A strong conditional mutualism limits and enhances seed dispersal and germination of a tropical palm

Seed predation and seed dispersal can have strong effects on early life history stages of plants. These processes have often been studied as individual effects, but the degree to which their relative importance co-varies with seed predator abundance and how this influences seed germination rates is poorly understood. Therefore, we used a combination of observations and field experiments to determine the degree to which germination rates of the palm Astrocaryum mexicanum varied with abundance of a small mammal seed predator/disperser, Heteromys desmarestianus, in a lowland tropical forest. Patterns of abundance of the two species were strongly related; density of H. desmarestianus was low in sites with low density of A. mexicanum and vice versa. Rates of predation and dispersal of A. mexicanum seeds depended on abundance of H. desmarestianus; sites with high densities of H. desmarestianus had the highest rates of seed predation and lowest rates of seed germination, but a greater total number of seeds were dispersed and there was greater density of seedlings, saplings, and adults of A. mexicanum in these sites. When abundance of H. desmarestianus was experimentally reduced, rates of seed predation decreased, but so did dispersal of A. mexicanum seeds. Critically, rates of germination of dispersed seeds were 5 times greater than undispersed seeds. The results suggest that the relationship between A. mexicanum and H. desmarestianus is a conditional mutualism that results in a strong local effect on the abundance of each species. However, the magnitude and direction of these effects are determined by the relative strength of opposing, but related, mechanisms. A. mexicanum nuts provide H. desmarestianus with a critical food resource, and while seed predation on A. mexicanum nuts by H. desmarestianus is very intense, A. mexicanum ultimately benefits because of the relatively high germination rates of its seeds that are dispersed by H. desmarestianus.     

Tracking Seed Fates of Tropical Tree Species: Evidence for Seed Caching in a Tropical Forest in North-East India

Rodents affect the post-dispersal fate of seeds by acting either as on-site seed predators or as secondary dispersers when they scatter-hoard seeds. The tropical forests of north-east India harbour a high diversity of little-studied terrestrial murid and hystricid rodents. We examined the role played by these rodents in determining the seed fates of tropical evergreen tree species in a forest site in north-east India. We selected ten tree species (3 mammal-dispersed and 7 bird-dispersed) that varied in seed size and followed the fates of 10,777 tagged seeds. We used camera traps to determine the identity of rodent visitors, visitation rates and their seed-handling behavior. Seeds of all tree species were handled by at least one rodent taxon. Overall rates of seed removal (44.5%) were much higher than direct on-site seed predation (9.9%), but seed-handling behavior differed between the terrestrial rodent groups: two species of murid rodents removed and cached seeds, and two species of porcupines were on-site seed predators. In addition, a true cricket, Brachytrupes sp., cached seeds of three species underground. We found 309 caches formed by the rodents and the cricket; most were single-seeded (79%) and seeds were moved up to 19 m. Over 40% of seeds were re-cached from primary cache locations, while about 12% germinated in the primary caches. Seed removal rates varied widely amongst tree species, from 3% in Beilschmiedia assamica to 97% in Actinodaphne obovata. Seed predation was observed in nine species. Chisocheton cumingianus (57%) and Prunus ceylanica (25%) had moderate levels of seed predation while the remaining species had less than 10% seed predation. We hypothesized that seed traits that provide information on resource quantity would influence rodent choice of a seed, while traits that determine resource accessibility would influence whether seeds are removed or eaten. Removal rates significantly decreased (p < 0.001) while predation rates increased (p = 0.06) with seed size. Removal rates were significantly lower for soft seeds (p = 0.002), whereas predation rates were significantly higher on soft seeds (p = 0.01). Our results show that murid rodents play a very important role in affecting the seed fates of tropical trees in the Eastern Himalayas. We also found that the different rodent groups differed in their seed handling behavior and responses to changes in seed characteristics.     

The effects of seed abundance on seed predation and dispersal by rodents in <Emphasis Type="Italic">Castanopsis fargesii</Emphasis> (Fagaceae)

Based on the animal dispersal hypothesis and the predator satiation hypothesis, we examined the effects of seed abundance at both population (i.e., mast seeding) and community levels on seed predation and dispersal of Castanopsis fargesii (Fagaceae), a rodent-dispersed mast species in Eastern Asia. In a subtropical evergreen broadleaved forest in the Dujiangyan region of Sichuan Province, China, individual seeds with coded tin tags were tracked in two contrasting stands (seed-poor and seed-rich) over two years (2000, a low-seed year; 2001, a high-seed year). Our results showed that: (1) small rodents did not harvest the tagged seeds of C. fargesii more rapid in the high-seed year than in the low-seed year in either stand. But, seed harvest was significantly faster in the seed-rich stand than in the seed-poor stand. (2) The removal proportion was significantly lower in the high-seed year than in the low-seed year for either stand, but the removal proportion was slightly higher in the seed-poor stand than in the seed-poor stand. This indicates that high seed abundance decreases seed removal (predator satiation hypothesis). (3) There were only small differences about seed caching, seed survival and seedling establishment of C. fargesii between years and stands. During the survey, no cached seeds survived to geminate in the spring for both stands and years. (4) Mean dispersal distances of the cached seeds are much shorter in the high-seed year (3.1 m) than in the low-seed year (8.1 m) in the seed-rich stand, though similar trend is not examined in the seed-poor stand. Our results indicate that seed predation and dispersal of C. fargesii are influenced by both mast seeding and community-level seed abundance, which is not completely consistent with either the animal dispersal hypothesis or the predator satiation hypothesis, but seems more related to the predator satiation hypothesis.     

Tree-to-tree variation in seed size and its consequences for seed dispersal versus predation by rodents

Individual variation in seed size and seed production is high in many plant species. How does this variation affect seed-dispersing animals and, in turn, the fitness of individual plants? In this study, we first surveyed intraspecific variation in seed mass and production in a population of a Chinese white pine, Pinus armandii. For 134 target trees investigated in 2012, there was very high variation in seed size, with mean seed mass varying among trees almost tenfold, from 0.038 to 0.361 g. Furthermore, 30 of the 134 trees produced seeds 2 years later, and for these individuals there was a correlation in seed mass of 0.59 between years, implying consistent differences among individuals. For a subset of 67 trees, we monitored the foraging preferences of scatter-hoarding rodents on a total of 15,301 seeds: 8380 were ignored, 3184 were eaten in situ, 2651 were eaten after being cached, and 395 were successfully dispersed (cached and left intact). At the scale of individual seeds, seed mass affected almost every decision that rodents made to eat, remove, and cache individual seeds. At the level of individual trees, larger seeds had increased probabilities of both predation and successful dispersal: the effects of mean seed size on costs (predation) and benefits (caching) balanced out. Thus, despite seed size affecting rodent decisions, variation among trees in dispersal success associated with mean seed size was small once seeds were harvested. This might explain, at least in part, the maintenance of high variation in mean seed mass among tree individuals.     

啮齿动物对不同林木种子的搬运和取食微生境选择机制

不同植物种子依靠不同的方式实现扩散,啮齿动物对林木种子搬运后在取食点微生境和贮藏方式的选择存在偏好,研究其贮藏行为与微生境的关系是探究幼苗建成的关键。在秦岭中段火地塘林区,采用标签标记法,以锐齿槲栎、华山松和油松种子为材料,探究了小型啮齿动物对松栎混交林建群种种子扩散过程的影响。结果表明:1)油松种子原地取食率显著高于锐齿槲栎和华山松种子,且啮齿动物更倾向于搬运后取食(60%)和埋藏(4.33%)华山松种子,搬运后取食距离也为华山松最大(2.49 m);锐齿槲栎小种子被搬运后埋藏的距离最大(4.92 m)。2)除华山松种子外,其他类型种子被搬运后单个取食的比例均在85%以上;油松种子不存在埋藏点,而其他类型种子90%以上均以单个形式被埋藏。3)大部分种子被啮齿动物搬运后选择在裸地丢弃;锐齿槲栎大种子(87.5%)、小种子(78.57%)和华山松种子(53.33%)较大比例被啮齿动物埋藏在灌丛下方,埋藏在裸地的种子较少。4)大部分种子在灌丛下方被取食,仅华山松种子被啮齿动物搬运到洞穴取食;除油松种子被大量原地取食外,其他类型种子被搬运到取食点的种子比例基本呈现由微生境植被复杂到简单(灌丛—草丛—灌丛边缘—裸地)而逐渐减小的趋势。种子的营养价值及取食和搬运过程中啮齿动物付出的成本是影响种子命运的关键性因子,且啮齿动物对种子埋藏和取食地点的微生境存在较明显的选择性。     

Seed Dispersal of a High Quality Fruit by Specialized Frugivores: High Quality Dispersal?1

Dispersal quality, as estimated by the cumulative effects of dispersal, germination, seed predation, and seedling survival, was examined for Beilschmiedia pendula (Lauraceae) in Monteverde, Costa Rica. I determined the pattern of dispersal by finding seeds deposited by birds, protected the seeds from seed predators with cages to assess germination and seedling survival, and examined seed predation rates with marked seeds. Seed predation, germination, and seedling survival were compared between seeds naturally dispersed by birds and seeds placed at randomly located sites. Approximately 70 percent of seeds dispersed by birds (N= 244) were deposited <10 m from crown edges of fruiting B. pendula trees, although some seeds were dispersed at least 70 m away. Larger seeds were more likely to be dispersed under or close to the parent trees, and larger seeds produced larger seedlings. Seed size was not correlated directly with seedling survival, but larger seedlings at three months were most likely to survive one year. Seed predation by mammals and insects and seedling mortality due to fungal pathogens were concentrated beneath the crowns of parent trees. Seedlings and saplings were more abundant beneath fruiting B. pendula trees, but individuals farther away were taller on average. Thus, dispersal is beneficial for B. pendula, but such benefits appear most pronounced at a small spatial scale; seeds dispersed >30 m from the crown edges actually had a lower probability of survival than those dispersed 10–20 m. Only 10 percent of B. pendula. seeds received high‐quality dispersal in terms of landing in the zone with the highest per seed probability of seedling survival 10–20 m from parental crowns.     

Effects of mast seeding and rodent abundance on seed predation and dispersal of <Emphasis Type="Italic">Quercus aliena</Emphasis> (Fagaceae) in Qinling Mountains,Central China

Rodents act as seed predators and dispersers and play an important role in the regeneration of plants. Seed production and rodent abundance may influence caching rodents’ decision to consume or cache seeds. We studied how did seed production and rodent abundance co-influence seed predation and dispersal by rodents in the mast seed years (2011 and 2013) and non-mast seed years (2012 and 2014) in the Qinling Mountains of Shaanxi Province, Central China. We found that: (1) The seed removal rates were much faster in the non-mast seed years than in the mast seed years. (2) Although the total number of seeds consumed (including eaten in situ and after removal) was higher in the non-mast seed years than in the mast seed years, no significant differences were found in the seeds that were eaten in situ and after removal among the 4 years. (3) Significant differences were observed in seeds that were cached among the 4 years, and more seeds were cached in the non-mast seed years than in the mast seed years. (4) The primary and secondary seed dispersal distances (including cached and eaten) were all longer in the non-mast seed years than in the mast seed years. Overall, these results indicate that non-mast seeding with low per capita seed availability could increase both seeds consumption and caching by rodents. Our results are partially supporting the predator satiation hypothesis.     

The intermediate dispersal hypothesis: seed dispersal is maximized in areas with intermediate usage by hoarders

Seed dispersal and predation are paramount for tropical plant diversity. When encountered by scatter-hoarding frugivores, seeds can be either eaten, dispersed or ignored. But even after dispersal, seed caches are still subjected to predation. Many factors are known to influence these dynamics; however, how frequently hoarders use certain patches has seldom been related to cache predation rates. We used the interaction between agoutis (Dasyprocta leporina), a scatter-hoarding rodent, and Joannesia princeps, a tropical tree, as a model to investigate how the number of visits by hoarders in certain areas influences cache predation and seed fate. Camera-traps were used for 30 days in twenty different locations in Tijuca National Park to assess number of visits by agoutis. Thereafter, we placed seed piles on the same areas and determined their fate using the spool-and-line method to track seeds for over one hundred days. We found a non-linear relationship between how often an area is used by hoarders and the final proportion of dispersed seeds. At areas with a low number of visits, proportion of dispersed seeds was low due to low removal. As frequency of visits by hoarders increased, seed removal and the number of dispersal events increased but so did cache predation. Thus, in areas intensively used by hoarders, high cache predation resulted in a low number of dispersed seeds that remained alive in caches. As a result, dispersal was maximized in areas with intermediate use by scatter-hoarders, where there was a balance between primary seed dispersal and cache predation.

     

Seed dispersal of three sympatric oak species by forest rodents in the Qinling Mountains, Central China

Forest rodents play an essential role as seed dispersal vectors through their caching behaviors. Using seeds of Quercus aliena, Q. glandulifera, and Cyclobalanopsis engleriana (Fagaceae), which are dominant, but poorly studied species, in the Qinling Mountains, Central China, we investigated seed predation and dispersal by forest rodents in 2010 and 2011. There were significant differences in rodent seed-eating and caching strategies among the three tree species. Seeds of Q. aliena and C. engleriana had hard coats, high nutrition contents (e.g., protein, fat, and starch), and long germination schedules (C. engleriana only). They were less frequently eaten in situ, but more likely to be eaten after removal or cached. Seeds of Q. glandulifera had soft coats and low nutrition contents and were more often eaten in situ and less likely to be eaten after removal or cached. Our findings indicated that forest rodents were primarily responsible for seed predation and dispersal of these three tree species in the Qinling Mountains, and seed traits, especially coat hardness, nutrition content, and germination schedule, were important factors influencing rodent eating and caching behaviors. In addition, seed dispersal process of each tree species differed significantly between the 2 years, reflecting the effect of mast seeding on the eating and caching strategies of forest rodents.     

Small rodents as significant dispersers of tree seeds in a Neotropical forest

Abstract. Through seed dispersal and predation, terrestrial mammals should be an important component of the mechanisms that determine patterns of tree recruitment in tropical forests. Despite their great abundance and ubiquity in Neotropical forests, small rodents as seed predators and dispersers remain largely forgotten. To investigate the fates of seeds in a hunted primary forest in Belize, we tagged seeds of Astrocaryum mexicanum (Palmae), Ampelocera hottlei (Ulmaceae), and Pouteria sapota (Sapotaceae) and placed them into open plots, exclosures accessible only to small mammals, and exclosures accessible to medium-sized and small mammals. The exclosure experiments and fates of the seeds show that the spiny pocket mouse, Heteromys desmarestianus (Heteromyidae), was the dominant handler of seeds of the first two species and also removed a significant proportion of the very large-seeded Pouteria. Most of the seeds were killed immediately upon removal, but many of the seeds (3–18 %) of the first two species were scatterhoarded (dispersed and buried in the soil) by Heteromys. Some of the scatterhoarded seeds (29%) remain buried and therefore protected from predation by other animals. Agoutis (Dasyprocta punctata), a caviomorph rodent, buried 13 % of the seeds of Pouteria, and Heteromys consumed and dispersed but did not bury Pouteria seeds. Results of this study support predictions by some researchers that small rodents are dominant terrestrial granivores in Neotropical forests. The role of small rodents as seed dispersers, however, has never been fully appreciated.     

Introduction of mammalian seed predators and the loss of an endemic flightless bird impair seed dispersal of the New Zealand tree Elaeocarpus dentatus

Understanding the mutualistic services provided by species is critical when considering both the consequences of their loss or the benefits of their reintroduction. Like many other Pacific islands, New Zealand seed dispersal networks have been changed by both significant losses of large frugivorous birds and the introduction of invasive mammals. These changes are particularly concerning when important dispersers remain unidentified. We tested the impact of frugivore declines and invasive seed predators on seed dispersal for an endemic tree, hinau Elaeocarpus dentatus, by comparing seed dispersal and predation rates on the mainland of New Zealand with offshore sanctuary islands with higher bird and lower mammal numbers. We used cameras and seed traps to measure predation and dispersal from the ground and canopy, respectively. We found that canopy fruit handling rates (an index of dispersal quantity) were poor even on island sanctuaries (only 14% of seeds captured below parent trees on islands had passed through a bird), which suggests that hinau may be adapted for ground‐based dispersal by flightless birds. Ground‐based dispersal of hinau was low on the New Zealand mainland compared to sanctuary islands (4% of seeds dispersed on the mainland vs. 76% dispersed on islands), due to low frugivore numbers. A flightless endemic rail (Gallirallus australis) conducted the majority of ground‐based fruit removal on islands. Despite being threatened, this rail is controversial in restoration projects because of its predatory impacts on native fauna. Our study demonstrates the importance of testing which species perform important mutualistic services, rather than simply relying on logical assumptions.     

Scatter-hoarding rodents use different foraging strategies for seeds from different plant species

Seed predation and dispersal by scatter-hoarding rodents are key processes that determine seed survival, and thus, plant regeneration within forests. For decades, there has been much debate on the important effects of seed size (one of the most important seed traits) on rodent foraging preference. Furthermore, the possible selective forces in the evolution of seed size may be influenced by primary selectivity and how rodents treat seeds after harvesting. In this study, different-sized seeds from four species (Pinus armandii, Pinus densata, Abies sp., and Viburnum sp.) harvested by scatter-hoarding rodents were studied in an alpine forest in Southwestern China for two consecutive years. Our results showed that seed size influenced rodent foraging preferences, with bigger seeds being preferred over smaller seeds, within and across species. Rodents only removed and cached the larger seeds of P. armandii, and ate the seeds of the other three species in situ. Rodents are purely seed predators for these three species. For the cached seeds of P. armandii, significantly positive correlations were observed between seed size and dispersal distance among both primary and secondary cached seeds in 2006, but not in 2005. Our results indicate that among many coexisting species with widely different-sized seeds, scatter-hoarding rodents played important roles in the seed dispersal of the big-seeded species alone. This caching behavior could offset the limited seed dispersal of large-seeded and wingless species (P. armandii), in comparison with that of small winged seed species (P. densata and Abies sp.) and frugivore-dispersed species (Viburnum sp.).     

Adaptive advantages of myrmecochory: the predator-avoidance hypothesis tested over a wide geographic range

The predator‐avoidance hypothesis states that once released from the parent plant, myrmecochorous seeds are rapidly taken by ants to their nests, where they are protected from predators. Previous studies conducted to test this hypothesis have frequently neglected two major aspects necessary for its verification: 1) the influence of processes acting after the seed release and 2) the spatial evenness of such processes. Thus, large‐scale variations in the mechanisms acting beyond seed release, and possibly influencing seed escape from predators, remain poorly documented. Here, we present the results of a post‐dispersal seed‐removal experiment on the myrmecochorous herb Helleborus foetidus, aimed at verifing the predator‐avoidance hypothesis by considering two key post‐release aspects of seed fate: seed destination (dispersed or nondispersed) and seed burial (buried or not buried). Experiments were performed in four different regions in the Iberian Peninsula. After three days of exposure of seeds to the main predator (fieldmice Apodemus sylvaticus), ca 30% of the seeds were removed. Seed destination affected the proportion of seeds escaping predation, but the sign, magnitude and statistical significance of the effect varied among the geographical regions. In the southern region (Cazorla), seeds dispersed in ant nests or intermediate destinations suffered scarcely any predation, but seeds under reproductive‐age plants experienced losses ca 50%. Conversely, in the northern region (Caurel), seeds in nests suffered significantly greater losses than seeds under plants or intermediate destinations, suggesting that nests were especially unsafe destinations. Seed burial had a strong impact on seed escape from predators, and its effect was highly consistent among geographical regions. In view of the consistency of its effect at different spatial scales, seed burial was a more general mechanism for predation avoidance than seed relocation to ant nests, which was habitat‐ and/or ant‐species‐dependent. Our results thus only partially support the predator‐avoidance hypothesis for the evolution of myrmecochory.     

A new hypothesis for the importance of seed dispersal in time

Most studies on seed dispersal in time have focused on seed dormancy and the physiological triggers for germination. However, seed dispersed by animals with low metabolic and moving rates, and long gut-passage times such as terrestrial turtles, could be considered another type of dispersal in time. This study tests the hypothesis that seeds dispersed in time may lower predation rates. We predicted that seeds deposited below parent trees after fruiting fall has finished is advantageous to minimize seed predators and should show higher survival rates. Four Amazonian plant species, Dicranostyles ampla, Oenocarpus bataua, Guatteria atabapensis and Ocotea floribunda, were tested for seed survival probabilities in two periods: during fruiting and 10-21 days after fruiting. Experiments were carried out in two biological stations located in the Colombian Amazon (Caparú and Zafire Biological Stations). Seed predation was high and mainly caused by non-vertebrates. Out of the four plant species tested, only Guatteria atabapensis supported the time escape hypothesis. For this species, seed predation by vertebrates after the fruiting period increased (from 4.1% to 9.2%) while seed predation by non-vertebrates decreased (from 54.0% to 40.2%). In contrast, seed predation by vertebrates and by non-vertebrates after the fruiting period in D. ampla increased (from 7.9% to 22.8% and from 40.4% to 50.6%, respectively), suggesting predator satiation. Results suggest that for some species dispersal in time could be advantageous to avoid some type of seed predators. Escape in time could be an additional dimension in which seeds may reach adequate sites for recruitment. Thus, future studies should be address to better understand the survival advantages given by an endozoochory time-dispersal process.     

Seed dispersal, plant recruitment and spatial distribution of Bactris acanthocarpa Martius (Arecaceae) in a remnant of Atlantic forest in northeast Brazil

Seed dispersal ecology of Bactris acanthocarpa Mart. (Arecaceae), an Atlantic forest understory palm, was investigated during two years as an attempt to test the following predictions: (i) seeds of Bactris are dispersed by mammals and large-gaped birds; (ii) Bactris benefits from seed dispersal in terms of seed predation avoidance, improvement of seed germination and seedling survival; and (iii) spatial distribution of adults is related to patterns of seed dispersal. The study was conducted at Dois Irmãos Reserve, a 387.4-ha reserve of Atlantic forest in northeastern Brazil (8º S–35º W). Black–rumped agoutis (Dasyprocta prymnolopha) and Guianan squirrels (Sciurus aestuans) were identified as the seed dispersers/predators, moving seeds short distances (< 4 m from parents) and at low rates (0.04-0.05 diaspore/palm/day). Pyrene burial prevented seed predation by vertebrates and reduced by half seed infestation by Scolytidae beetles. Only buried pyrenes germinated. Pyrene predation was not correlated with distance from conspecific adults. In contrast, early seedling mortality was higher near conspecific adults. Most adults (64%) had their nearest conspecific adult neighbour > 4 m away in contrast to 96% of seedlings that occurred concentrated within 4 m from adults (77% under the palm crowns). Here, we present evidence that spatial distribution of B. acanthocarpa is partly due to low rates of seed removal, short-distance seed dispersal by agoutis and squirrels, and early seedling mortality associated with presence of seedlings under palm crowns.     

Early fate of Myristica hypargyraea seeds dispersed by Ducula pacifica in Tonga,Western Polynesia

Abstract Although pigeons from the genus Ducula are considered among the best avian dispersers of large seeds in Asia and the Pacific, little has been documented on their role. The early fate of dispersed and undispersed seeds of the large‐seeded tree Myristica hypargyraea A. Gray was studied in order to understand the advantage of seed dispersal by the Pacific Pigeon, Ducula pacifica Gmelin in Tonga. Frequency of visits by frugivores to fruiting trees and dispersal distance of seeds were measured. Pre‐dispersal vertebrate seed predation was assessed, then post‐dispersal predation was measured over 160 days. Overall, pre‐dispersal seed predation by parrots was low but variable among trees sampled. Most seeds (54.7%) in the study area were estimated to be dispersed by D. pacifica; 79.7% of those ingested were expelled directly beneath conspecific fruiting crowns, 20% were dispersed locally and < 0.3% were dispersed more than 300 m into a different forest type. Flying foxes (Pteropus tonganus Quoy and Gaimard) dispersed very few seeds (0.7%) and all were dropped below fruiting crowns. Between 4% and 39% of dispersed and undispersed seeds were still viable, or had established seedlings after 160 days. Most seeds had been removed or killed by rats, and seed survival was highest for locally dispersed seeds (approx. 20 m from source trees and within the M. hypargyraea forest). Although D. pacifica was the only frugivore observed to disperse seeds into this higher zone of survival, overall they did not confer a great advantage to seed survival since significant numbers of seeds/seedlings also persisted under fruiting crowns (27% under crowns compared with 39% locally dispersed). Nevertheless, D. pacifica was the only vector by which seeds were regularly moved within the M. hypargyraea forest and over longer distances, and hence, D. pacifica still plays a significant role in the regeneration of M. hypargyraea.     

Toucans (Ramphastos ambiguus) facilitate resilience against seed dispersal limitation to a large‐seeded tree (Virola surinamensis) in a human‐modified landscape

Large‐seeded plants may suffer seed dispersal limitation in human‐modified landscapes if seed dispersers are absent or unable to disperse their seeds. We investigated dispersal limitation for the large‐seeded tree Virola surinamensis in a human‐modified landscape in southern Costa Rica. During two fruiting seasons, we monitored crop size, seed removal rates, the number of fruiting conspecifics within 100 m, and feeding visitation rates by frugivores at trees located in high and low forest disturbance conditions. Seed removal rates and the total number of seeds removed were high regardless of the disturbance level, but these parameters increased with tree crop size and decreased with the number of fruiting V. surinamensis trees within a 100 m radius. Trees at low disturbance levels were more likely to be visited by seed dispersers. Black mandibled toucans (Ramphastos ambiguus) and spider monkeys (Ateles geoffroyi) were the most important seed dispersers, based on visitation patterns and seed removal rates. Spider monkey feeding visits were more frequent at high disturbance levels, but the monkeys preferentially visited isolated trees with large yields and surrounded by a low number of fruiting Virola trees within 100 m. Toucan visitation patterns were not constrained by any of the predictors and they visited trees equally across the landscape. We suggest that isolated and highly fecund Virola trees are an important food resource for spider monkeys in human‐modified landscapes and that toucans can provide resilience against seed dispersal limitations for large‐seeded plants in human‐modified landscapes in the absence of hunting.     

A telemetric thread tag for tracking seed dispersal by scatter-hoarding rodents

The seeds of many tree species are dispersed more than once, and this secondary seed dispersal is believed to enhance seedling recruitment. However, the effectiveness of secondary seed dispersal has rarely been assessed because it is difficult to track seeds until they die or germinate. We describe a new technique that uses thread tags attached to radio transmitters (telemetric thread tags) to track long-distance multistep seed dispersal by scatter-hoarding rodents. These telemetric thread tags can be turned off with a magnet and are reactivated when the seed moves. This method allows for seed tracking with minimal cache disturbance or distance bias, over long time spans, multiple seed movements, and with few effects on animal behavior. We used telemetric thread tags to track seed dispersal of the palm tree Astrocaryum standleyanum in a Neotropical forest, and achieved near-complete recovery of dispersed seeds tracked over distances as far as 241?m. We were also able to record the recovery time and fate of cached seeds without disturbing caches. Neither the removal rate nor the dispersal distance differed between seeds with telemetric thread tags and thread-tagged seeds. We conclude that telemetric thread tags can be used to document secondary seed dispersal by scatter-hoarding animals with unprecedented efficacy and precision. Given the size of these tags relative to the size of seeds and their dispersers, this method is applicable to the majority of tree species that are secondarily dispersed by scatter-hoarding mammals.     

Constraints on treeline advance in a warming climate: a test of the reproduction limitation hypothesis

Aims Several mechanistic hypotheses have been developed to explain the existence of alpine treelines worldwide. The reproduction limitation hypothesis (RLH) postulates that reproductive processes such as seed production and dispersal are restricted in treeline environments, thereby limiting the establishment of new individuals in advance of extant treelines. Despite its popularity, no study has tested this hypothesis in a comprehensive fashion. In this experiment, we attempted to answer whether there are enough viable seeds being dispersed beyond treeline for sexually mediated treeline advance, and what the implications of climate change might be on these processes.Methods We established 30 plots across two aspects (north vs. south) and three elevational habitats (forest, treeline and tundra) in a white spruce (Picea glauca) boreal forest-alpine tundra ecotone in southwest Yukon, Canada. In each plot, tree characteristics, seed production and predispersal damage were measured. Additionally, eight dispersal trays were positioned in each plot to measure seed rain, and germination trials with and without predation exclosures were constructed in a subset of plots to quantify dispersal and germination success.Important findings Results were highly variable both temporally and spatially. In 2014, a mast year, 69% of adult trees produced cones compared to 0.4% in the following year. Higher density of trees in forest plots compared to treeline and tundra resulted in greater seed production at lower elevations. Across all plots, 88% of seeds were damaged before dispersal or were not viable. Treeline plots had significantly greater predispersal damage. Seed rain was greater in south-facing plots than north-facing plots. Less than 2% of seeds produced on the landscape were dispersed into Tundra plots, located 50 m above treeline. There was a net movement of seeds from the north-facing slope to the south at our study site, likely due to prevailing winds during the dispersal period. Germination counts were more than double on north-facing slopes and one-third higher inside exclosures. Cumulatively, the results provide some evidence for the RLH. Collectively, the high amount of predispersal damage and non-viable seeds, variability associated with dispersal and significant seed predation can functionally influence treeline dynamics. These findings suggest that global treeline distribution models, which rely largely on temperature, may not be entirely accurate for predicting treeline advance—at least at finer temporal scales. Many stochastic factors need to align temporally for successful advance, which is likely to result in a lag of many decades between the period of temperature amelioration and an increased number of trees beyond extant treelines.     

Pre‐dispersal seed predators and fungi differ in their effect on Luehea seemannii capsule development,seed germination,and dormancy across two Panamanian forests

Pre‐dispersal seed predation can greatly reduce crop size affecting recruitment success. In addition, non‐fatal damage by seed predators may allow infection by fungi responsible for post‐dispersal seed losses. The objectives of this study were (1) to quantify pre‐dispersal seed predation and fungal infection in a Neotropical tree species, Luehea seemannii, that produces dehiscent fruits and wind‐dispersed seeds, and (2) to link pre‐dispersal effects on seed quality to seed survival in the soil. To examine how seed predators and fungi influence seed losses, mesh exclosures, fungicide, and the combination of both treatments were applied to separate branches in the canopy of trees in Gamboa and Parque Natural Metropolitano (PNM), Panama. To determine if treatments affect seed viability and survival in the soil, half of the seeds collected from each treatment were buried for 4 weeks in forest soils and subsequently allowed to germinate before and after the breaking of dormancy. Overall, 24 percent of developing fruit were lost to insect attack. In contrast, fungi infected only 3 percent of seeds at the pre‐dispersal stage. For seeds germinated directly after collection, fungicide significantly increased germination in the wetter site (Gamboa) but decreased germination in the drier site (PNM). The pre‐dispersal insect exclosure treatment increased the fraction of seeds that remained dormant after burial in the soil. This result suggests that exposure to insect predators may cause physical damage to seeds that results in the loss of physical dormancy but does not necessarily increase the susceptibility of seeds to pathogen attack in the soil.