Ants as diaspore removers of non-myrmecochorous plants: a meta-analysis

Diaspore (e.g. seeds, fruits) dispersal is pivotal for plant communities and often involves several steps and different dispersing agents. Most studies focusing on diaspore dispersal by animals have highlighted the role of vertebrates, neglecting the role of ants in the diaspore dispersal of non-myrmecochorous plants. Diaspore dispersal by ants is especially relevant in the current scenario of declining of vertebrate populations and, consequently, collapse of the dispersal system of large-seeded plants. Although ants can never compensate for the dispersal service provided by vertebrates, they can mitigate the impact of vertebrate decline via removal of diaspores deposited on the ground. We have used a meta-analytical approach to investigate the contribution of ants in the removal of non-myrmecochorous diaspores (through vertebrate exclusion experiments). We considered the number of diaspore removal as effect size and factors such as plant growth forms, diaspore and ant size, habitat type as moderators. In addition, we investigated the role of such factors on the diaspore removal distance by ants. Ants played complementary role to non-myrmecochorous diaspore removal services provided by vertebrates (mean Hedges’ g of −0.30). The ant diaspore removal was 69% higher for diaspores from shrubs than that of tree diaspores and removal of small-sized diaspores were 69% and 70% higher in comparison to medium- and large-sized diaspores, respectively. Regarding the diaspore removal distance by ants, those of tree species were removed 32% farther than those of shrub species, and diaspores were removed three- times farther in the savanna than in rainforest ecosystems. Our results highlight the shrubs and small-sized diaspores. Regarding the diaspore removal distance, the ants can be crucial for the dispersal of tree diaspores and in the savanna ecosystems. Finally, considering the biodiversity crisis, the ants may play an even more important role than appreciated in diaspores dispersal.     

Diaspore removal and potential dispersers of the rare and protected Paeonia officinalis L. (Paeoniaceae) in a changing landscape

Paeonia officinalis L., a rare and protected species, mostly occurs in open and semi‐open habitats and is often threatened by forest and shrubland spread. To explore the still undocumented dispersal features of this species, we address the following questions. What are the relative roles of ants, small rodents, and birds as diaspore removers in open habitat and woodland? Which animal groups constitute the potential disperser assemblage and how do they shape the spatial patterns of seed dispersal? Do diaspores fit the ornithochory syndrome or do they only mimic fleshy fruits? Two experiments were performed to quantify diaspore fall and diaspore removal by animal groups, above ground and on the ground. Ants did not contribute to dispersal. In open habitats, no seed removal was detected, either on follicles or once diaspores had fallen to the ground. In woodland, diaspores were weakly removed by vertebrates on follicles and were mainly removed by rodents on the ground. As a consequence, we suggest that long‐distance dispersal events are very rare, weakening the possible escape into space of populations subject to forest spread. Several traits indicate that diaspores fit the ornithochory syndrome, but other traits are strongly reminiscent of mimetic diaspores deceiving bird dispersers. © 2007 CNRS. Journal compilation © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society, 2007, 154 , 13–25.     

Importance of elaiosome size to removal of ant-dispersed seeds

Several studies relate removal of diaspores from different ant-dispersed plant species to the size of their claiosomes. This study is the first one to relate intraspecific variation in claiosome size to removal of diaspores by ants. This approach circumvents the problem posed by interspecific variation in chemistry and morphology of elaiosomes. We used the systemHepatica nobilis Mill. (Ranunculaceae) andMyrmica ruginodis Nyl. The elaiosome was the attractive part of the diaspore and its attractiveness decreased quickly after release from the fruit. In experimental runs where ants collected diaspores, the elaiosome size of accepted diaspores was larger than of those rejected and the largest diaspores were collected first. Since size of diaspore, elaiosome and achene were correlated, the diaspores that were removed first had both the largest elaiosome and achene. However, our experiments suggested that elaiosome size was more important to removal than achene size or the elaiosome:achene size ratio. If ant dispersal improves plant fitness, elaiosome size and hence diaspore size would be expected to increase over time. However, such directional selection mediated by the ants is probably counterbalanced by the plant. Seed predators and a negative trade-off between number and size of seeds would, among other factors, select for smaller diaspore size,i.e. counteract the effect of the ants' preference for larger elaiosomes.     

Epizoochorous dispersal by ungulates depends on fur,grooming and social interactions

The transport phase of the animal‐mediated plant dispersal process is critical to dispersal effectiveness as it determines the spatial distribution of the diaspores released and their chance for further recruitment. Assessing this specific phase of the dispersal process generally requires combining diaspore retention times with the associated distances covered. Here, we specifically tested the effect of grooming behavior, interindividual contacts and ungulate fur on diaspore retention times and associated dispersal distances for the hooked diaspores of Xanthium strumarium L. experimentally attached to tamed individuals of three ungulate species. We used a comparative approach based on differing fur quality on different body zones of these three ungulates. During 6‐hr sessions, we monitored for grooming and social interactions that may induce intended or inadvertent diaspore detachment. Additionally, we proposed innovative approaches to directly assessing diaspore dispersal distances by red deer in situ. Fat‐tailed functions fitted diaspore retention time, highlighting the potential for long‐distance dispersal events. The longer the hair, the higher the retention capacity of diaspores in the animal's fur. As predicted, donkey retained diaspores longer than red deer and dwarf goat; and we also confirmed that diaspores attached to the short hair of the head fell off more quickly than did those on the other body zones. Dwarf goat groomed more often than both red deer and donkey, but also when it carried diaspores. Up to 14% of the diaspores detached from animal fur after specific grooming behavior. We observed, in controlled conditions, for the first time and for each ungulate species, interindividual transfers of diaspores, representing 5% of the diaspores attached to animals’ fur. Our results militate for incorporating animal behavior into plant dispersal modeling approaches.     

Deconstructing a floral phenotype: do pollinators select for corolla integration in Lavandula latifolia?

An experimental field study was undertaken to assess whether correlational selection generated by pollinators can account for observed phenotypic integration of the two corolla lips in the zygomorphic flowers of the insect‐pollinated Mediterranean shrub, Lavandula latifolia (Labiatae). The experiment consisted of manipulating the upper and lower corolla lips according to a two‐way factorial design with interaction, and involved the complete (lower lip) or extensive (distal two thirds of upper lip) excision of one or the two lips. Per‐flower male (proportion of pollen grains removed) and female (number of pollen tubes down the style) pollination success, and maternal fecundity (seed set), of experimental flowers were evaluated after exposure to natural pollination in the field. Artificially induced corolla variation had no significant effects on either male or female pollination success, and two aberrant floral morphologies, characterized by lack of corolla integration, had a maternal fecundity advantage over normal two‐lipped phenotypes. These results do not support a predominant role of correlational selection by pollinators in maintaining corolla integration in L. latifolia, but are instead consistent with the alternative view that integration is mainly the consequence of genetic and/or developmental factors.     

Rubovietnamia coronula sp. nov. (Rubiaceae: Gardenieae) from the Philippines

Rubovietnamia coronula Alejandro and Meve, a new coastal Rubiaceae species from Davao del Sur, Philippines is here described and compared with Rubovietnamia nonggangensis and R. sericantha. This third species of Rubovietnamia is distinct from the two known species by its long leaf petioles, prominently keeled stipules, reduced calyx and corolla, outward curling of corolla lobes in anthesal flowers, included anthers and stigma, glabrous fruits with nectariferous disk, and numerous seeds.     

D3: The Dispersal and Diaspore Database – Baseline data and statistics on seed dispersal

Seed dispersal is hard to measure, and there is still a lack of knowledge about dispersal-related traits of plant species. Therefore, we developed D³, the Dispersal and Diaspore Database (available at www.seed-dispersal.info), which aims at simplifying ecological and evolutionary analyses by providing and integrating various items related to seed dispersal: empirical studies, functional traits, image analyses and ranking indices (quantifying the adaptation to dispersal modes).Currently, the database includes data for more than 5000 taxa and 33 items as well as digital images of diaspores (i.e. the dispersal units), seeds, fruits and infructescences. The included items cover common traits like diaspore mass, size, shape, terminal velocity and seed number per diaspore. Furthermore, we present newly or further developed items like ecomorphological categorizations of the diaspore and fruit as well as information from literature on prevailing dispersal modes. Finally, we introduce several items which are not covered in other databases yet: surface structure and form of the diaspore, the exposure of the diaspores in the infructescence and dispersal rankings. Dispersal rankings allow estimations of how well certain species are adapted to a specific dispersal mode in comparison to a larger species set. They are calculated as the percentile rank of an indicator of species’ dispersal potential in relation to a larger species set.Especially for the new and further developed items we outline the basic concepts in detail, describe the measurement and categorization methods and show how to interpret and integrate these data for single species as well as for larger species sets. Thereby, we calculate baseline statistics of seed dispersal of the Central European flora. We found that diaspores of 72% of the taxa show specializations related to long-distance dispersal, i.e. most often elongated appendages or nutrient-rich tissues. Diaspore masses, sizes and terminal velocities vary over several orders of magnitude and can be approximated by lognormal distributions.     

Morphology of Heliotropium (Boraginaceae) Dispersal Units1

In flowers of Heliotropium s.l. the primary carpel tips are overtopped by commissural outgrowths. Therefore the stylar cleft mimics a lateral orientation of the carpels. In species in which the fruit splits into four diaspores the separation tissues run through both the median and the transverse fruit planes. In species where only two two-seeded nutlets are developed the fruit splits within the false septa and each half is composed of parts of both carpels (“syn-mericarpids”).     

Two‐tier morpho‐chemical defence tactic in Aethionema via fruit morph plasticity and glucosinolates allocation in diaspores

Fruit dimorphism and the production of glucosinolates (GSLs) are two specific life history traits found in the members of Brassicales, which aid to optimize seed dispersal and defence against antagonists, respectively. We hypothesized that the bipartite dispersal strategy demands a tight control over the production of fruit morphs with expectedly differential allocation of defensive anticipins (GSLs). In dimorphic Aethionema, herbivory by Plutella xylostella at a young stage triggered the production of more dehiscent (seeds released from fruit) than indehiscent fruit morphs (seeds enclosed within persistent pericarp) on the same plant upon maturity. Total GSL concentrations were highest in the mature seeds of dehiscent fruits from Aethionema arabicum and Aethionema saxatile among the different ontogenetic stages of the diaspores. Multivariate analyses of GSL profiles indicated significantly higher concentrations of specific indole GSLs in the diaspores, which require optimal defence after dispersal (i.e., seeds of dehiscent and fruit/pericarp of indehiscent fruit). Bioassays with a potentially coinhabitant fungus, Aspergillus quadrilineatus, support the distinct defensive potential of the diaspores corresponding to their GSL allocation. These findings indicate a two‐tier morpho‐chemical defence tactic of Aethionema via better protected fruit morphs and strategic provision of GSLs that optimize protection to the progeny for survival in nature.     

Spatio‐temporal pattern of specific gravity of mangrove diaspore: implications for upstream dispersal

Mangrove plants, which develop highly productive forests on tropical–subtropical coastlines and river estuaries, rely mainly on river and sea water currents for their diaspore dispersal. Mangrove diaspores are basically dispersed in brackish to sea waters; thus whether they sink or float during the dispersal period could be changed dynamically, both spatially and temporally, depending on the salinity to which they are exposed, as well as on their specific gravity (SG). We found that the SG of diaspores of two mangrove species, Rhizophora stylosa and Bruguiera gymnorrhiza, which are dominant species and form a typical zonation (B. gymnorrhiza in inland areas and R. stylosa in more seaward areas) in the study area, changed spatially and temporally. Bruguiera gymnorrhiza gradually lost its SG in accordance with elapsed time, while R. stylosa lost its SG in the first 6 h and gained gradually according to elapsed time. Hydrodynamic simulation of dispersal patterns, in combination with observed specific gravity changes of both diaspores and river water, demonstrated that the spatio‐temporal pattern of specific gravity change was closely related to the difference in dispersal behaviors between the species. The diaspore of B. gymnorrhiza generally disperses upstream, and covers wider ranges than that of R. stylosa, at least in the early phase of dispersal. These dispersal behaviors agreed well with the distribution pattern of the species across estuaries in the study site. To date, hydrochory has been considered to be a mostly passive process governed by the dynamics of water current and subsequent sediment movement, with fixed diaspore characteristics such as shape and buoyancy. The present study shed new light on an active and dynamic process in hydrochory and found that the buoyancy of diaspores may be controlled by changes in their spatial and temporal SG.     

DIASPORE SIZE,SHAPE, AND FALL BEHAVIOR IN WIND-DISPERSED PLANT SPECIES

Seeds and fruit of 38 anemochorous species were dropped in still air to simulate their descent under natural conditions. Fall rate and lateral distance were recorded as indices of wind-borne dispersal capability. Differences in fall rates among plumed species were dependent on interspecific variation in diaspore weight and plume area, while fall rates of winged species were strongly differentiated by contrasting wing shapes. In Acer platanoides and Asclepias syriaca, representing wing and plume architectures, respectively, the range of diaspore weight was artificially extended by removing embryos or adding lead weights. In both of these species, rate of descent of altered diaspores was controlled by weight relative to wing or plume area. The wing morphology of A. platanoides showed lower fall rates than the plumed A. syriaca above 45 mg, while the plume morphology of A. syriaca achieved lower fall rates below this weight. Compared with wide variation in diaspore weight, members of the Compositae showed relatively low variation in plume loading (diaspore weight/plume area) and fall speed. These observations suggest functional and phyletic constraints on diaspore architecture. Such constraints may limit evolutionary change in diaspore size and performance.     

Studying the quantity component of seed dispersal effectiveness from exclosure treatments and camera trapping

The quantity component of effectiveness of seed dispersal by animals is determined by two events: fruit removal (intensity of the interaction) and animal visitation to the plant (frequency of interactions). Considering dispersal of Prosopis flexuosa seeds as case study, this work aimed at investigating the strengths and weaknesses of the two methods for assessing the quantity component of seed dispersal effectiveness: exclosures and camera traps. Prosopis fruits were offered for 48 hr. Exclosure treatments were performed using two types of wire‐screen cages, allowing access to ants (“closed exclosure”) and to small mammals up to 100 g (“open to small mammals”), and a treatment without exclosure (“open to all removers”). The camera trapping experiment was carried out using vertically oriented cameras placed at approximately 1.80 m height and focused on the fruits. The cameras were set in “motion detect mode,” taking series of three consecutive photographs. The exclosures largely allowed estimation of fruit removal by size‐based groups of animals, but did not provide information on species identity. In contrast, camera traps were able to identify all visitors to species level and could not only determine the number of visits by each species but also the proportion of visits, which resulted in removal of fruits. Camera trapping allowed discriminating among small mammals playing different roles, without underestimating fruit removal by scatter‐hoarding species. The quality of estimation of the quantity component of seed dispersal is remarkably better when the camera trapping method is applied. Additional information obtained, such as activity patterns of visitors, can contribute to a better understanding of the seed dispersal process.     

Seed dispersal by neotropical waterfowl depends on bird species and seasonality

1. Waterbird‐mediated endozoochory is an essential mechanism for the dispersal of sessile organisms in freshwater ecosystems. However, in the neotropics there are no previous studies of how different waterbird species vary in the dispersal functions they perform, and how seasonality influences endozoochory. In this study, we identified plant diaspores dispersed in faeces of five South American waterfowl (Brazilian teal Amazonetta brasiliensis, yellow‐billed teal Anas flavirostris, ringed teal Callonetta leucophrys, coscoroba swan Coscoroba coscoroba, and white‐faced whistling‐duck Dendrocygna viduata).
2. We collected 165 faecal samples from five wetlands in southern Brazil surrounded by pasture and rice fields, then separated and measured intact seeds and other diaspores. Using generalised linear models, we tested how diaspore abundance and taxonomic richness differed among bird species and between cold (April–September) and warm (October–March) periods. We also analysed bird‐specific and seasonal variations in diaspore composition through principal coordinates analysis and permutational multivariate analysis of variance. We used indicator species analysis to determine which diaspore species discriminated between bird species and seasons. Finally, we measured diaspore length in order to analyse differences among waterfowl species in the size of diaspores dispersed.
3. We found 2,066 intact diaspores from 40 different plant taxa, including seeds of 37 angiosperms and diaspores of Lycophyta (Isoetes cf. maxima), Pteridophyta (Azolla filiculoides), and Charophyceae. There was at least one diaspore in 65% of all faecal samples. Diaspores of native amphibious and emergent plants were dominant. We found 1,835 diaspores (from 33 taxa) in the cold period but only 231 (23 taxa) in the warm period. Seeds of the grass Zizaniopsis bonariensis and of the sedge Rynchospora sp. were the most abundant taxa. A strong interaction between bird species and season was the most important predictor of variation in both taxonomic richness and abundance of diaspores. The taxonomic composition of diaspores differed among waterfowl species and season. Indicator species analysis identified 12 plant taxa associated with particular bird species and seasons. Coscoroba swan, the largest bodied species in our study dispersed a higher proportion (8.2%) of large (length >2 mm) seeds.
4. Despite considerable overlap, there are important differences in the plants dispersed by each species, and the smallest (ringed teal) and largest (coscoroba swan) birds are particularly different. All five waterfowl species are distributed over wide areas of South America and here we demonstrated that they are likely to be important plant vectors connecting wetland species at different geographical scales. Many of these plants have previously been assumed to lack mechanisms for long‐distance dispersal.

     

Picrorhiza tungnathii sp. nov. from western Himalaya,India

The new species Picrorhiza tungnathii Pusalkar is described and illustrated from the western Himalaya, India. It is distinguished from the allied P. kurrooa Royle ex Benth. by being 10–25 cm tall, having a moderately dense, (10–)15–25‐flowered spike, a zygomorphic, 2‐lipped, glandular‐ciliate corolla that is equaling or slightly exceeding the calyx and partly visible or sub‐exserted between the calyx lobes, a conspicuously long (longer than the corolla lobes), curved corolla tube (1/2–4/5 the length of the calyx), unequal corolla lobes that are ovate‐lanceolate to lanceolate, acute to sub‐acuminate and moderately ciliate, a mid‐lobe of the upper lip that is obliquely erect, galeate with retuse or emarginate apex, lateral corolla lobes that are slightly smaller than the mid‐lobe of the upper lip, a lower corolla lip that is slightly shorter than the lateral lobes, obliquely erect or spreading, didynamous, long‐exserted (2–3 times the corolla) stamens, pollen of the Paederota‐type and a style that is 2–3 times as long as the corolla.     

New mutualism for old: indirect disruption and direct facilitation of seed dispersal following Argentine ant invasion

The indirect effects of biological invasions on native communities are poorly understood. Disruption of native ant communities following invasion by the Argentine ant (Linepithema humile) is widely reported to lead indirectly to the near complete collapse of seed dispersal services. In coastal scrub in southeastern Australia, we examined seed dispersal and handling of two native and two invasive alien plant species at Argentine ant-invaded or -uninvaded sites. The Argentine ant virtually eliminates the native keystone disperser Rhytidoponera victoriae, but seed dispersal did not collapse following invasion. Indeed, Argentine ants directly accounted for 92% of all ant-seed interactions and sustained overall seed dispersal rates. Nevertheless, dispersal quantity and quality among seed species differed between Argentine ant-invaded and -uninvaded sites. Argentine ants removed significantly fewer native Acacia retinodes seeds, but significantly more small seeds of invasive Polygala myrtifolia than did native ants at uninvaded sites. They also handled significantly more large seeds of A. sophorae, but rarely moved them >5 cm, instead recruiting en masse, consuming elaiosomes piecemeal and burying seeds in situ. In contrast, Argentine ants transported and interred P. myrtifolia seeds in their shallow nests. Experiments with artificial diaspores that varied in diaspore and elaiosome masses, but kept seed morphology and elaiosome quality constant, showed that removal by L. humile depended on the interaction of seed size and percentage elaiosome reward. Small diaspores were frequently taken, independent of high or low elaiosome reward, but large artificial diaspores with high reward instead elicited mass recruitment by Argentine ants and were rarely moved. Thus, Argentine ants appear to favour some diaspore types and reject others based largely on diaspore size and percentage reward. Such variability in response indirectly reduces native seed dispersal and can directly facilitate the spread of an invasive alien shrub.     

Experimental studies of diaspore attachment to animal coats: predicting epizoochorous dispersal potential

The transport of diaspores on animal hairs depends on the ability of a diaspore to attach to the hair and to be retained in it over longer periods of time. Whereas several studies of diaspore retention on animal hairs have been conducted recently, the process of diaspore attachment to the hair has not yet been studied systematically. We describe a new method to quantify the attachment potential (AtP) of plant diaspores. Attachment potential was measured as the proportion of diaspores of a given species that attached to pieces of an animal coat in a standardised experiment. The experiment was conducted for 58 plant species (herbs and grasses) and three different coat types: sheep wool, cattle and roe deer hair. Attachment potentials differed widely between the three coat types, but also between plant species. We found diaspore surface structure (a quantitative measure of diaspore morphology) and diaspore exposition (describing the morphology of the infructescence) to be the most important plant traits regulating AtP. An influence of seed mass on attachment potential could not be detected. For sheep wool, a general linear model (with diaspore exposure as a factor and diaspore surface structure as covariate) explained 77% of the variation in AtPs. To validate this model, we predicted AtPs for 27 additional species and compared these to the measured Atps; the predicted and measured AtPscorrelated significantly with r _s = 0.68. A comparison of attachment and retention potentials to sheep wool for 127 randomly selected plant species showed that attachment and retention are only very weakly correlated, indicating that both processes act rather independently of each other. Since many diaspores seem to perform well in only one of these processes, attachment can be considered to be as equally as decisive as retention in terms of epizoochorous dispersal. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Geographic variation for elaiosome–seed size ratio and its allometric relationship in two closely related Corydalis species

Abstract

Background: Elaiosomes serve as a reward for seed-dispersing ants. The size of the elaiosome and the elaiosome–seed mass (ESM) ratio are expected to affect seed dispersal, whilst seed size affects the establishment of seedlings. Elaiosomes and seeds can undergo independent change, thus variation in these traits may arise through heterogeneous selection for seedling establishment and for dispersal. Only a few studies have examined intraspecific variation in these traits.

Aims: The aim of this study was to determine if the ratio of elaiosome–seed mass was different in two co-occurring congeneric plant species (Corydalis intermedia and C. solida). Under the hypothesis that the ESM ratio affected diaspore attractiveness to ants, the allometric relationship between elaiosome and seed mass was used to infer how selection by ants may shape the diaspore.

Methods: Seed and elaiosome mass were measured in fruits collected from central and marginal populations of the two plant species. The allometric relationship between seed and elaiosome mass was obtained using major axis regression. In situ cafeteria experiments estimated the removal rate of diaspores by ants.

Results: Intra- and interspecific variation in diaspore traits were found. The selfing C. intermedia produced heavier seeds and elaiosomes than the outcrossing C. solida. Ants removed more diaspores from C. intermedia where both species were present. A slope larger than one characterised the allometric relationship between elaiosome and seed mass in both species. This slope was twice as steep in the central populations of C. intermedia compared to marginal ones.

Conclusions: Results indicate that in C. intermedia elaiosome mass must increase more than proportionally with increasing seed mass for the diaspore to remain attractive to ants. The direction of interspecific differences suggests that a plant-mating system may affect selection for dispersal.