (i) to highlight the various ways plant dispersal by animals can be affected by current anthropogenic change and (ii) to show the important role of plant and (particularly) animal physiology in shaping seed-dispersal interactions. We argue that large-bodied seed dispersers may be particularly important for plant conservation because seed dispersal of large-seeded plants is often more specialized and because large-bodied animals are targeted by human exploitation and have smaller population sizes. We further argue that more specialized seed-dispersal systems on island ecosystems might be particularly at risk from climate change both owing to small population sizes involved but also owing to the likely thermal specialization, particularly on tropical islands. More generally, the inherent vulnerability of seed-dispersal mutualisms to disruption driven by environmental change (as well as their ubiquity) demands that we continue to improve our understanding of their conservation physiology.

Dispersal and predation ofEschweilera ovataseeds in the Atlantic Forest of Southern Bahia, Brazil

A majority of Neotropical rain-forest trees have fruits evolved for animal consumption suggesting that seed-dispersal mutualisms are fundamental interactions structuring these ecosystems (Howe 1986, Howe & Smallwood 1982, van Roosmalen 1985). However, whether frugivores act as seed dispersers or predators of particular plant species is unknown for most tropical trees. Trees of the family Lecythidaceae are widespread in Neotropical rain forests forming an important component of the plant community (Aparecida Lopes 2007, Mori 1990, Moriet al. 2001, Sabatier & Prevost 1990), yet studies of plant–animal interactions are few (Jorge & Peres 2005, Silvius & Fragoso 2003, Trivediet al. 2004). Results suggest that Lecythidaceae trees with zoochoric fruits are principally dispersed by bats, birds, rodents and primates (Prance & Mori 1983), although we know little about animal interactions withEschweileraseeds.

Alpine flora may depend on declining frugivorous parrot for seed dispersal

Globally, bird numbers are declining, with potentially serious flow-on effects on ecosystem processes, such as seed dispersal mutualisms. However, management to maintain seed dispersal may be inappropriate if unexpected animals are the most important dispersers. Numbers of the world’s only alpine parrot, the New Zealand kea (Nestor notabilis), have declined drastically over the last 120years after an intense period of official persecution. Today <5000kea remain in the wild. Previously it has been assumed that like other parrots, kea would destroy most of the seeds they eat, thereby contributing little to seed dispersal. The New Zealand alpine flora is rich in fleshy-fruited species yet has a limited disperser fauna. Consequently, we investigated the relevance of kea as a seed disperser in New Zealand’s alpine ecosystems. Field-based foraging observations coupled with faecal analyses showed kea were by far the most important extant alpine avian frugivore. Kea selected more fruiting species (21 vs. 17species), consumed more fruit, and dispersed more seeds (8137 vs. 795) than all other birds combined. Rates of seed predation by kea were extremely low, and evident in only 25% of species eaten. Kea are the only species that make frequent long-distance flights within and between mountain ranges. Hence, much of the effective long-distance dispersal of the alpine flora may be currently performed by kea. Conservation of kea is therefore important both for ensuring the survival of the species and for their role in seed-dispersal mutualisms for which there are few extant substitutes.

Implications of newly-formed seed-dispersal mutualisms between birds and introduced plants in northern California, USA

I examined the role of bird dispersal in invasiveness of three non-native plant species in California, USA: Triadica sebifera, Ligustrum lucidum, and Olea europaea. I selected these species because their invasiveness in California is uncertain, but a survey of ornithologists highlighted them as likely bird-dispersed. I quantified bird frugivory of these plants, compared them with a native species (Heteromeles arbutifolia), and explored the management implications of dispersal mutualisms for these and other incipient invasive plants. Fruit removal by birds was sufficient to permit spread for all study species. Seed dispersers (rather than seed predators) and pulse feeders (flocking species with potential for long distance dispersal) performed most fruit removal for the non-native species, a pattern indicative of an effective dispersal regime. The number of fruiting trees per stand was a significant predictor of bird visitation. Founding population size may thus be important in management of invasive, bird-dispersed plants. Disperser-defined niches were relatively narrow because a few disperser species performed the majority of fruit removal from study trees, but each fruit species was consumed by a variety of potential dispersers. This results in strong pairwise niche overlap between some plant species. Ordinated by bird use, study site-species combinations clustered more by geographic location than by plant species, emphasizing the opportunistic nature of bird foraging. None of the non-native focal plant species appears dispersal limited, and all have formed novel mutualisms in California. It is possible that these plants are now in lag phases preceding bird-mediated invasion. Consideration of bird dispersal when evaluating invasiveness is therefore an imperative.

Quantitative analysis of the effects of the exotic Argentine ant on seed-dispersal mutualisms

Although it is increasingly clear that exotic invasive species affect seed-dispersal mutualisms, a synthetic examination of the effect of exotic invasive species on seed-dispersal mutualisms is lacking. Here, we review the impacts of the invasive Argentine ant (Linepithema humile) on seed dispersal. We found that sites with L. humile had 92 per cent fewer native ant seed dispersers than did sites where L. humile was absent. In addition, L. humile did not replace native seed dispersers, as rates of seed removal and seedling establishment were all lower in the presence of L. humile than in its absence. We conclude that potential shifts in plant diversity and concomitant changes in ecosystem function may be a consequence of Argentine ant invasions, as well as invasions by other ant species. Because very few studies have examined the effects of non-ant invasive species on seed-dispersal mutualisms, the prevalence of disruption of seed-dispersal mutualisms by invasive species is unclear.