Costs and benefits of non‐random seed release for long‐distance dispersal in wind‐dispersed plant species

The dispersal ability of plants is a major factor driving ecological responses to global change. In wind‐dispersed plant species, non‐random seed release in relation to wind speeds has been identified as a major determinant of dispersal distances. However, little information is available about the costs and benefits of non‐random abscission and the consequences of timing for dispersal distances. We asked: 1) to what extent is non‐random abscission able to promote long‐distance dispersal and what is the effect of potentially increased pre‐dispersal risk costs? 2) Which meteorological factors and respective timescales are important for maximizing dispersal? These questions were addressed by combining a mechanistic modelling approach and field data collection for herbaceous wind‐dispersed species. Model optimization with a dynamic dispersal approach using measured hourly wind speed showed that plants can increase long‐distance dispersal by developing a hard wind speed threshold below which no seeds are released. At the same time, increased risk costs limit the possibilities for dispersal distance gain and reduce the optimum level of the wind speed threshold, in our case (under representative Dutch meteorological conditions) to a threshold of 5–6 m s^–1. The frequency and predictability (auto‐correlation in time) of pre‐dispersal seed‐loss had a major impact on optimal non‐random abscission functions and resulting dispersal distances. We observed a similar, but more gradual, bias towards higher wind speeds in six out of seven wind‐dispersed species under natural conditions. This confirmed that non‐random abscission exists in many species and that, under local Dutch meteorological conditions, abscission was biased towards winds exceeding 5–6 m s^–1. We conclude that timing of seed release can vastly enhance dispersal distances in wind‐dispersed species, but increased risk costs may greatly limit the benefits of selecting wind conditions for long‐distance dispersal, leading to moderate seed abscission thresholds, depending on local meteorological conditions and disturbances.     

Tracking wind‐dispersed seeds using 15N‐isotope enrichment

Seed dispersal influences a wide range of ecological processes. However, measuring dispersal patterns, particularly long‐distance dispersal, has been a difficult task. Marking bird‐dispersed seeds with stable ¹⁵N isotopes has been shown to be a user‐friendly method to trace seed dispersal. In this study, we determined whether ¹⁵N urea solution could be used to enrich seeds of two common wind‐dispersed plants, Eupatorium glaucescens (Asteraceae) and Sericocarpus tortifolius (Asteraceae). We further tested if the water type (distilled versus tap) in ¹⁵N urea solutions influences the level and variability of enrichment of plant seeds, and if increasing spraying frequency per se increases enrichment. Because droughts may lower seed set or kill plants, we wanted to investigate if the additional use of an externally applied anti‐transpirant affects the intake of externally applied ¹⁵N into seeds. The results demonstrate that ¹⁵N enrichment of seeds can facilitate dispersal experiments with wind‐dispersed plants. The use of distilled water in ¹⁵N urea solutions did not increase ¹⁵N enrichment compared to tap water. Further, enrichment was more efficient at lower spray frequencies. Both the use of tap water and low frequencies could lower time, effort and project costs. The results suggest that species can be protected from drought using an anti‐transpirant without decreasing the incorporation of ¹⁵N into seeds.     

食果动物传播种子的跟踪技术

研究食果动物传播种子的主要问题之一是难以跟踪种子命运和估计种子域。到目前为止,已有不少方法用于研究食果动物与种子扩散和种子命运的关系,如直接观察法、同位素标记法、金属标记法、磁铁标记法、荧光染料法、微粒体标记法、线标法和遗传技术等。近年来,一些研究将数字编号用于种子标记,并已成为发展的主流。本文综述了以往跟踪种子命运和估计种子域的一些重要方法,并讨论了它们各自的优缺点及其应用。     

Distribution of myrmecochorous species over the landscape and their potential long-distance dispersal by emus and kangaroos

Topographical heterogeneity can create a mosaic of substrate types leading to the formation of isolated plant populations. Seed dispersal then becomes crucial for the colonization of such suitable but remote substrate types. We surveyed the distribution of seven elaiosome-bearing species (myrmecochores) over 5 km² of natural heathland in southwestern Australia. Ants are the standard means of dispersal of these species, which provide limited dispersal (usually of a few metres). Six species were associated with particular substrate types (dune or swale) and all occurred as discrete populations, on average 270–500 m apart, with closest dune edges 280 m apart. We evaluated the possible roles of emus and kangaroos as alternative agents of long-distance seed dispersal between substrate types. Their droppings contained viable seeds of three of the target species, as well as other myrmecochores, and were evenly distributed over the substrate types. While migration of these plant species between preferred substrate types seems unlikely when considering only their standard dispersal agents (ants), it is highly likely in the presence of emus (in particular) and kangaroos that act as non-standard dispersers. This may have important consequences for plant species conservation by increasing habitat connectivity and favouring regional persistence.     

Interactions between Ants and Non‐myrmecochorous Fruits in Miconia (Melastomataceae) in a Neotropical Savanna

The aim of this study was to evaluate the role of ants as secondary seed dispersers of six primarily bird‐dispersed Miconia species in the cerrados of southeastern Brazil. Vertebrate exclosure and seed germination experiments were performed for M. albicans, M. alborufescens, M. corallina, M. ferruginata, M. ibaguensis, and M. irwinii. Excluding vertebrates did not significantly alter fruit removal rate for any of the Miconia species relative to open controls. Fruits on stalks and fallen fruits were removed and transported to nests mainly by species of Atta, Acromyrmex, and Ectatomma (dispersal distance ranging from 0.1 to 45.2 m), while Camponotus ants tended to be observed removing the fruit pulp (seed cleaning) where the fruits were found. Seed manipulation by Atta decreased germination of M. irwinii, but not M. ferruginata. Germination did not occur in intact fruits, and thus seed cleaning was an important service provided by the ants. Ant nest soils did not inhibit germination of any of the Miconia species, suggesting they are a good substrate for long‐lived Miconia seeds. We conclude that ant activity could have important effects on the fate of Miconia seeds adapted for bird dispersal.     

Secondary seed dispersal by ants in Neotropical cerrado savanna: species‐specific effects on seeds and seedlings of Siparuna guianensis (Siparunaceae)

1. Most woody plant species in tropical habitats are primarily vertebrate‐dispersed, but interactions between ants and fallen seeds and fruits are frequent. This study assesses the species‐specific services provided by ants to fallen arillate seeds of Siparuna guianensis, a primarily bird‐dispersed tree in cerrado savanna. The questions of which species interact with fallen seeds, their relative contribution (versus vertebrates) to seed removal, and the potential effects on seedling establishment are investigated. 2. Seeds are removed in similar quantities in caged and control treatments, suggesting that ants are the main dispersers on the ground. Five ant species attended seeds. Pheidole megacephala (≈0.4 cm) cooperatively transported seeds, whereas the smaller Pheidole sp. removed the seed aril on spot. Large (> 1.0 cm) Odontomachus chelifer, Pachycondyla striata, and Ectatomma edentatum individually carried seeds up to 4 m. Bits of aril are fed to larvae and intact seeds are discarded near the nest entrance. 3. Overall, greater numbers of seedlings were recorded near ant nests than in control plots without nests. This effect, however, was only detected near P. megacephala and P. striata nests, where soil penetrability was greater compared with controls. Soil nutrients did not differ between paired plots. 4. This study confirms the prevalence of ant–seed interactions in cerrado and shows that ant‐derived benefits are species‐specific. Ant services range from seed cleaning on the spot to seed displacement promoting non‐random spatial seedling recruitment. Although seed dispersal distances by ants are likely to be shorter than those by birds, our study of S. guianensis shows that fine‐scale ant‐induced seed movements may ultimately enhance plant regeneration in cerrado.     

Interference competition among disperser ants affects their preference for seeds of an ant‐dispersed sedge Carex tristachya (Cyperaceae)

For animal‐dispersed plants, evolutionary direction of seed traits is largely determined by the trait preference of disperser animals. Thus, clarifying conditions determining the disperser's preferences is important for understanding the evolution of dispersal traits in animal‐dispersed plants. The intensity of the interference competition among dispersers may be a factor affecting the seed trait preference of disperser animals, because it often weakens the food preference of various animals. To test this possibility, we examined correlation between the intensity of interference competition among disperser ants and their trait preference for seeds of an ant‐dispersed sedge, Carex tristachya Thunb. (Cyperaceae). By a cafeteria experiment conducted in the field, we first confirmed the overall preference by disperser ants for the elaiosome, which is a seed appendage facilitating the dispersal by ants. Second, we detected the negative correlation between the preference for elaiosomes and the frequency of interference among ants at a depot. Third, we compared this trend between dominants and subordinates of ants and revealed that the negative correlation was seen only in dominant species. These results suggest that the intensity of interference competition and the variation in its effect on animal species at different social status play important roles for the evolution of seed traits via the modification of seed trait preference by disperser animals.     

Interactions between ants and seeds of two myrmecochorous plant species in recently burnt and long‐unburnt forest sites

Myrmecochory (seed dispersal by ants) is a common seed dispersal strategy of plants in fire‐prone sclerophyll vegetation of Australia, yet there is little understanding of how fire history may influence this seed dispersal mutualism. We investigated the initial fate of seeds of two myrmecochorous plant species, the small‐seeded Pultenaea daphnoides J.C. Wendl. and the large‐seeded Acacia pycnantha Benth., in replicated burnt (3.25 years since fire) and unburnt (53 years since fire) forest plots in the Mount Lofty Ranges, South Australia. Specifically we measured (i) seed removal rates; (ii) the frequency of three ant–seed interactions (seed removal, elaiosome robbery and seed ignoring); (iii) the relative contribution of different ant species to ant–seed interactions; and (iv) the abundance of common interacting ant species. Rates of seed removal from depots and the proportion of seeds removed were higher in recently burnt vegetation and the magnitude of these effects was greater for the smaller‐seeded P. daphnoides. The overall proportion of elaiosomes robbed was higher in unburnt vegetation; however, the decrease in elaiosome robbery in burnt vegetation was greater for P. daphnoides than for A. pycnantha. Ants ignored seeds more frequently in burnt vegetation and at similar rates for both seed species. In total, 20 ant species were observed interacting with seeds; however, three common ant species accounted for 66.3% of ant–seed interactions. Monomorium sydneyense almost exclusively robbed elaiosomes, Rhytidoponera metallica typically removed seeds and Anonychomyrma nr. nitidiceps showed a mix of the three behaviours towards seeds. Differences in the proportions of seeds removed, elaiosomes robbed and seeds ignored appeared to be largely driven by an increase in abundance of A. nr. nitidiceps and a decrease in abundance of M. sydneyense in burnt vegetation. Understanding how these fire‐driven changes in the initial fate of myrmecochorous seeds affect plant fitness requires further investigation.     

The role of Rhytidoponera metallica (Hymenoptera,Formicidae) in facilitating post‐fire seed germination of three ant‐dispersed legume species

The fire avoidance hypothesis proposes that a benefit of seed dispersal by ants (myrmecochory) is to protect seeds from being killed during fire and to facilitate post‐fire germination of seeds that require heat shock to break their physical dormancy. The aim of this study was to quantify the effect of fire and seed burial by a predominant seed‐dispersing ant, Rhytidoponera metallica (subfamily: Ectatomminae) on germination levels of three ant‐dispersed legume species (Pultenaea daphnoides, Acacia myrtifolia and Acacia pycnantha). Experimental burial of seeds within aluminium cans at a site prior to being burnt and at an adjacent unburnt site showed that fire increased germination levels, particularly for seeds buried at 1‐ and 2‐cm deep and that overall, germination levels differed among the three plant species. To quantify seed burial depths and post‐fire germination levels facilitated by R. metallica ants, seeds were fed to colonies prior to fire at the burnt and unburnt sites. Of the seeds buried within nests that were recovered, between 45% and 75% occurred within the upper 6 cm of the soil profile, although unexpectedly, greater percentages of seeds were recovered from the upper 0–2 cm of nests in the unburnt site compared with nests in the burnt site. Germination levels of buried seeds associated with R. metallica nests ranged from 21.2% to 29.5% in the burnt site compared with 3.1–14.8% in the unburnt site. While increased seed germination levels were associated with R. metallica nests following fire, most seeds were buried at depths below those where optimal temperatures for breaking seed dormancy occurred during the fire. We suggest that R. metallica ants may provide fire avoidance benefits to myrmecochorous seeds by burying them at a range of depths within a potential germination zone defined by intra‐ and inter‐fire variation in levels of soil heating.     

Improving measurements of the falling trajectory and terminal velocity of wind‐dispersed seeds

Seed dispersal by wind is one of the most important dispersal mechanisms in plants. The key seed trait affecting seed dispersal by wind is the effective terminal velocity (hereafter “terminal velocity”, V _t ), the maximum falling speed of a seed in still air. Accurate estimates of V _t are crucial for predicting intra‐ and interspecific variation in seed dispersal ability. However, existing methods produce biased estimates of V _t for slow‐ or fast‐falling seeds, fragile seeds, and seeds with complex falling trajectories. We present a new video‐based method that estimates the falling trajectory and V _t of wind‐dispersed seeds. The design involves a mirror that enables a camera to simultaneously record a falling seed from two perspectives. Automated image analysis then determines three‐dimensional seed trajectories at high temporal resolution. To these trajectories, we fit a physical model of free fall with air resistance to estimate V _t . We validated this method by comparing the estimated V _t of spheres of different diameters and materials to theoretical expectations and by comparing the estimated V _t of seeds to measurements in a vertical wind tunnel. V _t estimates closely match theoretical expectations for spheres and vertical wind tunnel measurements for seeds. However, our V _t estimates for fast‐falling seeds are markedly higher than those in an existing trait database. This discrepancy seems to arise because previous estimates inadequately accounted for seed acceleration. The presented method yields accurate, efficient, and affordable estimates of the three‐dimensional falling trajectory and terminal velocity for a wide range of seed types. The method should thus advance the understanding and prediction of wind‐driven seed dispersal.     

Implications of nonrandom seed abscission and global stilling for migration of wind‐dispersed plant species

Migration of plant populations is a potential survival response to climate change that depends critically on seed dispersal. Biological and physical factors determine dispersal and migration of wind‐dispersed species. Recent field and wind tunnel studies demonstrate biological adaptations that bias seed release toward conditions of higher wind velocity, promoting longer dispersal distances and faster migration. However, another suite of international studies also recently highlighted a global decrease in near‐surface wind speeds, or ‘global stilling’. This study assessed the implications of both factors on potential plant population migration rates, using a mechanistic modeling framework. Nonrandom abscission was investigated using models of three seed release mechanisms: (i) a simple drag model; (ii) a seed deflection model; and (iii) a ‘wear and tear’ model. The models generated a single functional relationship between the frequency of seed release and statistics of the near‐surface wind environment, independent of the abscission mechanism. An Inertial‐Particle, Coupled Eulerian‐Lagrangian Closure model (IP‐CELC) was used to investigate abscission effects on seed dispersal kernels and plant population migration rates under contemporary and potential future wind conditions (based on reported global stilling trends). The results confirm that nonrandom seed abscission increased dispersal distances, particularly for light seeds. The increases were mitigated by two physical feedbacks: (i) although nonrandom abscission increased the initial acceleration of seeds from rest, the sensitivity of the seed dispersal to this initial condition declined as the wind speed increased; and (ii) while nonrandom abscission increased the mean dispersal length, it reduced the kurtosis of seasonal dispersal kernels, and thus the chance of long‐distance dispersal. Wind stilling greatly reduced the modeled migration rates under biased seed release conditions. Thus, species that require high wind velocities for seed abscission could experience threshold‐like reductions in dispersal and migration potential if near‐surface wind speeds continue to decline.     

Unexpected side effects in biocrust after treating non‐native plants using carbon addition

Carbon addition has been proposed as an alternative to herbicide and manual removal methods to treat non‐native plants and reduce non‐target effects of treatments (e.g. impacts on native plants; surface disturbance). On Mojave Desert pavement and biocrust substrates after experimental soil disturbance and carbon addition (1,263 g C/m² as sucrose), we observed declines in lichens and moss cover in sucrose‐treated plots. To further explore this unforeseen potential side effect of using carbon addition as a non‐native plant treatment, we conducted biocrust surveys 5 and 7 years after treatments, sampled surface soils to observe if treatments additionally affected soil filamentous cyanobacteria, and conducted laboratory trials testing the effects of different levels of sucrose on cyanobacteria and desert mosses. Sucrose addition to biocrust plots reduced lichen and moss cover by 33–78% and species richness by 40–80%. Sucrose reduced biocrust cover in biocrust plots to levels similarly detected in pavement plots (<1%). While cyanobacteria in the field did not appear to be affected by sucrose, laboratory tests showed negative effects of sucrose on both cyanobacteria and mosses. Cyanobacteria declined by 41% 1 month after exposure to 5.4 g C/m² equivalent solutions. We detected injury to photosynthesis in mosses after 96 hour exposure to 79–316 g C/m² equivalent solutions. Caution is warranted when using carbon addition, at least in the form and concentration of sucrose, as a treatment for reducing non‐native plants on sites where conserving biocrust is a goal.     

Habitat protection,cattle grazing and density‐dependent reproduction in a desert tree

Anthropogenic activities usually trigger changes in the population density of plants. Thus, land management practices can influence density‐dependent demographic parameters and species interactions. We investigated plant‐pollinator interactions and reproduction in Prosopis flexuosa, the largest tree species in the Central Monte desert of Argentina, an important economic and cultural resource for humans and a functionally prominent species. We hypothesized that reproductive output of P. flexuosa would be limited at low densities, and that exclusion of catle grazing would enhance population density and consequently interaction frequency with pollinators and reproductive success. The study was conducted in and around Ñacuñán Biosphere Reserve (Mendoza, Argentina), where cattle grazing has been excluded for over 35 years. Working in five pairs of protected and cattle grazed 1‐ha plots, we recorded density of adult trees, pollinator visitation frequency to inflorescences and seeds per inflorescence in focal trees. Adult tree density was higher in protected plots than in cattle grazed plots. Density of reproductive trees was positively correlated with seed production, suggesting positive density dependence for reproduction (Allee effect). Pollinator visitation to inflorescences and seed production was higher in protected plots compared with plots under cattle grazing. Suppression of anthropogenic degradation has resulted in higher adult tree density in protected plots, indirectly higher pollinator visitation to inflorescences and higher reproductive success of trees. Increased frequency of plant‐pollinator interactions and tree reproduction suggest success of management practices aimed at protecting P. flexuosa woodlands.     

Reduced germination success of temperate grassland seeds sown in dung: consequences for post‐dispersal seed fate

• Endozoochory is one of the main drivers shaping temperate grassland communities by maintaining plant populations of its constituents and enabling plants to colonize new habitats. Successful endozoochorous dispersal implies that seeds not only get consumed and survive the digestive tract but are also able to develop into viable seedlings in a dung environment.
• We experimentally assessed the germination probability and timing of 15 annual and perennial temperate European grassland species in cattle and horse dung and in different climatic conditions (greenhouse and outdoor conditions).
• Interspecific variation in germinability and germination timing are found, while life strategy had only an effect on germination timing. We found adverse effects of both cattle and horse dung on the germination characteristics of all tested grassland species, but the effects of cattle dung were more pronounced. In comparison with the control treatment, fewer seeds emerged in dung and more time was needed to germinate. Also, germination metrics clearly differed between the artificial greenhouse and outdoor conditions, with generally a lower germinability in outdoor conditions.
• According to our results, a large cost seems to be associated with endozoochorous dispersal in this stage of the life cycle, as seed dispersal effectiveness strongly depends on the quality of the deposition site with a lowered survival and germination probability when seeds are deposited in dung.

     

Biospeckle activity in coffee seeds is associated non‐destructively with seedling quality

Seeds age during storage, resulting in a decline in germination and seedling quality. Seed quality tests are important to monitor this decline. However, such tests are usually destructive and require large seed numbers and long time. For coffee seeds the standard germination test and assessment of seedling quality takes 30 days. Biospeckle has been used previously as a non‐destructive optical tool to monitor biological activity in a range of tissues. Biospeckle was applied 3–6 days after imbibition (DAI) to investigate an association with coffee seedling quality after 30 days. Two distinct areas of biospeckle activity were demonstrated, concurring with the locations of the embryonic axis and the cotyledons in the apical and central seed parts, respectively. Moisture content analysis revealed that embryos of imbibed seeds contained more water than endosperm. Different areas within the endosperm did not differ in moisture content, while the moisture content of the axis was higher than that of the cotyledons, and this did not change from 4 DAI. Therefore, it was concluded that high biospeckle activity was not the result of increased water content in any seed part, but more likely of growth and metabolism in the axis and cotyledons, which had been described previously. A threshold biospeckle ratio apical : central of 1.02 after 6 days distinguished between seeds that produced dead and viable seedlings after 30 days and provided similar results as a tetrazolium test, a widely acknowledged but destructive test for seed quality. Thus, biospeckle data provided a non‐destructive early parameter for seedling quality, based on embryo growth during germination.     

The potential of seed‐eating birds to spread viable seeds of weeds and other undesirable plants

The potential for seed‐eating birds to spread viable seeds was investigated using captive‐feeding trials to determine seed preference, passage time through the gut, and viability of passed seeds for bronzewing pigeons (Phaps chalcoptera), peaceful doves (Geopelia striata), crested pigeons (Ocyphaps lophotes), Senegal doves (Streptopelia senegalensis), zebra finches (Taeniopygia guttata), black ducks (Anas superciliosa) and wood ducks (Chenonetta jubata). Test seeds were bladder clover (Trifolium spumosum), crimson clover (Trifolium incarnatum), gorse (Ulex europaeus), canola (Brassica napus) and red panicum (Setaria italica). Their consumption was compared with that of commercial seed mixes. Although all test seeds were recognizable foods, their consumption usually decreased in the presence of other foods, except for canola, where consumption rates were maintained. Hard‐seeded bladder clover was the only species where viable seeds were passed by obligate seedeaters. In contrast, viable seeds of canola and gorse were passed by seed‐eating omnivorous/herbivorous ducks, although the germination of passed seeds (42%) was reduced significantly compared with that of untreated control seed (67%). Field validation with wild, urban bronzewings and Australian magpies (Gymnorhina tibicen) offered canola and commercial seed yielded similar outcomes, with a range of viable seeds recovered from magpie soft pellets. Mean seed passage time in captive birds ranged from 0.5 to 4.3 h for all test seeds and commercial seed mixes, suggesting that these bird species may potentially disperse seed over moderate distances. Despite the low probability of individual birds spreading viable seed, the high number of birds feeding in the wild suggests that the potential for granivorous and seed‐eating omnivorous birds to disperse viable seeds cannot be discounted, particularly if exozoochorous dispersal is also considered.     

Interaction between ants and seeds of a nonmyrmecochorous neotropical tree, Cabralea canjerana (Meliaceae), in the Atlantic forest of southeast Brazil

On the forest floor of two Atlantic forest sites in southeast Brazil, we recorded 26 ant species (12 genera) interacting with the seeds of Cabralea canjerana (Meliaceae), a typical ornithochorous tree whose seeds are covered by a lipid-rich aril. The ants treat the arillate seeds in three different ways: (1) the large ponerine ants Pachycondyla striata and Odontomachus chelifer individually remove the seeds to their nests, (2) many species (Pheidole spp.) recruit workers to remove the aril on the spot, or (3) Solenopsis spp. recruit nestmates and cover the seeds with soil before removing the aril on the spot. The ants remove the aril exceptionally rapidly, and removal greatly facilitates seed germination. Seed predation by insects below fruiting trees is severe, and field experiments using vertebrate exclosures showed that rodents also prey heavily upon seeds found near parent trees. Ponerine ants actively remove seeds from this predation-prone zone. By removing bird-manipulated and naturally fallen seeds, ants can play a key role in the fate of medium-sized seeds like those of C. canjerana.     

Species‐specific germination responses to fire‐associated heat of elephant‐dispersed seeds in Nimule National Park,South Sudan

Fire‐related heat and endozoochory by elephants have independently been found to be important for savanna plant seed germination, yet there is little information on how heat affects germination of elephant‐dispersed seeds. We measured the germination behavior (time to germination and proportion of seeds germinating) of 11 species of seeds extracted from African savanna elephant dung and subjected them to various intensities of heat as a proxy for fire exposure. The effects of heat were inconsistent and varied significantly by species, with some species having increased time to germination in response to heat and others having reduced time to germination. More studies are needed to expand the number of seed species examined and tease apart the interaction between elephant‐mediated endozoochory and fire.