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Bird-mediated seed dispersal: Reduced digestive efficiency in active birds modulates the dispersal capacity of plant seeds
Abstract and Figures
Plant populations in fragmented ecosystems rely largely on internal dispersal by animals. To unravel the mechanisms underlying this mode of dispersal, an increasing number of experimental feeding studies is carried out. However, while physical activity is known to affect vertebrate digestive processes, almost all current knowledge on mechanisms of internal seed dispersal has been obtained from experiments with resting animals. We investigated how physical activity of the mallard (Anas platyrhynchos), probably the quantitatively most important biotic dispersal agent in aquatic habitats in the entire Northern Hemisphere, affects gut passage survival and retention time of ingested plant seeds. We fed seeds of nine common wetland plants to mallards trained to subsequently swim for 6 hours in a flume tank at different swimming speeds (activity levels). We compared gut passage survival and retention times of seeds against a control treatment with mallards resting in a conventional dry cage. Intact gut passage of seeds increased significantly with mallard activity (up to 80% in the fastest swimming treatment compared to the control), identifying reduced digestive efficiency due to increased metabolic rates as a mechanism enhancing the dispersal potential of ingested seeds. Gut passage speed was modestly accelerated (13% on average) by increased mallard activity, an effect partly obscured by the interaction between seed retention time and probability of digestion. Gut passage acceleration will be more pronounced in digestion-resilient seed species, thereby modulating their dispersal distances. Our findings imply that seed dispersal potential by mallards calculated from previous experiments with resting birds is highly underestimated, while dispersal distances may be overestimated for some plant species. Similar effects of physical activity on digestive efficiency of mammals suggests that endozoochorous dispersal of plant seeds by vertebrates is more effective and plays a quantitatively more important ecological role in both terrestrial and aquatic ecosystems than previously thought.
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... On the third chapter (under revision in Movement Ecology), I assessed the functional connectivity by means of molecular markers of four hygrophilous selected species: Oenanthe aquatica, Lycopus europaeus, Typha latifolia and Phragmites australis that differ in their dispersal modes and reproductive strategies. In Oenanthe and Lycopus, pollen transfer is mediated by insects and seed dispersal by water (occasionally endozochory by birds); while in Typha and Phragmites pollen and seeds are adapted to wind dispersal (occasionally exozochory by birds) (Hroudova et al. 1992;Kühn et al. 2004;Green et al. 2008;Kleyer et al. 2008;Brochet et al. 2009;Kleyheeg et al. 2015). All species can develop clonal rhizomes but is extremely rare in Oenanthe aquatica (Dickerman and Wetzel 1985;Kühn et al. 2004;Klimešová and Bello 2009;Packer et al. 2017 as well as habitat heterogeneity and patch size have a positive effect on bee diversity based on the assumption that different habitats provide a greater variety of nesting and food opportunities, while a negative effect of isolation degree was expected. ...
... In Oenanthe aquatica and Lycopus europaeus, pollen transfer is mediated by insects and seed dispersal by water, while in Typha latifolia and Phragmites australis pollen and seeds are adapted to wind dispersal (Kühn et al. 2004;Kleyer et al. 2008). Occasionally, seeds can be dispersed by animals, mainly water birds through exozoochory in Typha and Phragmites and endozoochory in Lycopus and Oenanthe (Hroudova et al. 1992;Green et al. 2008;Brochet et al. 2009;Kleyheeg et al. 2015). Lycopus europaeus develops clonal rhizomes and stem tubers ...
... This seems to support IBD for all species, albeit to varying degrees; with a smoother decrease in the outcrossing Oenanthe compared with the selfing/clonal species. This is supported by the significant genetic divergence in all species measured by F ST (Tables B3-B6) and an increase of global F ST from outcrossing to selfing/clonal to mainly clonal species (Table 3.6), as expected ( of Oenanthe aquatica on the feathers of water birds (Hroudova et al. 1992) and nutlets of Lycopus europaeus can be dispersed through endozoochory by mallards (Kleyheeg et al. 2015). ...
Species assembly from a regional pool into local metacommunities and how they colonize and coexist over time and space is essential to understand how communities response to their environment including abiotic and biotic factors. In highly disturbed landscapes, connectivity of isolated habitat patches is essential to maintain biodiversity and the entire ecosystem functioning. In northeast Germany, a high density of the small water bodies called kettle holes, are good systems to study metacommunities due to their condition as “aquatic islands” suitable for hygrophilous species that are surrounded by in unsuitable matrix of crop fields. The main objective of this thesis was to infer the main ecological processes shaping plant communities and their response to the environment, from biodiversity patterns and key life-history traits involved in connectivity using ecological and genetic approaches; and to provide first insights of the role of kettle holes harboring wild-bee species as important mobile linkers connecting plant communities in this insular system. t a community level, I compared plant diversity patterns and trait composition in ephemeral vs. permanent kettle holes). My results showed that types of kettle holes act as environmental filers shaping plant diversity, community-composition and trait-distribution, suggesting species sorting and niche processes in both types of kettle holes. At a population level, I further analyzed the role of dispersal and reproductive strategies of four selected species occurring in permanent kettle holes. Using microsatellites, I found that breeding system (degree of clonality), is the main factor shaping genetic diversity and genetic divergence. Although, higher gene flow and lower genetic differentiation among populations in wind vs. insect pollinated species was also found, suggesting that dispersal mechanisms played a role related to gene flow and connectivity. For most flowering plants, pollinators play an important role connecting communities. Therefore, as a first insight of the potential mobile linkers of these plant communities, I investigated the diversity wild-bees occurring in these kettle holes. My main results showed that local habitat quality (flower resources) had a positive effect on bee diversity, while habitat heterogeneity (number of natural landscape elements surrounding kettle holes 100–300m), was negatively correlated. This thesis covers from genetic flow at individual and population level to plant community assembly. My results showed how patterns of biodiversity, dispersal and reproduction strategies in plant population and communities can be used to infer ecological processes. In addition, I showed the importance of life-history traits and the relationship between species and their abiotic and biotic interactions. Furthermore, I included a different level of mobile linkers (pollinators) for a better understanding of another level of the system. This integration is essential to understand how communities respond to their surrounding environment and how disturbances such as agriculture, land-use and climate change might affect them. I highlight the need to integrate many scientific areas covering from genes to ecosystems at different spatiotemporal scales for a better understanding, management and conservation of our ecosystems.
... Although increasing, the amount and detail of information on longdistance movements of waterbirds is still limited. Most previous studies have estimated long-distance dispersal by migratory birds mainly by multiplying retention time distributions with the known flight speed of a bird (Charalambidou et al., 2005;Soons et al., 2008;Kleyheeg et al., 2015). This provides maximum dispersal distances based on the assumption of unidirectional flight at a constant speed, initiated directly after seed ingestion. ...
... The shape of the retention curve is, however, affected by more seed traits than size alone and looks different for different plant species. Most importantly, seed survival (intact passage) interacts with retention time, whereby resistant seeds are able to survive sustained exposure to digestive processes, resulting in a fatter tail of the retention time distribution and longer dispersal distances (Kleyheeg et al., 2015). Resistance to digestion of seeds within the same size range depends among other factors on seed shape and seed coat traits (Wongsriphuek et al., 2008;Kleyheeg et al., 2018), which should be considered when estimating dispersal distances for specific plant species. ...
... The integration of the detailed movement behavior of the dispersal agent into mechanistic models inevitably yields lower dispersal distance estimates than when assuming continuous unidirectional flight. Previous studies multiplying retention times with mallard flight speed estimated dispersal distances in the range of 300-1,400 km for mallards in North-America (Mueller and van der Valk, 2002), while others reported distances typically around 200 km and rarely exceeding 450 km (Kleyheeg et al., 2015), at least up to 312 km (Farmer et al., 2017), or a vast majority of dispersal events within 350 km (Soons et al., 2008). Viana et al. (2013b) compared these calculations with estimations based on ring recovery data during autumn migration and found median dispersal distances of 21-63 km based on ring recovery data vs. 148-840 km based on average flight speed of mallard and teal (A. ...
Long-distance seed dispersal is an important ecosystem service provided by migratory animals. Plants inhabiting discrete habitats, like lakes and wetlands, experience dispersal limitation, and rely heavily on zoochory for their spatial population dynamics. Granivorous waterbirds may disperse viable seeds of wetland plants over long distances during migration. The limited knowledge of waterbird migration has long hampered the evaluation of the importance of waterbirds in seed dispersal, requiring key metrics such as realistic dispersal distances. Using recent GPS tracking of mallards during spring migration, we built a mechanistic seed dispersal model to estimate realistic dispersal distances. Mallards are abundant, partially migratory ducks known to consume seeds of >300 European plant species. Based on the tracking data, we informed a mallard migration simulator to obtain a probabilistic spring migration model for the mallard population wintering at Lake Constance in Southern Germany. We combined the spring migration model with seed retention curves to develop seed dispersal kernels. We also assessed the effects of pre-migratory fasting and the availability of suitable deposition habitats for aquatic and wetland plants. Our results show that mallards at Lake Constance can disperse seeds in the northeastern direction over median distances of 293 and 413 km for seeds with short and long retention times, respectively, assuming a departure immediately after foraging. Pre-migratory fasting strongly affected the dispersal potential, with only 1–7% of ingested seeds left for dispersal after fasting for 12 h. Availability of a suitable deposition habitat was generally <5% along the migratory flyway. The high probability of seed deposition in a freshwater habitat during the first stopover, after the mallards completed the first migratory flight, makes successful dispersal most likely to happen at 204–322 km from Lake Constance. We concluded that the directed long-distance dispersal of plant seeds, realized by mallards on spring migration, may contribute significantly to large scale spatial plant population dynamics, including range expansion in response to shifting temperature and rainfall patterns under global warming. Our dispersal model is the first to incorporate detailed behavior of migratory waterbirds and can be readily adjusted to include other vector species when tracking data are available.
... Experimental feeding trials with captive waterfowl have repeatedly shown that seed survival and retention time depend primarily on seed size (e.g., Soons et al., 2008;Mueller & Valk, 2002;Wongsriphuek, Dugger, & Bartuszevige, 2008;Reynolds & Cumming, 2016) and digestive tract performance (e.g., Figuerola, Green, Black, & Okamura, 2004;Leeuwen, Tollenaar, & Klaassen, 2012;Kleyheeg, Leeuwen, Morison, Nolet, & Soons, 2015). The size or volume of seeds consumed by waterfowl varies over several orders of magnitude and is an important determinant of endozoochorous dispersal capacity between and within plant species (Figuerola, Charalambidou, Santamaría, & Green, 2010;Soons et al., 2008). ...
... Similarly, digestive performance is highly variable between waterfowl species (Barnes & Thomas, 1987;Kehoe & Ankney, 1985), between individuals of the same species Whyte & Bolen, 1985), and even within individuals over time (Charalambidou, Santamaría, Jansen, & Nolet, 2005;Kleyheeg et al., 2015;Leeuwen, Tollenaar, et al., 2012). Digestive tract morphology of waterfowl is highly adaptive, as shown for small intestine length, which increased dramatically with increasing food consumption in Bewick's swans (Cygnus bewickii Gils et al., 2008) and mallards (Anas platyrhynchos Miller, 1975), as well as for gizzard size, which responds rapidly to changes in diet quality in the field Whyte & Bolen, 1985) and in captivity (Kehoe, Ankney, & Alisauskas, 1988;Miller, 1975). ...
... For resilient large seeds, which survive mechanical treatment in the gizzard, the retention in the gizzard eventually results in longer gut passage times than for small seeds. On the other hand, soft large seeds (e.g., those used in Kleyheeg et al., 2015) will always be destroyed with prolonged retention in the gizzard and only the few seeds that do pass rapidly will be excreted intact, resulting in short retention times. ...
Many plants and invertebrates rely on internal transport by animals for long‐distance dispersal. Their dispersal capacity is greatly influenced by interactions with the animal's digestive tract. Omnivorous birds adjust their digestive tract morphology to seasonally variable diets. We performed feeding trials in waterfowl to unravel how changing organ size, in combination with seed size, affects dispersal potential. We subjected captive mallards to mimics of summer (animal‐based), winter (plant‐based), and intermediate diets, and analyzed gut passage of seeds before and after the treatment (trials 1 and 2). To test the effect of gut morphology on seed digestion, we measured digestive organ size after euthanasia. Three hours before euthanasia, differently sized seeds were fed to test how seed size affects gut passage by determining their relative position in the digestive tract (trial 3). Trials 1 and 2 showed that intact seed passage was lower in the plant‐based than in the animal‐based diet group. Retention time changed only within groups, decreasing in the animal‐based, and increasing in the plant‐based diet group. No post‐diet differences in organ size were detected, probably due to large between‐individual variation within groups. Digestive tract measures did not explain variation in seed survival or retention time. Trial 3 revealed that small seeds pass the digestive tract rapidly, while large seeds are retained longer, particularly in the gizzard. Differential retention in the gizzard, the section where seeds can be destroyed, is likely why larger seeds have a lower probability to pass the digestive tract intact. Our results confirm that rapid, flexible adaptation to diet shifts affects seed digestion in waterfowl, although we could not conclusively relate this to organ size. Large interindividual variation in digestive efficiency between mallards feeding on the same diet may provide opportunities for seed dispersal in the field throughout the annual cycle.
... Most importantly, feeding trials unequivocally demonstrate that destruction of seeds in the gizzard, rather than scarification, chemical or intestinal treatments, is limiting for viable gut passage. Especially large seeds have low probabilities of passing the gizzard undamaged in the first place, despite the larger force required to break them [11][12][13]43,44]. After losses due to breakage, the viability of defecated intact seeds depends on effects of combined scarification and chemical treatment, mediated by seed volume and seed coat strength. ...
... However, also seeds with weaker seed coats suffer greatly from the combined treatment. The latter may explain the remarkably low survival of the smallest seeds used in Kleyheeg et al. [43], which indeed had a very permeable seed coat, and this seems to be the second-most important determinant of intact gut passage. Wongsriphuek et al. [31] showed that seeds with high fibre content (indicating a stronger seed coat) had a higher probability of intact gut passage and a lower germination, supporting the seed coat effects found in this study. ...
... In general, the germinability of treated versus control seeds was relatively high compared to feeding trial studies (e.g. [12,43]). We have not tested the cumulative effect of the mechanical, chemical and intestinal treatments, which would more closely resemble the passage through the entire digestive tract and likely reduce general viability. ...
Waterbirds disperse a wide range of plant seeds via their guts, promoting biotic connectivity between isolated habitat patches. However, the intensity of digestive forces encountered by seeds, and therefore their potential to survive digestive tract passage, varies within and between waterbird species. Here, we investigate under controlled conditions how the interaction between seed traits and digestive strategies affect the germinability of seeds following waterbird-mediated dispersal. We exposed seeds of 30 wetland plant species to the main digestive processes in the dabbling duck digestive system: mechanical, chemical and intestinal digestion. These were simulated by 1) a pressure test and scarification treatment, 2) incubation in simulated gastric juice, and 3) incubation in intestinal contents of culled mallards (Anas platyrhynchos). We evaluated their separate and combined effects on seed germination, and identified the role of seed size and seed coat traits in resisting the digestive forces. Seeds were generally resistant to separate digestive processes, but highly sensitive to a combination. Resistance to mechanical break-down was reduced by up to 80% by chemical pre-treatment, especially for seeds with permeable coats. Scarified seeds were 12–17% more vulnerable to chemical and intestinal digestive processes than undamaged seeds. Large seeds and seeds with thin, permeable coats were particularly sensitive to chemical and intestinal digestion. These results indicate that efficient digestion of seeds requires multiple digestive processes. The gizzard, responsible for mechanical digestion, plays a key role in seed survival. Omnivorous birds, which have relatively light gizzards compared to pure herbivores or granivores, are thus most likely to disperse seeds successfully. Regardless of digestive strategy, small seeds with tough seed coats are most resistant to digestion and may be adapted to endozoochorous dispersal by waterbirds.
... Research, particularly over the last decade, has shifted focus from simply determining what waterbirds are dispersing to developing a mechanistic understanding of the processes underlying the patterns of dispersal in these wetland systems (Soons et al. 2008;Viana et al. 2013b;Kleyheeg et al. 2014). To explore the mechanisms contributing to the spatial patterns of seed dispersal we must recognise all phases of dispersal; ...
... Research on the retention times of propagules in the gut of captive waterbirds has provided key insights into the propagule traits (e.g. seed size) that facilitate endozoochory (Soons et al. 2008 Kleyheeg et al. 2014). However, estimates of the retention times of propagules remain highly variable Soons et al. 2008;Brochet et al. 2010c;García-Álvarez et al. 2015) and thus more studies are required to establish generalities across propagule species and vectors. ...
... These trials provide essential information on the time taken for seeds to pass through the digestive tract, and are used to quantify the proportion of seeds that survive gut passage and remain viable (Soons et al. 2008). In addition, feeding trails can be used to determine how variation in seed traits amongst plant species can affect the dispersal parameters (Soons et al. 2008;Kleyheeg et al. 2014), providing further insights into the mechanisms underpinning successful endozoochorous dispersal. Recently, feeding trials have been used to quantitatively compare the potential for waterbird mediated dispersal amongst a variety of wetland plants Soons et al. 2008;Brochet et al. 2010c). ...
... Current estimations of dispersal distances following transportation by mallards and other waterbirds are based on simple models, often identifying only maximum dispersal distances as estimated from gut retention time and flight speed during non-stop unidirectional flights directly after seed ingestion (e.g. Charalambidou, Santamar ıa & Langevoord 2003;Soons et al. 2008;Kleyheeg et al. 2015; but see Viana et al. 2013a). Indeed, long-distance dispersal (LDD) is of disproportional importance for spatial plant population dynamics (Cain, Milligan & Strand 2000;Nathan 2006), and migratory mallards and teal (A. ...
... Here, we quantify the dispersal patterns of seeds transported internally by mallards during their frequent daily movements in the autumn-winter period, taking advantage of the detailed information which has recently become available on all essential components of this dispersal mechanism: (i) the range of seed species ingested (Kleyheeg, Klaassen & Soons 2016;Soons et al. 2016a); (ii) empirically determined gut passage times and survival rates across a range of seed traits (Soons et al. 2008;van Leeuwen et al. 2012;Kleyheeg et al. 2015); and (iii) mallard movement data from high-resolution GPS tracks across a range of landscapes (Kleyheeg 2015). We combined these components in a single, mechanistic, spatially explicit model to analyse seed dispersal patterns. ...
... We combined these components in a single, mechanistic, spatially explicit model to analyse seed dispersal patterns. We specifically evaluated the relative contributions of landscape-dependent mallard movement behaviour and of seed volume, the latter being consistently reported as one of the most relevant seed traits determining gut passage time and survival Soons et al. 2008;van Leeuwen et al. 2012;Kleyheeg et al. 2015), in establishing these patterns. ...
Dispersal via animals (zoochory) is a primary mechanism for seed exchange between habitat patches. Recent studies have established that many plant species can survive waterbird gut passage. To quantify the patterns and consequences of waterbird‐mediated dispersal, information on ingestion and gut passage must be combined with bird movement data. Such analysis has recently revealed seed dispersal kernels by migrating waterbirds. However, since many waterbird populations are largely resident, and migrating populations spend only a minor part of the main dispersal season (autumn–winter) on active migration, daily regional‐scale movements probably cause more frequent dispersal.
We synthesized high‐resolution empirical data on landscape‐scale movements and seed gut passage times in a key disperser species, the mallard ( A nas platyrhynchos ), using a spatially explicit, mechanistic model to quantify dispersal distributions resulting from daily autumn–winter movements. We evaluated how landscape composition and seed traits affect these dispersal patterns.
The model indicates that mallards generate highly clumped seed deposition patterns, dispersing seeds primarily between core areas used for foraging and resting. Approximately 34% of all dispersed seeds are transported to communal roost areas, which may function as reservoirs for mallard‐dispersed species, and 7% are transported between foraging areas. Landscape‐dependent movement patterns strongly affect the dispersal distributions, resulting in multi‐modal dispersal kernels, with dispersal distances increasing with fragmentation of freshwater foraging habitat. Seed size‐related gut retention times determine the proportion of seeds being dispersed away from the ingestion area, with larger seeds (20 mm ³ ) having a 8–10% higher potential for long‐distance dispersal than smaller seeds (0·2 mm ³ ), if surviving gut passage. However, twice as many small seeds will finally accomplish long‐distance dispersal due to their higher gut passage survival.
Synthesis . Firstly, this study reveals how seed dispersal patterns resulting from daily waterfowl movements are shaped by landscape‐dependent differences in movement patterns. Secondly, seed survival appears more important than retention time in determining the scale of long‐distance dispersal by non‐migrating mallards. We conclude that the frequent flights of staging waterbirds result in directed dispersal over distances inversely related to wetland availability, indicating that they maintain landscape connectivity across a range from wet to increasingly dry landscapes.
... These trials provide essential information on the time taken for seeds to pass through the digestive tract, and are used to quantify the proportion of seeds that survive gut passage and remain viable (Soons et al., 2008). In addition, feeding trails can be used to determine how variation in seed traits among plant species can affect the dispersal parameters (Soons et al., 2008;Kleyheeg et al., 2014), providing further insights into the mechanisms underpinning successful endozoochorous dispersal. Recently, feeding trials have been used to quantitatively compare the potential for waterbird-mediated dispersal among a variety of wetland plants (Charalambidou et al., 2005;Soons et al., 2008;Brochet et al., 2010). ...
... We investigated how variation in seed traits affects the dispersal parametersretention time, recoverability and germinabilityof wetland plants dispersed by two different waterfowl vectors in southern Africa. Previous research has suggested that seed size and hardness are important traits that can produce variation in dispersal (Soons et al., 2008;Kleyheeg et al., 2014). Furthermore, differences between vectors in body size and digestive physiology, for example, can also have important consequences for the dispersal of wetland plants (Viana et al., 2013a;Garc ıa-Alvarez et al., 2015). ...
... For each of the four cases, all numerical covariates were centred and individual bird was included as a random effect to account for differences among individuals. Seed species was also included as a random effect to avoid pseudo-replication due to multiple observations for equal seed sizes (see Kleyheeg et al., 2014). ...
Patterns of seed dispersal are strongly influenced by disperser and propagule traits. However, the relative importance of these characteristics for dispersal outcomes is unclear.
We investigated differences in the potential dispersal of wetland plants between Egyptian goose ( Alopochen aegyptiaca ) and red‐billed teal (Anas erythrorhyncha ), two southern African Anatidae. The seeds of seven wetland plants with varying traits were fed to the birds and the dispersal parameters of gut passage time, recoverability and germinability of ingested seed were determined.
We tested the effect of disperser species and seed traits on dispersal parameters. In addition, we determined whether increased retention times lead to lower recovery and germination of ingested seed. We predicted that the seed traits of small size and increased hardness would be better at mediating the trade‐off between retention time and recoverability and germination, but that this might differ between vectors.
The dispersal parameters varied significantly between Egyptian goose and red‐billed teal. In particular, Egyptian goose had longer average and maximum retention times of seeds, but also higher recoverability. Furthermore, short seeds had significantly longer average retention time and were also recovered in the highest numbers. Short seed length potentially facilitates endozoochory by two complementary mechanisms. First, short seeds are less digestible, leading to higher recoverability. Second, due to lower digestibility, short seeds are able to survive at longer retention times to be dispersed further, similarly to hard seeds (with hardness positively correlated with seed mass).
Our results suggest that small seed length and hardness are optimal seed traits facilitating endozoochory in wetland plants. Dispersal parameters were also influenced by the bird species and indicate that differences in vector morphology and digestive physiology may likely have important consequences for seed dispersal. Hence, vector characteristics should be given more explicit consideration in future studies of seed dispersal in aquatic systems.
... Differential levels of activity in birds could translate into differences in gut retention times, with more active individuals showing shorter retention times (Kleyheeg et al., 2015;Van Leeuwen et al., 2012), ultimately affecting both seed retention time and germination rates. Therefore, evidence suggests that different individuals of a given species may not provide functionally equivalent seed dispersal services (Zwolak, 2018). ...
... In the wild, males of some bird species are more territorial and often present higher activity levels compared to females (Evans & Stutchbury, 2012;Williams & Rabenold, 2005), which could TA B L E 1 Results from multiple linear models addressing the effects of body mass and sex on seed retention time in the gut, and binomial generalized linear models testing the effect of body mass, seed retention time, and treatment (gut passed vs. control) on seed germination. induce an accelerated gut passage time (Kleyheeg et al., 2015;Van Leeuwen et al., 2012). Although we did not collect data on the activity level of the thrushes during our experiment, it is unlikely that remarkable differences in mobility could be expressed given the spatial limitation imposed by the cages. ...
Frugivorous animals play crucial roles dispersing seeds away from parental plants and influencing plant recruitment. Most studies focus on comparisons of seed dispersal services provided by distinct species of animals, but neglect how within-species variation may affect dispersal. Individual traits, such as body mass and sex, are related to metabolic rates, gut load capacity, and transit times that potentially influence dispersal quantity and quality. Here, we aim at answering if individual traits (body mass and sex) of Pale-breasted Thrushes (Turdus leucomelas) affect seed dispersal quality by testing the following hypotheses (a) individual traits influence seed retention time and germination, (b) seed retention time affects seed germination, and (c) seed passage through the gut enhances germination. We found that females retained seeds in the gut for longer periods than males. Gut passed and manually depulped seeds had similar germination success. However, heavier birds, irrespective of sex, had longer seed retention times and promoted higher germination. Our results indicate that intraspecific differences in morphological traits of frugivores are a source of variation in dispersal outputs and may help to explain complex patterns of seed dispersal. We highlight the importance of considering the quality of seed dispersal at an individuallevel, as well as at a species-level, and reinforce that some individuals may contribute more to seed germination, and potentially recruitment, than others. Finally, a decrease in body masses of tropical birds in response to global warming may cascade to a decrease in seed dispersal quality.
... Differential levels of activity in birds could translate into differences in gut retention times, with more active individuals showing shorter retention times (Kleyheeg et al., 2015;Van Leeuwen et al., 2012), ultimately affecting both seed retention time and germination rates. Therefore, evidence suggests that different individuals of a given species may not provide functionally equivalent seed dispersal services (Zwolak, 2018). ...
... In the wild, males of some bird species are more territorial and often present higher activity levels compared to females (Evans & Stutchbury, 2012;Williams & Rabenold, 2005), which could TA B L E 1 Results from multiple linear models addressing the effects of body mass and sex on seed retention time in the gut, and binomial generalized linear models testing the effect of body mass, seed retention time, and treatment (gut passed vs. control) on seed germination. induce an accelerated gut passage time (Kleyheeg et al., 2015;Van Leeuwen et al., 2012). Although we did not collect data on the activity level of the thrushes during our experiment, it is unlikely that remarkable differences in mobility could be expressed given the spatial limitation imposed by the cages. ...
Frugivorous animals play crucial roles dispersing seeds away from parental plants and influencing plant recruitment. Most studies focus on comparisons of seed dispersal services provided by distinct species of animals, but neglect how within‐species variation may affect dispersal. Individual traits, such as body mass and sex, are related to metabolic rates, gut load capacity, and transit times that potentially influence dispersal quantity and quality. Here, we aim at answering if individual traits (body mass and sex) of Pale‐breasted Thrushes ( Turdus leucomelas ) affect seed dispersal quality by testing the following hypotheses (a) individual traits influence seed retention time and germination, (b) seed retention time affects seed germination, and (c) seed passage through the gut enhances germination. We found that females retained seeds in the gut for longer periods than males. Gut passed and manually depulped seeds had similar germination success. However, heavier birds, irrespective of sex, had longer seed retention times and promoted higher germination. Our results indicate that intraspecific differences in morphological traits of frugivores are a source of variation in dispersal outputs and may help to explain complex patterns of seed dispersal. We highlight the importance of considering the quality of seed dispersal at an individual‐level, as well as at a species‐level, and reinforce that some individuals may contribute more to seed germination, and potentially recruitment, than others. Finally, a decrease in body masses of tropical birds in response to global warming may cascade to a decrease in seed dispersal quality.
Abstract in Portuguese is available with online material.
... Experimental feeding under controlled conditions for dispersal vectors is an effective and feasible way to measure endozoochory parameters, with minimal damage to dispersal vectors [28]. Even though experimental results have repeatedly highlighted that seed retention time depends largely on seed traits [22,29,30] and digestive processes [31,32], there have been no consistent conclusions on the effect of seed traits on dispersal effectiveness. For example, smaller seeds have a higher survival rate and shorter retention time within mallard guts [29], whereas other studies showed that seed size had little impact on the dispersal potential by teals [6,28], making further research more important and necessary. ...
... Moreover, the present results showed that retention time squared had a significant negative effect on the number of recovered seeds. Another study indicated that a short retention time with a lower risk of digestion results in a higher number of recovered seeds [32]. Additionally, the present findings indicated that germination decreased along with a greater retention time, which was similar to the results of a previous study [28]. ...
Simple Summary
Quantifying the effects of seed traits on waterbird-mediated seed dispersal effectiveness contributes to understanding wetland plant ecology and hence can be used for improving wetland conservation and restoration, especially in the global scenario of wetland degradation and destruction. Waterbirds, especially dabbling ducks, can effectively disperse wetland plant seeds through their guts (endozoochory). Here, we experimentally quantified the effects of seed traits (length and lignin) on retention time, retrieval, and germination of surviving seeds. The results showed that the germination rate of recovered seeds was higher than the controls, suggesting that endozoochory contributes to seed germination. Local seed dispersal was more efficient, and long-distance dispersal was possible. Furthermore, smaller seeds passed through the guts faster, and there was no significant effect of disperser species on germination. We concluded that waterbird-mediated endozoochory plays an important role in wetlands.
Abstract
Seed dispersal is an important ecological process in wetland ecosystems and helps maintain community structure and ecosystem biodiversity. Waterbird-mediated endozoochory is an effective and feasible dispersal mechanism for wetland plants; however, the influence of vectors and seed traits on this mechanism remains unclear. To investigate the effects of vector species and seed traits (length and lignin) on retention time, retrieval and germination of gut-surviving seeds, we fed Baikal teals (Anas formosa) and green-winged teals (Anas crecca) eight common plant seeds (Polygonum aviculare, Rumex dentatus, Polygonum orientale, Vallisneria natans, Ranunculus polii, Polygonum hydropiper, Carex cinerascen and Euphrasia pectinata) in the Shengjin Lake wetland (a Ramsar site). We collected fecal samples at intervals of 2–6 h for 36 h, and found that the percentage of recovered seeds differed significantly among teal and plant species (3%~30%); 94% of viable seeds were recovered within 12 h after feeding. Moreover, the germination rate of the recovered seeds (25%~56%) was higher than that of the control. The seed retention time was affected by seed lignin and disperser species; higher lignin made digestion difficult with higher retrieval. Smaller seeds passed through the guts but had no significant effect on recovered seeds. Seed length and disperser species showed no significant correlation with germination. These findings suggested endozoochory by dabbling ducks as an effective wetland seed dispersal mechanism.
... Experimental studies of waterbird endozoochory have revealed strong variation in gut retention times and NFF seed survival between individual birds Kleyheeg et al., 2015), and retention time curves are influenced by many factors including diet, age, stress and gender (Kleyheeg et al., 2018;van Leeuwen, Tollenaar, et al., 2012). We did not consider the differences between seven individual gulls used to generate our experimental retention time curve, but instead we compared it with a theoretical curve generated from Viana et al. (2016) and Yoshiwaka et al. (2019). ...
... Results in captivity may be influenced by the lack of flying activity. Kleyheeg et al. (2015) found that seed passage through the digestive tract of mallards increased by up to 80% with physical activity compared with animals resting in conventional cages, but there was little effect on the shape of the retention time curve. We did not study long-distance migratory flights, hence captive experiments may reasonably reflect the field conditions in which gulls were spending the majority of the day stationary, and often roosting after completing a feeding bout. ...
Grading the fecal consistency of carnivores is a frequently used tool for monitoring gut health and overall digestion. Several fecal consistency grading systems are available for mainly felids and canids. No such system exists for the brown bear (Ursus arctos Linnaeus, 1758). We aim at extending current fecal consistency grading systems with a scoring system for brown bears. The system was set up during a diet study with nine individuals fed a variety of diets including beef meat, rabbit, fruit, and grass‐fruit‐pellet mix in an incomplete crossover design. One additional individual was included opportunistically and was fed the typical zoo diet (vegetable‐fruit‐meat‐pellet diet). All feces from the collection period were photographed, graded by “handling the feces” and visually inspected for dietary components. Based on a total of 446 feces, a six‐point scale for uniform fecal consistencies was established. In 11% of all feces, two distinct consistencies could be distinguished, a feature that appears in other carnivore species as well. Hence, an additional grading system for dual consistencies was developed. The fecal consistency of brown bears is heavily dependent on the diet items processed before defecation with the general observation that the more vegetation or whole prey, the firmer the feces, and at certain proportions of the latter, the higher the chance for dual fecal consistencies to occur. The results indicate that in bears, diet may have a strong effect on fecal consistency, hampering animal health assessments without prior knowledge of the diet.
Research Highlight
We provide a fecal consistency scale for the objective grading of brown bear feces. Dual fecal consistencies occurred for which a separate scale was developed. Diet has a major effect on consistency and may hamper health assessments.
... Experimental studies of waterbird endozoochory have revealed strong variation in gut retention times and NFF seed survival between individual birds Kleyheeg et al., 2015), and retention time curves are influenced by many factors including diet, age, stress and gender (Kleyheeg et al., 2018;van Leeuwen, Tollenaar, et al., 2012). We did not consider the differences between seven individual gulls used to generate our experimental retention time curve, but instead we compared it with a theoretical curve generated from Viana et al. (2016) and Yoshiwaka et al. (2019). ...
... Results in captivity may be influenced by the lack of flying activity. Kleyheeg et al. (2015) found that seed passage through the digestive tract of mallards increased by up to 80% with physical activity compared with animals resting in conventional cages, but there was little effect on the shape of the retention time curve. We did not study long-distance migratory flights, hence captive experiments may reasonably reflect the field conditions in which gulls were spending the majority of the day stationary, and often roosting after completing a feeding bout. ...
Non‐frugivorous waterbirds disperse a wide variety of plants by endozoochory, providing longer‐dispersal distances than other mechanisms. Many waterbirds visit both agricultural and natural landscapes during their daily movements, but potential bird‐mediated dispersal of weed plants within and from agricultural landscapes to other habitats is commonly overlooked. Gulls (Laridae) are expanding in numbers and increasingly exploiting anthropogenic habitats worldwide, with possible growing implications for the spread of weeds. Yet, to date, there are no studies on the spatial distribution of weed dispersal by waterbirds.
We developed a plant dispersal model based on movements of 19 Larus fuscus using ricefields, via GPS telemetry. We combined daily movements with two curves estimating the retention times of plant seeds in their guts: (a) an experimental curve based on retention time in captivity for four weeds with dry fruits known to be dispersed by gulls: Juncus bufonius, Cyperus difformis, Polypogon monspeliensis and the alien Amaranthus retroflexus; (b) a theoretical curve based on the interspecific scaling relationship between body mass and mean retention time.
Median dispersal distances of weed plant seeds by gulls ranged between 690 and 940 m, but maximum distances exceeded 150 km. The theoretical retention time model showed higher median dispersal distances than the experimental retention time model. Spatial patterns of weed deposition were very similar between retention time methods, and most strongly depended on gull movements. Variation between individual gulls had little influence on seed shadows. About 92% of all seeds (>10,000 intact seeds per day) were dispersed within the ricefield area of 370 km². The remaining 8% of seeds were deposited beyond ricefields into other habitats, 42% of which reached moist environments (other irrigated agriculture, rivers and natural wetlands) presumably suitable for weed establishment.
Synthesis. Gulls can disperse weed plants over long distances across a mosaic of habitats. This implies exchange of weed plant species between human‐dominated and natural areas by waterbirds as dispersal vectors. This spatial study highlights the importance of non‐frugivorous birds for long‐distance plant dispersal, which is generally an overlooked mechanism in studies aiming to predict and manage expansion of weed plants.
... In Oenanthe aquatica and Lycopus europaeus, pollen transfer is mediated by insects and seed dispersal is mediated by water, while in Typha latifolia and Phragmites australis pollen and seeds are adapted to wind dispersal (Kühn et al. 2004;Kleyer et al. 2008). Occasionally, seeds can be dispersed by animals, mainly water birds through exozoochory in Typha and Phragmites and endozoochory in Lycopus and Oenanthe (Hroudova et al. 1992;Green et al. 2008;Brochet et al. 2009;Kleyheeg et al. 2015). Hereafter, species are referred by their genus. ...
... Finally, it is important also to account for dispersal via birds such as waterfowl (Charalambidou et al. 2005;Brochet et al. 2009;Soons et al. 2016). Previous studies have shown that seeds of Phragmites australis and Typha latifolia can be dispersed on the feathers of ducks (Brochet et al. 2009), seeds of Oenanthe aquatica on the feathers of water birds (Hroudova et al. 1992), and nutlets of Lycopus europaeus can be dispersed through endozoochory by mallards (Kleyheeg et al. 2015). However, to disentangle the effect of dispersal vectors in population connectivity, more direct observations are needed. ...
In plants, long-distance dispersal is both attenuated and directed by specific movement vectors, including animals, wind, and/or water. Hence, movement vectors partly shape metapopulation genetic patterns that are, however, also influenced by other life-history traits such as clonal growth. We studied the relationship between area, isolation, plant-species richness, reproduction, and dispersal mechanisms with genetic diversity and divergence in 4 widespread wetland plant-species in a total of 20 island-like kettle-hole habitats surrounded by an intensive agricultural landscape. Our results showed that genetic parameters reflect the reproduction strategies with the highest genetic diversity being observed in the non-clonal, outcrossing Oenanthe aquatica compared to the clonal Lycopus europaeus, Typha latifolia, and Phragmites australis. Lycopus showed a positive relationship between genetic diversity and kettle-hole area, but a negative relationship with the number of neighboring kettle holes (less isolation). Genetic diversity increased with plant-species richness in the clonal species Phragmites and Lycopus; while it decreased in the non-clonal Oenanthe. Finally, genetic divergence and, therefore, connectivity differed between alternative dispersal strategies, where wind-dispersed Typha and Phragmites had a higher gene flow between the analyzed kettle holes compared with the insect-pollinated, hydrochorous Lycopus and Oenanthe. Our study provides information on genetic patterns related to reproduction and dispersal mechanisms of 4 common wetland species contributing to the understanding of the functioning of plant metacommunities occurring in kettle holes embedded in agricultural landscapes.
... The feeding and roosting ecology of a species are key factors in explaining population structure and meta-population functioning (Kleyheeg et al. 2015). For fruit bats, when food and/ or roost resources are limited, or spread over time and space, individuals might be forced to disperse to follow resource distribution (Bessa et al. 2015;Kleyheeg et al. 2015). ...
... The feeding and roosting ecology of a species are key factors in explaining population structure and meta-population functioning (Kleyheeg et al. 2015). For fruit bats, when food and/ or roost resources are limited, or spread over time and space, individuals might be forced to disperse to follow resource distribution (Bessa et al. 2015;Kleyheeg et al. 2015). Our two study species forage on fruit and nectar, resources that typically show high variation over time and space (Trewhella et al. 2001). ...
Pteropus livingstonii and Pteropus seychellensis comorensis are endemic fruit bat species that are among the most threatened animals in the Comoros archipelago. Both species are pollinators and seed dispersers of native and cultivated plants and are thus of crucial importance for the regeneration of natural forests as well as for cultivated plantations. However, these species are subject to strong anthropogenic pressures and face one of the highest rates of natural habitat loss reported worldwide. Yet little is known about the population genetic structure of these two species, making it difficult to define relevant conservation strategies. In this study, we investigated for the two flying fox species (1) the level of genetic diversity within islands, as well as across the archipelago and (2) the genetic structure between the two islands (Anjouan and Mohéli) for P. livingstonii and between the four islands of the archipelago (Anjouan, Mohéli, Grande Comore and Mayotte) for P. s. comorensis using mitochondrial and microsatellite markers. The results revealed contrasting patterns of genetic structure, with P. s. comorensis showing low genetic structure between islands, whereas P. livingstonii exhibited high levels of inter-island genetic differentiation. Overall, the genetic analyses showed low genetic diversity for both species. These contrasting genetic patterns may be the result of different dispersal patterns and the populations’ evolutionary histories. Our findings lead us to suggest that in terms of conservation strategy, the two populations of P. livingstonii (on Anjouan and Mohéli islands) should be considered as two separate management units. We recommend focusing conservation efforts on the Anjouan population, which is the largest, exhibits the highest genetic diversity, and suffers the greatest anthropogenic pressure. As for P. s. comorensis, its four populations could be considered as a single unit for conservation management purposes. For this species, we recommend protecting roosting trees to reduce population disturbance.
... Feeding and roosting ecology of a species represent key factors to explain population structure and meta-population functioning (Kleyheeg et al., 2015). For fruit bats, when food and/or roost resources are limited, or spread over time and space, individuals might be forced to disperse to track resource distribution (Bessa et al., 2015;Kleyheeg et al., 2015). ...
... Feeding and roosting ecology of a species represent key factors to explain population structure and meta-population functioning (Kleyheeg et al., 2015). For fruit bats, when food and/or roost resources are limited, or spread over time and space, individuals might be forced to disperse to track resource distribution (Bessa et al., 2015;Kleyheeg et al., 2015). ...
The Comoros Islands are known for their important biodiversity with a high endemism rate for each taxonomic group. This natural richness face huge anthropogenic pressures due to a high rate of habitat loss and fragmentation estimated to be the highest in the word. Wild endemic mammals are the most threatened fauna in these islands. These species are often characterized by small population sizes making them highly vulnerable to disturbances. Indeed, small population size makes populations prone to allee effect, genetic drift or inbreeding depression, which subsequently conducts to a decrease of species’ evolutionary potential, thus diminishing their long term viability. In order to understand the effect of habitat disturbance on the Comoros Islands natural fauna, I studied two endemic and highly threatened flying fox species (Pteropus livingstonii with a population size estimated of 1300 individuals and P.seychellensis comorensis whose population is estimated to few thousands of individuals). For that, I combined different approaches including spatial distribution and ecological niche modeling, as well as population demography and socio-economic approaches. This integrated approach is crucial to identify the different causes of mammals’ population loss and propose relevant conservation measures. In a first part of this thesis, I show the results of the spatial distribution modeling and habitat selection of the two flying fox species as well as their geographic distribution ranges using Species Distribution Modelling (SDM) and Ensemble of Small Models approach specifically adapted to rare and threatened species. This first part allowed me to assess which ecological variables and anthropogenic pressures are determinant for the distribution of both species as well to characterize the degree of threat of the two species. In the second part of this thesis, I studied the genetic diversity and population structure of both species among the four islands of Comoros with the aim to look for possible gene flow breaks between sub-populations but also to uncover which species face a high risk of extinction. This study highlights that these two phylogenetic and morphologically related species show different genetic structures among islands. In a third part, I explored the feasibility and costs of a non-invasive genetic monitoring protocol to obtain accurate population size, demographic parameters and develop a long-term monitoring of P. livingstonii. Due to the sensitivity of this species to capture and handling but also because of its rareness, a direct monitoring using classical capture-recapture method was not possible. This study showed that this approach is realistic but involves a high cost that seems to be unsuitable with the budgets available for conservation of the species in the Comoros Islands. In a fourth part of my thesis, I characterized the anthropogenic pressures that impacts both species using a socio-economic characterization of these islands (forest exploitation and hunting pressures among others) by using semi-structured interviews and a Q-methodology approach. This allows me to understand the relationship of local communities with the local biodiversity as well as to interpret the ongoing natural habitat evolution and to predict its future. In the last chapter (fifth), I combined the results of all the different but complementary approaches used along the thesis with the aim to propose a management plan appropriate for these two species.
... This dispersal mechanism has generally been overlooked, despite that it could potentially lead to the long-distance spread of herbs that are typically associated with dispersal through abiotic agents (Green et al., 2022). Defecation of viable seeds could be due to digestive trade-offs driven by seasonal changes in diet and its processing for nutrient assimilation (Herrera, 1984;Kleyheeg et al., 2015;Soons et al., 2016). ...
In the intricate web of plant–animal interactions, granivore birds can play a dual antagonist–mutualist role as seed predators and dispersers. This study delves into the ecological significance of the house sparrow (Passer domesticus) as seed disperser by endozoochory. A sample of individual droppings and faecal pools were collected from a communal roost in central Spain to examine the presence of seeds. Seed viability was determined using the tetrazolium test. Our findings revealed that around 22% of the analysed droppings contained seeds, contradicting the prevalent notion of house sparrow solely as seed predator. Viability tests demonstrated that 53.9% of the defecated seeds were viable, although it varied between plant species, including those from fleshy‐fruited common fig and five species of dry‐fruited herbs. This study challenges the traditional perspectives on the ecological role of the house sparrow, and glimpses on their contribution to seed dispersal. Understanding the nuanced roles of granivore species like the house sparrow is crucial for developing holistic conservation and management strategies in urban and agricultural landscapes. Future studies are encouraged to unravel the actual role of this cosmopolitan species as disperser of a likely broad spectrum of wild, cultivated and exotic plants.
... They argue that this is explained by a loss of seeds due to more frequent germination events in areas with high frequency in mudflat exposure due to water level fluctuations and an increase in non-viable seeds and scouring of the sediment in areas with a low frequency in mudflat exposure. These effects of current water level fluctuations on the soil seed bank can be highly variable and dependent on environmental conditions such as soil moisture (Haukos and Smith, 1994;Ter Heerdt et al., 2017;Van Leeuwen et al., 2014) and presence of seed-dispersing birds that are dependent on specific water depths (Farley et al., 2022;Kleyheeg et al., 2015). In our study, the transect along the elevational gradient, (e.g., changes in water level due to seasonal fluctuations) is directly related to the distance to the vegetation border. ...
... The effects of vegetation management, such as prescribed fire, can also affect the availability of L. subcoriacea and other fleshy fruits in time and space [51,116] and influence L. subcoriacea SDE Q [59], but this variation was not included in our experiments. Finally, more nuanced, empirical information on dispersers (e.g., fruit-specific SRT, or perching times) could be incorporated into our model to potentially improve our understanding of L. subcoriacea seed dispersal [117,118]. ...
The primacy of endozoochory for the maintenance and expansion of many woody plant populations is well known, but seed dispersal is not well understood for most species. This is especially true for rare species, where small population size and low fruit production can limit field- or observation-based experiments. Additionally, the effect of environmental heterogeneity on disperser movement is rarely investigated but has been shown to improve estimates of plant population spatial patterns and dynamics. We used simulation experiments to explore the effects of environmental heterogeneity and disperser movement on Lindera subcoriacea seed dispersal, a rare shrub from the southeastern United States with avian-dispersed seeds. Our experiments incorporated environmental heterogeneity and simulated disperser movement for five bird species, based on either landscape permeability or straight path rules. We anticipated that permeability-based movement would result in greater dispersal distances and seed dispersal effectiveness, which characterizes both quantity and quality. Generally, we did not find differences in seed dispersal between permeability and straight path experiments. However, we did find that permeability-based experiments had greater deposition into suitable habitat during flight (23 vs. 1%). These rare but longer distance depositions may be especially important for plants that are influenced by gap or interpopulation dynamics. We also found consistently greater dispersal into high quality habitats regardless of disperser species in permeability experiments, implying that incorporating species-specific assessments of landscape utilization (occupancy) could influence the effectiveness of seed dispersal. Our study suggests that including environmental heterogeneity in seed dispersal models can provide additional insights not provided by avian parameters (e.g., gut capacity, seed retention time, and flight speed) commonly used to inform dispersal models.
... Birds tended to excrete a single seed when they ate larger fruits bearing larger seeds. Some studies have documented that retention time tends to be shorter for larger seeds (Hoppes, 1988;Levey and Grajal, 1991;Murray et al., 1993Murray et al., , 1994Fukui, 2003;Kleyheeg et al., 2015). Moreover, although defecated and regurgitated samples were not distinguished in this study, larger seeds may be more frequently regurgitated. ...
Frugivorous birds are the primary seed dispersers for fleshy-fruited plants through defecation. In general, smallsized species disperse seeds across short distances from parental plants. However, multiple seeds or seeds of different plant species are frequently mixed in the fecal mass, because birds are prone to eat multiple fruits of a few plant species during foraging. This suggests birds deposit seeds as clumps in the field, causing inter- and intraspecific competition. However, the exact number of dispersed seeds for each defecation is very hard to estimate in field. It may also vary according to several variables, such as body size of birds and number of seeds per fruit. To clarify seed deposition patterns, we captured small frugivorous birds and collected the feces and regurgitations. The number of seeds excreted in fecal samples was investigated. From 2003 to 2019, a total number of 21518 seeds from 60 plant species were collected from 2214 birds of 17 species. Average number of seeds included in the fecal sample was 9.7 ± SD 18.4 (range: 1–340). The frequency of the number of excreted seeds was not normally distributed and the mode value was one in all cases and for five main dispersers. In most cases (64.8–74.5%), birds excreted a single seed. Furthermore, the effects of morphological traits of birds and plants on number of excreted seeds were analyzed using GLMM. The body mass of birds had a positive effect on the number of excreted seeds. However, fruit and seed weight exhibited negative effects, suggesting the number of excreted seeds is smaller when smaller birds eat larger fruits bearing larger seeds. The seed deposition pattern based on excretion of a single seed may avoid seed and seedling aggregation at local sites
... As for the phytogeography of the species, 85% of the species inventoried in MNP occur on the African continent, 22% in the Maputaland Coastal Forest Mosaic ecoregion, where this study was developed, which converges with the results of research carried out in the same ecoregion stating that it is part of the Maputaland endemism (Smith and Leader-Williams 2006;Matimele et al. 2016;Darbyshire et al. 2019). On the other hand, 63% of species occur in other terrestrial ecoregions of Africa, and 15% of species occur in other terrestrial ecoregions of the World; this occurrence of species in other terrestrial ecoregions of Africa and the World can be explained by the dispersion theory at long distance (Carlquist 1966;Queiroz 2005;Gillespie et al. 2012;Bacon et al. 2015;Antonelli et al. 2018;Hackel and Sanmartín 2021), which is mostly made by cyclonic winds (Vittoz and Engler 2007), by migratory birds and sea currents (Eichberg et al. 2005;Costa et al. 2013;Kleyheeg et al. 2015;van Leeuwen 2018;van Toor et al. 2018). ...
Floristic research is essential for the conservation of biodiversity and one of the biggest challenges given the high level of human disturbances in Mozambican ecosystems. Coastal vegetation plays an important role in the environmental protection of dunes, preventing the advance of seawater toward the continent, in dune erosion and in the maintenance of ecosystem services. Seeking to support the protection of these environments, the present study aims to characterize the floristic aspects of the coastal dune forest in the Maputo National Park, Mozambique, associating this knowledge with future social, biological and environmental gains at the local, regional and global levels. This study addressed the following methodological procedures: (1) floristic sampling, where specimens of all woody, fertile or sterile individuals were collected from the sampled areas and identified; (2) analysis of floristic similarity between the studied area and the coastal floras of East and West Africa; (3) characterization of vegetation in terms of plant habit, ecological groups, dispersion and pollination syndromes and phytogeography. Families with the highest number of species in descending order were Rubiaceae, Loganiaceae, Meliaceae, Sapotaceae and Ebenaceae. The results showed that the greatest number of individuals are trees, of late secondary stage, zoochoric and melittophilous. The studied area is similar in vegetation to East-coast Africa, but differs from the West coastal. The different climatic environments that gave rise to different terrestrial ecoregions might have contributed to high and low floristic similarities between the coastal flora of East and West Africa.
... However, we are unaware of any evidence for this, and similar speculation has been rebutted in the case of shorebirds carrying seeds and migrating from the UK to Iceland, which also do not empty their guts beforehand (Lovas-Kiss et al., 2019). Forced activity in mallards (Anas platyrhynchos) had little effect on gut retention time of seeds, but increased the proportion of ingested seeds which survived gut passage (Kleyheeg et al., 2015). Furthermore, gut retention time is generally much longer for herbivores such as geese than for true frugivores (Yoshikawa et al., 2019). ...
Aim: How plants can disperse in response to global change is a critical question, yet major knowledge gaps persist about long-distance dispersal (LDD) mechanisms. We studied the potential a migratory waterfowl has for LDD of flowering plants via gut passage of seeds (endozoochory), comparing spring and autumn migration.
Location: United Kingdom and Iceland
Taxon: Pink-footed Goose (Anser brachyrhynchus, Baillon) and Angiosperma.
Methods: We studied endozoochory by Pink-footed geese migrating within and between the UK and Iceland by faecal sampling and GPS tracking. We collected 614 faecal samples from 14 areas in the UK and one in Iceland. Using GPS tracks to and from these areas, we estimated how far seeds can be dispersed by Pink-footed geese, and where to or from.
Results: We recorded 5507 intact seeds of 35 species (27 terrestrial) from 15 plant families, with lower seed abundance per dropping when birds were migrating northwards in the UK during spring than upon their arrival in autumn. Species richness of plant seeds was highest in Iceland and in autumn. Only four plant species dispersed had an “endozoochory syndrome”. GPS movements showed that seeds retained in guts for up to 24h can be readily dispersed in both directions between the UK and Iceland, with maximum distances exceeding 2000 km, as well as between UK localities separated by 100s of km. Movements northwards of ≤400 km were even recorded in autumn. While at stopover sites, daily movements between roost and feeding sites often exceed 20 km.
Main conclusions: Pink-footed geese are LDD vectors for plants previously assumed to lack an LDD mechanism. Spring migration is not the only period when geese move plants to cooler latitudes. The Pink-footed goose can allow terrestrial and aquatic plants to cross the ocean and to keep pace with climate change.
... Captivity can change seed survival and retention time due to the limited mobility of the birds compared with those active in the field. Kleyheeg, et al. [39] found that seed survival increased significantly with forced activity in ducks. LBBGs spend long periods of the day inactive, roosting in rice fields or neighbouring habitats [40], so our experiment may reflect field conditions quite well. ...
Recent field data suggest that migratory gulls disperse many rice field weeds by gut passage (endozoochory), most of which are dry fruited and widely assumed to have no long-distance dispersal mechanisms, except via human activity. We investigated this mechanism with a feeding experiment, in which seeds of five common rice field weeds (in order of increasing seed size: Juncus bufonius, Cyperus difformis, Polypogon monspeliensis, Amaranthus retroflexus, and the fleshy-fruited Solanum nigrum) were fed to seven individuals of lesser black-backed gulls Larus fuscus held in captivity. We quantified seed survival after collecting faeces at intervals for 33 h after ingestion, then extracting intact seeds and running germination tests, which were also conducted for control seeds. All five species showed high seed survival after gut passage, of >70%. Gut retention times averaged 2–4 h, but maxima exceeded 23 h for all species. Germinability after gut passage was 16–54%, and gut passage accelerated germination in J. bufonius and S. nigrum, but slowed it down in the other species. All species had lower germinability after gut passage compared to control seeds (likely due to stratification prior to the experiment), but the loss of germinability was higher in smaller seeds. There was no evidence that the different dispersal syndromes assigned to the five species (endozoochory, epizoochory or barochory) had any influence on our results. In contrast, mean gut retention time was strongly and positively related to seed size, likely because small seeds pass more quickly from the gizzard into the intestines. Non-classical endozoochory of dry-fruited seeds by waterbirds is a major but overlooked mechanism for potential long-distance dispersal, and more research into this process is likely essential for effective weed management.
... The intestinal-phase was standardized to 2 hours (Vispo and Karasov 1997). Combined total simulated retention times ranged from 2 to 8 hours -which covered a range of typical total digestion times in waterbird species and mallards in particular (van Leeuwen et al. 2012a, b, Kleyheeg et al. 2015, Lovas-Kiss et al. 2020a. ...
Waterbirds disperse plant species via ingestion and egestion of seeds (endozoochory). However, our understanding about the regulating effects of seed traits, underlying mechanisms and possible (co)evolutionary processes is limited by our traditional reliance on data from feeding experiments with living waterbirds. Here, we overcome these limitations by developing and applying a new bioassay that realistically simulates digestive processes for Anseriformes waterbirds. We test three hypotheses: 1) seed survival and germination are most affected by mechanical digestion in the waterbird gizzard; 2) seed size, hardness, imbibition and shape regulate seed survival; and 3) plants growing in aquatic habitats benefit most from endozoochory by waterbirds. Experiments with 28 200 seeds of 48 plant species demonstrated species‐specific seed survival that was entirely determined by digestion in the avian gizzard. Intestinal digestion did not affect seed survival but affected seed establishment (germinability and germination time) for 21% of the species. Large, hard seeds survived the simulations the best, in contrast to generally higher seed survival for smaller seeds during in vivo experiments. This mechanistically explains that small seeds escape digestive processes rather than being inherently more resistant (the ‘escape mechanism'), while large seeds are retained until fully digested or regurgitated (the ‘resistance and regurgitation mechanism'). Plants growing in wetter habitats had similar seed survival, but digestive processes stimulated their germinability and accelerated their germination more than for terrestrial plants. This indicates a relative advantage of endozoochory for plant species growing in wet habitats, possibly reflecting a co‐evolutionary response related to dormancy breaking by gut passage. Simulating seed gut passage using a bioassay allowed establishing mechanisms and identifying relevant seed traits involved in seed dispersal by waterbirds. This information enhances our understanding of how animal species shape plant species distributions, which is extremely relevant now that current anthropogenic pressures already severely impact plant dispersal capacities.
... Our dataset includes a mixture of data demonstrating seed ingestion from the upper and lower digestive tracts, as well as from the feces of individual birds. The presence of seeds in the upper digestive tract of waterfowl has been shown to be a good proxy for seed dispersal by endozoochory (Kleyheeg et al., 2015;Soons et al., 2016;Costea et al., 2019). Previous studies have used part of this same dataset regarding seven dabbling duck species, including a comparison of traits between European plants whose seeds were ingested, and plants whose seeds were not (Dessborn et al., 2011;Soons et al., 2016). ...
Endozoochory by waterfowl is important for a broad range of angiosperms, most of which lack a fleshy fruit. This dispersal function contributes to the formation and maintenance of plant communities and may allow range shifts for plant species under global change. However, our current understanding of what seed or plant traits are important for this dispersal mechanism, and how they relate to variation in waterbird traits, is extremely limited. We addressed this question using a unique dataset identifying the plant species whose seeds are ingested by 31 different waterfowl species in Europe. We used RLQ and fourth-corner analyses to explore relationships between (1) bird morphological and foraging strategy traits, and (2) plant traits related to seed morphology, environmental preferences, and growth form. We then used Generalized Additive Models to identify relationships between plant/seed traits and the number of waterfowl species that disperse them. Although many waterfowl feed intentionally on seeds, available seed trait data provided little explanation for patterns compared to plant traits such as Ellenberg indicators of habitat preference and life form. Geese were associated with terrestrial plants, ingesting seeds as they graze on land. Diving ducks were associated with strictly aquatic plants, ingesting seeds as they feed at greater depths. Dabbling ducks ingest seeds from plants with high light and temperature requirements, especially shoreline and ruderal species growing in or around the dynamic and shallow microhabitats favored by these birds. Overall, the number of waterfowl vector species (up to 13 per plant species) increases for plants with greater soil moisture requirements and salinity tolerance, reflecting the inclination of most waterfowl species to feed in coastal wetlands. Our findings underline the importance of waterfowl dispersal for plants that are not strictly aquatic, as well as for plants associated with high salinities. Furthermore, our results reveal a soil moisture gradient that drives seed-bird interactions, in line with differences between waterfowl groups in their microhabitat preferences along the land-water continuum. This study provides an important advance in our understanding of the interactions that define plant dispersal in wetlands and their surroundings, and of what plants might be affected by ongoing changes in the distributions of waterfowl species.
... Consequently, seed passage time through the gut is reduced and dispersal distance can be shortened. Gut passage time of seeds in mallard Anas platyrhynchos decreased with moderate activities (Kleyheeg et al. 2015). On the contrary, some frugivores prioritize movement and allocate energy to the locomotory system. ...
Frugivore movement plays a critical role in animal‐mediated seed dispersal. Frugivores utilize resources that are heterogeneously distributed in the landscape and execute complex movement to exploit these resources. Employing the ‘movement ecology paradigm', we discuss the drivers behind frugivore movement, categorize movement into canonical activity modes and explore the potential impacts on seed dispersal effectiveness via removal and deposition of seeds. Among the movement drivers, frugivore physiology determines the goals, motion capacities determine how frugivores move across their heterogenous landscape, navigation capabilities determine how frugivores acquire and process both internal and external information that set them in motion, and biotic interactions further modulate frugivore movement. The movement process that emerges from the interactions of these drivers can be classified into different canonical activity modes that determine levels of seed removal and generate clumped, even or other spatial distributions of seed deposition. We provide a novel framework to integrate movement drivers, frugivore activities and seed dispersal services. We provide future directions utilizing advances in animal movement research to better understand the role of animal movement in the effectiveness of seed dispersal, highlighting potential impacts of increased anthropogenic activities. To advance a mechanistic understanding of animal‐mediated seed dispersal, we encourage increased collaboration between animal movement and plant ecologists.
... We do not have an obvious explanation to this result although we can speculate that differences between Rhizopogon and Suillus dispersal could be related to spore retention and survivorship through time and digestion, as occur with fruits and seeds (e.g. Janzen 1984; Kleyheeg et al. 2015). We cannot discard differences in fruit bodies abundance that makes Suillus more consumed or even in spore density that could enhance the probabilities of being dispersed farther away. ...
We aimed to evaluate if exotic ectomycorrhizal fungi from exotic pine plantations disperse through non-native, but also native, mammals in a mountain ecosystem devoid of native ECM plants. Among four non-native and three native mammal species, feces of non-native wild boar (Sus scrofa) and brown hare (Lepus europaeus), and native pampa fox (Lycalopex gymnocercus) were selected to inoculate seedlings of Pinus elliottii. These feces came from two transects in an elevation gradient (1350–2250 m asl) and different distances from a pine plantation (100–6000 m). We show that feces of wild boar, brown hare (non-native), and pampa fox (native) were effective as inoculum for establishing ectomycorrhizal pine seedlings. Through molecular analyses, we determined that two species are mostly consumed and successfully form ectomycorrhizas with pine roots: Suillus granulatus and Rhizopogon pseudoroseolus. We provide novel evidence for the long-distance dispersal of exotic ectomycorrhizal fungi by non-native and native animal vectors.
... Many traits have been proposed to impact TT and MRT in endothermic animals including body mass (Demment & Van Soest, 1985;Warner, 1981), dry matter intake Müller et al., 2013), diet (De Cuyper et al., 2020;Murray et al., 1994), gut physiology (Robbins, 1993;Stevens & Hume, 2004), rumination (Przybyło et al., 2019;Steuer et al., 2011), volancy (Frei et al., 2015;Hilton et al., 1998), foraging strata (Jackson, 1992) and physical activity level (Beirne et al., 2019;Kleyheeg et al., 2015). Table S1 details an extensive list of traits that have been shown to impact TT and MRT. ...
Animals are important vectors for transporting seeds, nutrients and microbes across landscapes. However, models that quantify the magnitude of these ecosystem services across a broad range of taxa often rely on generalised mass‐based scaling parameters for gut passage time. This relationship is weak and fundamentally breaks down when considering individual species, indicating that current models may incorrectly attribute or estimate the magnitude of dispersal.
We collated a large dataset of gut passage time for endothermic animals measured using undigested markers (n = 391 species). For each species, we compiled trait data, including body mass, morphology, gut physiology, diet and phylogeny. We then compared the ability of five statistical models (constant, generalised least squares, phylogenetic generalised least squares, general linear model and random forest) to estimate the time of first marker appearance (transit time; TT) and mean marker retention time (MRT) for particle and solute markers in mammals and birds separately.
For mammals, we found that the inclusion of additional traits appreciably reduced the median root‐mean squared error across all markers in a leave‐one‐out cross validation. For birds, however, additional traits did not significantly improve our ability to predict gut passage time across markers. This may have occurred due to the smaller number of bird species included in our analysis or the absence of important explanatory factors such as differences in gastrointestinal morphology.
Using the MRTparticle random forest model from this study, we updated two trait‐based dispersal models for seed and nutrient movement by mammals. The magnitude of dispersal in our updated predictions ranged from 66% to 176% of the original model formulation for different scenarios, highlighting the importance of gut passage time for dispersal models. Furthermore, the contribution by individual or groups of species was found sizeably altered in our updated models.
Future modelling studies of dispersal by mammals, for which empirical estimates of gut passage time are absent, will benefit from predicting gut passage time using statistical models that incorporate traits including animal morphology, diet and gut physiology.
A free Plain Language Summary can be found within the Supporting Information of this article.
... Thus, the condition of deposited seeds can be influenced by the link between behavioural types, mobility and gut passage time (which is typically shorter in highly active individuals). Sometimes, increased physical activity contributes to higher viability of seeds after gut passage (Kleyheeg, Van Leeuwen, Morison, Nolet, & Soons, 2015). However, the most common relationship between gut passage time and seed viability is likely to be unimodal because too short gut passage might not break seed dormancy, but too long might kill the seed (Jaganathan et al., 2016;Traveset et al., 2007; Perhaps less intuitively, seed condition might also be affected by the dominance rank of foragers. ...
Consistent individual tendencies in behaviour, or behavioural types, are likely to impact the dynamics and outcomes of animal‐mediated seed dispersal. We review the extant literature on this issue and outline a conceptual overview to guide this emerging field. We provide an overview of possible ways in which behavioural types can affect animal‐mediated seed dispersal. We summarize theoretical mechanisms linking behavioural types with seed dispersal outcomes and review how behavioural types might affect each stage of seed dispersal, beginning with fruit encounter and harvest, and ending with events that take place after seed deposition.
Since behavioural types involve correlations among different behaviours (i.e. behavioural syndromes), they can generate unexpected associations between different decisions that are involved in seed dispersal, with conflicting (or reinforcing) effects on different stages of seed dispersal. Thus, we draw particular attention to trade‐offs faced by seeds dispersed by individuals with different behavioural tendencies. We also note that since seed dispersal is a multiplicative process with different stages, disperser behavioural types that provide moderately efficient dispersal at each stage will be better for plants than behavioural types that are very efficient at some steps, but inefficient on others. Finally, we provide testable predictions on the links between behavioural types and characteristics of seed dispersal, including, for example, influences on the probability of seed harvest, dispersal distance, deposition sites and condition of dispersed seeds.
We argue that investigating the links between behavioural types and animal‐mediated seed dispersal will provide a better mechanistic understanding of seed dispersal and plant regeneration.
A free plain language summary can be found within the Supporting Information of this article.
... The dynamics in river habitats has also been examined in the annual Erysimum cheiranthoides growing on stony riverbanks along the river Meuse (Honnay et al., 2009). The species behaves as a very dynamic metapopulation and, similarly to our study, the metapopulation showed be transported by ducks on feathers and crusts of mud as well as in their guts over long distances (several hundreds of kilometers), whereby small seeds have the highest potential to be dispersed (Bílý, Mourková, & Bergmann, 2008;Figuerola & Green, 2002;Hohensee & Frey, 2001;Kleyheeg, Leeuwen, Morison, Nolet, & Soons, 2015;Soons et al., 2008;Viana, Santamaría, & Figuerola, 2016). Cyperus fuscus produces an enormous amount of small nutlets (Bryson & Carter, 2010), so that ducks should be ideal dispersers of this species. ...
Abstract Many ephemeral mudflat species, which rely on a soil seed bank to build up the next generation, are endangered in their natural habitat due to the widespread regulation of rivers. The aim of the present study was to elucidate the role of the soil seed bank and dispersal for the maintenance of genetic diversity in populations of near‐natural river habitats and anthropogenic habitats created by traditional fish farming practices using Cyperus fuscus as a model. Using microsatellite markers, we found no difference in genetic diversity levels between soil seed bank and above‐ground population and only moderate differentiation between the two fractions. One possible interpretation is the difference in short‐term selection during germination under specific conditions (glasshouse versus field) resulting in an ecological filtering of genotypes out of the reservoir in the soil. River populations harbored significantly more genetic diversity than populations from the anthropogenic pond types. We suggest that altered levels and patterns of dispersal together with stronger selection pressures and historical bottlenecks in anthropogenic habitats are responsible for the observed reduction in genetic diversity. Dispersal is also supposed to largely prohibit genetic structure across Europe, although there is a gradient in private allelic richness from southern Europe (high values) to northern, especially north‐western, Europe (low values), which probably relates to postglacial expansion out of southern and/or eastern refugia.
... passive browsing without seed digestion and/or focused seed predation and digestion) is likely. Indeed, a proportion of seeds can survive unharmed because complete digestion does not work continuously as a by-product of gut morphology and physiology, as well as due to other factors such as activity, stress and food features ( Kleyheeg et al. 2015). The observed proportion of viable seeds of the two most abundant herbs retrieved, and the lack of viability in the remaining species can also be influenced by gut transit conditions, reduced sample size and methodological limitations for assessing seed viability (Cope- land & McDonald 1995). ...
Establishing whether herb seed endozoochory is accidental or has evolved independently or in combination with other dispersal mechanisms may be valuable in the study of plant–animal interactions, but it remains unexplored for birds. We tested whether an Australian cockatoo, the galah (Eolophus roseicapilla), swallows entire seeds when feeding on other tissues without subsequent seed digestion, thus enhancing seed dispersal (the ‘foliage is the fruit’ hypothesis). Our preliminary sampling provides strong evidence supporting that this seed predator also acts as a legitimate endozoochorous disperser. A large proportion of droppings contained numerous seeds of six herb species of three plant families, surviving gut passage to be dispersed as viable propagules. The wide range in the number of seeds found in combinations with up to five species in particular droppings suggests both simultaneous and sequential passive ingestion without seed digestion and/or focused seed predation and digestion. As expected for inadvertent ingestion and inefficient digestion, our findings suggest that seed number and richness of dispersed plants are associated traits in this particular mutualistic interaction. This relationship can have important implications in community‐wide processes, favouring herbs whose seeds are disseminated in a viable state over those predated or negatively affected by gut transit.
... For example, gut passage time of seeds increased by up to 80% with physical activity in mallard ducks (Kleyheeg, van Leeuwen, Morison, Nolet, & Soons, 2015). ...
Seed dispersal distance (SDD) critically influences the survival of seedlings, spatial patterns of genetic diversity within plant populations, and gene flow among plant populations. In animal‐dispersed species, foraging behavior and movement patterns determine SDD. Direct observations of seed dispersal events by animals in natural plant populations are mostly constrained by the high mobility and low visibility of seed dispersers. Therefore, diverse alternative methods are used to estimate seed dispersal distance, but direct comparisons of these approaches within the same seed dispersal system are mostly missing.
We investigated two plant species with different life history traits, Leonia cymosa and Parkia panurensis, exclusively dispersed by two tamarin species, Saguinus mystax and Leontocebus nigrifrons. We compared SDD estimates obtained from direct observations, genetic identification of mother plants from seed coats, parentage analysis of seedlings/saplings, and phenomenological and mechanistic modeling approaches.
SDD derived from the different methods ranged between 158 and 201 m for P. panurensis and between 178 and 318 m for L. cymosa. In P. panurensis, the modeling approaches resulted in moderately higher estimates than observations and genotyping of seed coats. In L. cymosa, parentage analysis resulted in a lower estimate than all other methods. Overall, SDD estimates for P. panurensis (179 ± 16 m; mean ± SD) were significantly lower than for L. cymosa (266 ± 59 m; mean ± SD).
Differences among methods were related to processes of the seed dispersal loop integrated by the respective methods (e.g., seed deposition or seedling distribution). We discuss the merits and limitations of each method and highlight the aspects to be considered when comparing SDD derived from different methodologies. Differences among plant species were related to differences in reproductive traits influencing gut passage time and feeding behavior, highlighting the importance of plant traits on animal‐mediated seed dispersal distance.
... The second hypothesis is that the disjunct distribution pattern is the result of recent long distance seed dispersal between Taiwan and Kyushu. Typically, it is believed that long distance seed dispersal in plants is accomplished by birds or wind (birds; Kleyheeg et al., 2015, Viana et al., 2016Nathan et al., 2002, Tackenberg 2003. It is thought that the seeds of Pedicularis are mainly dispersed close to their origin by gravity (Juan et al. 2000, Liu et al. 2013) because they are relatively large and lack appendages for wind dispersal. ...
To classify the species of Pedicularis ser. Verticillatae Maxim. (Orobanchaceae) in Taiwan, phylogeographic analyses using internal transcribed spacer (ITS) regions of nuclear ribosomal DNA (nrDNA) and trnK (partial) regions of chloroplast DNA (cpDNA) were performed. It was determined that the Taiwanese populations formed a single strongly-supported clade with P. refracta (Maxim.) Maxim., an endemic of Kyushu, Japan. Little genetic variation between the Taiwanese populations and P. refracta was detected. Morphological analyses showed that the Taiwanese populations and P. refracta differed in three key characteristics: corolla length, distance between the rachis and the sinuses of the pinnae, and plant height. It was concluded that the Taiwanese populations should be treated as a variety of P. refracta (Kyushu populations); P. refracta var. transmorrisonensis (Hayata) Hurus. (lectotypified here). In addition, the phylogeographic analyses suggested that the disjunct distribution pattern between Taiwan and Kyushu was due to Quaternary vicariance events rather than to long distance dispersal of seeds.
... Moreover, causes of within-species or within-individual variations in SRT include both animal-side and plant-side factors, which could be incorporated into the future development of the modelling. The animal-side factors include sex, age, food type (Charalambidou et al. 2005), amount of food ingested and locomotive status (Kleyheeg et al. 2015). The main plant-side factors are seed size and shape and fleshy fruits' pulp content, such as secondary metabolites (Baldwin and Whitehead 2015). ...
Seed retention time (SRT), the time interval between seed ingestion and defaecation, is a critical parameter that determines the spatial pattern of seed dispersal created by an animal, and is therefore, an essential component of trait‐based modelling of seed dispersal functions. However, no simple predictive model of SRT for any given animal exists.
We explored the linkage between animal traits and SRT. We collected previously published data on mean SRT for 112 species of birds, mammals, reptiles and fishes and investigated the general allometric scaling of mean SRT with body mass for each taxon. Moreover, we analysed the effects of food habit and digestive strategy on mean SRT for birds and mammals.
In general, mean SRT increased with body mass in all four taxa, whereas the pattern of allometric scaling varied greatly among the taxa. Birds had a smaller intercept and larger slope than those of mammals, whereas reptiles had a much larger intercept and smaller slope than those of either birds or mammals. For birds, food habit was also detected as an important factor affecting SRT. We applied the allometric scaling that was obtained for birds to estimate mean SRT of extinct Mesozoic dinosaurs (Theropoda) – few of which are assumed to have acted as seed dispersers. SRT for large carnivorous theropods was estimated to be 4–5 days, when considering only body mass.
The present study provides allometric scaling parameters of mean SRT for a variety of seed‐dispersing animals, and highlights large variations in scaling among taxa. The allometric scaling obtained could be a critical component of further trait‐based modelling of seed dispersal functions. Further, the potential and limitations of the scaling of animal SRT with body mass and a future pathway to the development of trait‐based modelling are discussed.
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... Furthermore, it is very possible that the geese can disperse these same plant species over hundreds of kilometres during their long-distance migrations in a similar manner to migratory ducks, since the longest seed retention times in the guts of geese exceed the time required for migration (Viana et al. 2013;García-Álvarez et al. 2015). Geese have not been shown to empty their digestive tract before migrations, and flight activity is likely to increase seed survival (Kleyheeg et al. 2015). A role for geese as long-distance vectors in Arctic environments is strongly consistent with genetic and floristic analyses (Alsos et al. 2015). ...
Despite the abundance of migratory geese as herbivores in the Arctic, and ongoing changes in their populations and distributions, little is known about their role in seed dispersal. Climate change requires Arctic plants to adjust their distributions, and avian vectors may have an important role to play. We present the first study of endozoochory (internal transport) of Arctic plants by Canada geese. In central west Greenland, we collected 50 faecal samples, from which we extracted 2943 intact seeds from six species and four families, all but one of which (a non-native species) are extremely common and widespread in this part of Greenland. The majority (95%) of seeds were from Empetrum nigrum, but Carex nardina (3%) and Vaccinium uliginosum (2%) were also abundant. One seed of the non-native Persicaria lapathifolia was recorded. These results suggest migratory geese are likely to be vital vectors of Arctic plants. Although the sample size was small, there were indications that non-breeding geese may disperse more seeds than breeding geese, which stay closer to lakes to reduce the risk of predation, rarely accessing dwarf-scrub heath where non-breeders ingested seeds. Future research should address such possible links between reproductive status and seed dispersal in waterbirds.
... Proctor (1968) argued longer retention times occurred in caged birds and suggested that endozoochory remains possible in LDD. Proctor's long retention values of up to 340 hours were outliers (Appendix S3), were only associated with gizzard retention (creating uncertainty of their viability; Brochet et al., 2009 ), and the experiment was conducted on caged birds, which might process seeds diff erently than migrating birds ( Viana et al., 2013 ;Kleyheeg et al., 2015 ). However, this and our results suggest that endozoochory is possible in LDD. ...
Premise of the study:
A repeated pattern of American amphitropical disjunct species or sister species distributed on either side of the equator has long-fascinated botanists, but the modes of these disjunctions remain untested. We evaluated diaspore morphology to generate hypotheses on probable dispersal mechanisms.
Methods:
The sizes and structures of diaspores, habit, habitat, distribution, and dispersal units were collected for 108 species from literature searches and herbarium specimens. Variation was evaluated with summary statistics, χ(2) tests with Monte Carlo simulations, ANOVAs, and the nonparametric Mann-Whitney test.
Key results:
Seeds were the dispersing diaspore in 38.0% of the species, 45.4 were dispersed as fruits, and the remaining were dispersed as infructescences or spores. Diaspores were epizoochorous (52.8%), anemochorous (20.4%), achorous (15.7%), endozoochorous (8.3%), and hydrochorous (2.8%). Epizoochory was significantly greater than expected. Zoochory occurred more frequently than expected when considering achorous diaspores as animal-dispersed. Most species were associated with wetland, woodland, and grassland habitats. An ANOVA revealed that diaspores associated with hydrochory were larger and anemochory was smaller; all other syndromes were not significantly different.
Conclusions:
Botanists have long-held the assumption that bird migrations are responsible for amphitropical disjunctions. Our results support this hypothesis, with the majority of these events occurring by external attachment of small fruits. However, our results also indicate that anemochory might play a greater role in producing amphitropical distributions than previously thought and at a greater rate than endozoochory or hydrochory.
... Fish are known to ingest and disperse seeds (Boedeltje et al. 2015;van Leeuwen et al. 2012), but the velocity of dispersal is limited in the same way as dispersal by water: only sites connected by surface water can be connected by this seed dispersal mechanism. Waterfowl therefore play the more important role: they are numerous, seasonally granivorous, while seeds survive gut passage in relatively great numbers, and often show daily migrations, thereby crossing hydrological or other landscape barriers (Kleyheeg et al. 2015(Kleyheeg et al. , 2017b. Among the waterfowl frequenting the lakes, ponds and canals in the peat meadow areas there are large numbers of dabbling ducks, which have been shown to disperse seeds of a wide range of wetland and terrestrial plant species (Soons et al. 2016). ...
Restoration and conservation of species-rich nature reserves requires inclusion of landscape-scale connections and transport processes such as hydrologic flows and species dispersal. These are important because they provide suitable habitat conditions and an adequate species pool. This study aimed at identifying the key hydrologic flows and plant dispersal processes affecting a landscape with species-rich fen reserves where restoration measures are carried out to set back succession. It also intended to use this information for delineating the area relevant for conservation planning on an Operational Landscape Unit map. The study was carried out for complexes of fen ponds in former turbaries in the Vechtplassen area, The Netherlands. A number of recent insights on plant dispersal were integrated with knowledge on hydrologic flows in the present approach. The results showed that groundwater discharge to ensure mesotrophic, base-rich conditions, should be enhanced by restoring the groundwater recharge areas NE of the reserves. A nearby lake with suitable water chemistry was also identified as a key source of surface water to feed the fens in dry periods. Water dispersal was identified as important within the fen reserves, whereas dispersal by daily migrating dabbling ducks, typically occurring over 2–3 km, was the most important route connecting the reserves with the surrounding landscape. The delineation of the Operational Landscape Unit for this region provides a basis for conservation and restoration that take fundamental landscape connections and transport processes into account. This unique approach simultaneously considers hydrological transport processes as well as species dispersal in the larger landscape beyond the reserves themselves and therefore leads to greater success of restoration and conservation.
... They are opportunistic habitat generalists, frequenting all wetland types, and often living close to humans in agricultural and urban areas [11,13]. As such, they play a major role in wetland and terrestrial ecology, particularly as dispersal vectors of a wide variety of organisms including invertebrates [14,15], plants [10,[16][17][18][19], and viruses, such as AIV [8,20]. However, detailed studies of mallard movement patterns and the underlying mechanisms are scarce, hampering the assessment of the spatial scale of their contribution to ecological processes. ...
Background
Movement behaviour is fundamental to the ecology of animals and their interactions with other organisms, and as such contributes to ecosystem dynamics. Waterfowl are key players in ecological processes in wetlands and surrounding habitats through predator-prey interactions and their transportation of nutrients and other organisms. Understanding the drivers of their movement behaviour is crucial to predict how environmental changes affect their role in ecosystem functioning. Mallards (Anas platyrhynchos) are the most abundant duck species worldwide and important dispersers of aquatic invertebrates, plants and pathogens like avian influenza viruses. By GPS tracking of 97 mallards in four landscape types along a gradient of wetland availability, we identified patterns in their daily movement behaviour and quantified potential effects of weather conditions and water availability on the spatial scale of their movements. ResultsWe demonstrate that mallard movement patterns were highly predictable, with regular commuting flights at dusk and dawn between a fixed day roost and one or several fixed nocturnal foraging sites, linked strongly to surface water. Wind and precipitation hardly affected movement, but flight distances and home range sizes increased when temperatures dropped towards zero. Flight distances and home range sizes increased exponentially with decreasing availability of freshwater habitat. Total shoreline length and the number of water bodies in the landscape surrounding the roost were the best predictors of the spatial scale of daily mallard movements. Conclusions
Our results show how mallards may flexibly adjust the spatial scale of their movements to wetland availability in the landscape. This implies that mallards moving between discrete habitat patches continue to preserve biotic connectivity in increasingly fragmented landscapes. The high predictability of mallard movement behaviour in relation to landscape features makes them reliable dispersal vectors for organisms to adapt to, and allows prediction of their ecological role in other landscapes.
... Wild ducks tend to have larger gizzards and intestines than do captive ones (Charalambidou and Santamaría 2002), such that captive studies may tend to overestimate seed survival while perhaps underestimating retention times. On the other hand, the low activity levels of captive birds compared to those of wild ones, which spend much time swimming or flying, may lead to a major underestimation of the proportion of seeds that survive gut passage, as well as a slight overestimation of retention times (Kleyheeg et al. 2015). Recent studies addressed the effects of passage through the waterbird gut on germinability (the probability of germination) and germination rate (the time taken to germinate) of seeds. ...
Ducks, shorebirds, rails, gulls and other waterbirds act as vectors of seeds, spores and other plant diaspores carried internally in their guts, externally on their feathers, feet or bills, or used as nesting material. Darwin was the first to understand the significance of dispersal by migratory waterbirds in plant evolution, biogeography and ecology. Countless aquatic and terrestrial plants are dependent on
dispersal by waterbirds for long-distance dispersal, and this has probably been the case since the Cretaceous. However, plant ecologists and waterfowl biologists alike have been slow to recognize the importance of this dispersal mode as an ecosystem service. Seed dispersal by waterbirds plays a vital
role in plant population dynamics, population genetics and changes in species distributions in response to habitat change and climate warming. On the other hand, waterbirds also spread alien species, and their role as vectors should be taken into account when considering how to prevent and manage biological invasions.
... It is also worth noting that propagule retention and flying activity might influence each other, but we still lack a methodology to measure retention time while birds are flying. A study on the effect of physical activity (swimming) on seed retention time using mallards showed enhanced propagule survival but slightly shorter retention times at higher physical activity [89]. By contrast, traveling with the extra weight of a large (ingested) propagule load might affect flying performance [90]. ...
Propagule dispersal beyond local scales has been considered rare and unpredictable. However, for many plants, invertebrates, and microbes dispersed by birds, long-distance dispersal (LDD) might be regularly achieved when mediated by migratory movements. Because LDD operates over spatial extents spanning hundreds to thousands of kilometers, it can promote rapid range shifts and determine species distributions. We review evidence supporting this widespread LDD service and propose a conceptual framework for estimating LDD by migratory birds. Although further research and validation efforts are still needed, we show that current knowledge can be used to make more realistic estimations of LDD mediated by regular bird migrations, thus refining current predictions of its ecological and evolutionary consequences.
... This is partly in line with observations of Egawa and Tsuyuzaki (2013) that observed smallest seeds to move most frequently in sown plots compared with bigger seeds, which they contributed to snowmelt. Seed volume was the strongest predictor, which therefore adds to an increasing body of work showing that seed volume is a better proxy for dispersal via various dispersal vectors (e.g. by wind and ducks) than seed mass per se (Liu et al., 2012;Egawa and Tsuyuzaki, 2013;Kleyheeg et al., 2015). This study did not incorporate extremely complex seed shapes such as with hooks or plumes, which could decrease seed dispersal distances by rain compared with seeds with similar size and weight but without those appendages. ...
Water flows affect dispersal of propagules of many plant species, and rivers and streams are therefore very important dispersal vectors. However, small water flows such as trough rain and snow melt are much more common, but their effects on dispersal are barely studied. The importance of this form of dispersal deserves attention, especially when considering that climate change is predicted to change the amounts of rain and snow worldwide. Dispersal through melting snow and rain was addressed experimentally, using artificial soils mounted on slopes with different angles and subjected to a melting snow pack or an equivalent amount of dripping water. Seeds on the soil moved on average 3.02 cm (±1.81 S.E.) in rain treatments and 0.23 cm (±0.3 S.E.) in snow melt treatments. Tracking plastic granules in field conditions further showed that snow melt exhibited minimal dispersal capacity. Dispersal distances by rain were enhanced by increasing slope angles and with decreasing seed volume. Given that many species in cold environments have small seeds, dispersal by rain could provide an important (secondary) dispersal mechanism in these habitats.
... This, in combination with our finding that the frequency distribution of the percentage biomass of earthworms calculated for the entire set of pellets reached higher values than the data averaged per individual village, implies that assessments of diet based on pellet analysis should be performed for large samples of pellets representing just a few meals. Moreover, the nearly 240-fold difference in the weight of the examined pellets (in the terms of their extreme weight; Table S1) suggests the existence of potential relationships that we did not explore in our study: the consequence of ingesting different weights of food (reviewed in Trierweiler & Hegemann 2011) and the physiological and digestive processing resulting from the activity of birds (e.g. a restless phase at night when digestive efficiency is higher; Kleyheeg et al. 2015). The numbers of some larger prey items (e.g. ...
Earthworms (Oligochaeta, Lumbricidae) form a significant component of the food web and form the staple diet of many higher trophic level predators, such as invertebrate-feeding birds and mammals. Their almost complete digestion in the predator's gut hampers their detection or quantification in faeces or pellets except through labour-intensive microscopic examination. As a result, the evaluation of earthworms as a component of diet has been neglected in most studies based on pellet analysis. We assess whether the earthworm component of the diet of White Storks Ciconia ciconia be estimated reliably by measuring soil mass in pellets, and whether the fact that White Storks also consume European Moles Talpa europaea (themselves consumers of earthworms) affects this relationship. We found a significantly higher density of earthworm chaetae, but less soil material, in pellets containing the remains of Moles. This may indicate the secondary origin of some chaetae from the intestines of the ingested Moles. There was a strong relationship and close fit between the number of earthworm chaetae and the mass of soil (material <0.2 mm) retrieved from all the pellets analysed. Approximating the number of chaetae based on a soil mass of 192 mg per 1000 chaetae yielded results differing by only 4-5% from numbers of chaetae counted directly. This validates the proposed method of indirectly calculating the number of earthworms consumed from the ingested soil mass, which simplifies and shortens the time-consuming direct counting of chaetae and could contribute to a more detailed description and analysis of diets in wild birds. Such assessments are important in order to improve the detection of changes induced by the progressive simplification and loss of primary food web resources (such as earthworms) within agro-ecosystems as a consequence of both the rapid intensification of agricultural production and climate change. This article is protected by copyright. All rights reserved.
... There was no difference between aquatic and riparian species in this respect, except that anemochory was not suggested as a vector for aquatic species. Generally, these observations support existing evidence that waterfowl play an important role in the dispersal of freshwater wetland plants (Green, Figuerola & S anchez, 2002;Kleyheeg, 2015;Kleyheeg et al., 2015), even in flowing waters, with other vertebrates (including humans) being of secondary importance. In general, wind dispersal appears to play a more pronounced role in more terrestrial wetland (riparian) plant species, as demonstrated earlier (Soons, 2006). ...
Dispersal and colonisation are key processes determining species survival, and their importance is increasing as a consequence of ongoing habitat fragmentation, land-use change and climate change. Identification of long-distance dispersal events, including upstream dispersal, and of the dispersal mechanisms and resulting spatial dispersal patterns involved provides much-needed information for conservation in an era of rapid environmental change.
However, quantifying contemporary dispersal among populations is far from straightforward. We used the relatively well-defined, typically linear, spatial structure of streams, rivers and their associated riparian and aquatic plant populations to illustrate this. We performed a literature review on studies where dispersal and its directionality (upstream versus downstream) were explicitly quantified.
Upstream dispersal was detected in the majority (75%) of examined stream and riparian plant species and mediated mainly by waterfowl, but also by other animals and wind. However, upstream movements are generally less frequent than downstream. Upstream dispersal can occur in excess of tens and sometimes even hundreds of kilometres.
Most of the reviewed studies suffer from important methodological limitations that generate difficulties in detecting uncommon dispersal events. Major limitations include use of molecular ecological analyses based on unrealistic assumptions, and the inability to separate seed from pollen flow. On the basis of these findings, we outline a flexible research design using DNA-based assignment methods that allows quantification of contemporary dispersal in future studies. We suggest four key improvements: (i) assignment of propagules and/or seedlings; (ii) use of spatial models to inform sampling design; (iii) reducing the influence of unsampled populations and (iv) combined use of nuclear and uniparentally inherited DNA markers to separate gene flow (including pollen and sperm) in general from propagule-mediated dispersal. In combination with direct measurements of seed dispersal these facilitate empirical quantification of dispersal and the detection of uncommon dispersal events, allowing more realistic assessment of spatial population dynamics, relevant for sedentary and relatively immobile organisms
... A quarter of seeds ingested by ducks were retrieved intact, and of these more than a quarter retained their germinability. Note that we used resting animals, and due to the reduced efficiency of digestion in active birds, significantly more seeds can retain their germinability after passing through the digestive tract when the birds are active [24]. Some of the seeds were retained in the digestive system for more than 21 hours. ...
It was proposed previously that passive dispersal by migratory aquatic birds explain the widespread distribution of many wetland organisms. Several experimental studies have shown that many widespread wetland plant species can be readily dispersed within the guts of Anatidae. However, it is unclear whether plants with a more restricted distribution are able to disperse via waterbirds. This paper addresses the dispersal ability and germination ecology of the little-known Hungarian milkvetch Astragalus contortuplicatus, which occurs on banks of continental rivers and has a limited and unpredictable distribution. To test whether limited capacity for endozoochory by waterfowl could explain the sporadic appearance of this species, we force-fed ten captive mallards (Anas platyrhynchos) with 100 milkvetch seeds each. Droppings were collected for up to 45 h after feeding. Intact and viable seeds were found in the droppings of each mallard, and altogether 24.7% of seeds fed were recovered intact. The proportion of retrieved seeds that germinated (27.0%) was significantly higher than that of untreated control seeds (0.5%), but significantly lower than that of mechanically scarified seeds (96.0%). Retrieved seeds that germinated developed into healthy mature plants. Given the average flight velocity of mallards, seeds of A. contortuplicatus may travel up to 1600 km inside the digestive tract of migrating individuals. Our results suggest that avian vectors may be more important for the dispersal of rare higher plants (especially those with a hard seed-coat) than hitherto considered. Moreover, they suggest that rarity does not necessarily indicate limited dispersal ability, and may instead be explained by specific habitat requirements.
The paradoxical presence of toxic chemical compounds in ripe fruits represents a balance between plant enemies and allies: chemical traits can defend seeds against antagonistic herbivores, seed predators, or fungal pathogens, but also can impose costs by repelling mutualistic seed dispersers, although the costs are often difficult to quantify. Seeds gain fitness benefits from traveling far from the parent plant, as they can escape from parental competition and elude specialized herbivores as well as pathogens that accumulate on adult plants. However, seeds are difficult to follow from their parent plant to their final destination. Thus, little is known about the factors that determine seed dispersal distance. We investigated this potential cost of fruit secondary compounds, reduced seed dispersal distance, by combining two data sets from previous work on a Neotropical bat‐plant dispersal system (bats in the genus Carollia and plants in the genus Piper). We used data from captive behavioral experiments, which show how amides in ripe fruits of Piper decrease the retention time of seeds and alter food choices. With new analyses, we show that these defensive secondary compounds also delay the time of fruit removal. Next, with a behaviorally annotated bat telemetry data set, we quantified post‐feeding movements (i.e., seed dispersal distances). Using generalized additive mixed models we found that seed dispersal distances varied nonlinearly with gut retention times as well as with the time of fruit removal. By interrogating the model predictions, we identified two novel mechanisms by which fruit secondary compounds can impose costs in terms of decreased seed dispersal distances: (1) small‐scale reductions in gut retention time and (2) causing fruits to forgo advantageous bat activity peaks that confer high seed dispersal distances.
Shorebirds (Charadriiformes) undergo rapid migrations with potential for long‐distance dispersal (LDD) of plants. We studied the frequency of endozoochory by shorebirds in different parts of Europe covering a broad latitudinal range and different seasons. We assessed whether plants dispersed conformed to morphological dispersal syndromes. A total of 409 excreta samples (271 faeces and 138 pellets) were collected from redshank (Tringa totanus), black‐winged stilt (Himantopus himantopus), pied avocet (Recurvirostra avosetta), northern lapwing (Vanellus vanellus), Eurasian curlew (Numenius arquata) and black‐tailed godwit (Limosa limosa) in south‐west Spain, north‐west England, southern Ireland and Iceland in 2005 and 2016, and intact seeds were extracted and identified. Godwits were sampled just before or after migratory movements between England and Iceland. The germinability of seeds was tested. Intact diaspores were recovered from all bird species and study areas, and were present in 13% of samples overall. Thirteen plant families were represented, including Charophyceae and 26 angiosperm taxa. Only four species had an "endozoochory syndrome". Four alien species were recorded. Ellenberg values classified three species as aquatic and 20 as terrestrial. Overall, 89% of seeds were from terrestrial plants, and 11% from aquatic plants. Average seed length was higher in redshank pellets than in their faeces. Six species were germinated, none of which had an endozoochory syndrome. Seeds were recorded during spring and autumn migration. Plant species recorded have broad latitudinal ranges consistent with LDD via shorebirds. Crucially, morphological syndromes do not adequately predict LDD potential, and more empirical work is required to identify which plants are dispersed by shorebirds. Incorporating endozoochory by shorebirds and other migratory waterbirds into plant distribution models would allow us to better understand the natural processes that facilitated colonization of oceanic islands, or to improve predictions of how plants will respond to climate change, or how alien species spread. This article is protected by copyright. All rights reserved.
Dispersal of plant seeds by ducks and other waterbirds is of great importance to the ecology of freshwater habitats. To unravel the mechanisms of waterbird‐mediated seed dispersal, numerous laboratory experiments have been conducted, but effects of seed and waterbird traits on dispersal potential have rarely been investigated under field conditions.
Through analysis of the digestive tracts of 100 wild mallards ( Anas platyrhynchos ) across a winter season in the Netherlands, we assessed (i) the inter‐individual and seasonal variability of seeds in the digestive tract, (ii) the variability of digestive tract organ size and gizzard grit mass, and (iii) the potential effects of seed species traits and gut traits on the survival potential of ingested seeds.
We found 4548 ingested seeds of at least 66 plant species from a wide range of habitats, most of which were retained in the gizzard. Nineteen species had not previously been reported from mallard diets. Individual tracts contained anywhere between 0 and 1048 seeds, of up to 14 species (median of three species). Diet composition and digestive tract size varied substantially between individuals and over the course of the winter season. As predicted from controlled feeding studies, we found that also in wild mallards, size‐dependent gut passage survival favours the dispersal of small‐seeded species. Despite the large variation in gizzard and small intestine size in this study, their effect on the dispersal potential of ingested seeds in the field remains unclear. We found no difference in dispersal potential between plants species growing in wet or dry habitats.
This study demonstrates that wild mallards are opportunistic seed consumers with a very diverse diet as reflected by seed species composition in both the foregut and hindgut. However, we also show that serious limitations of field‐based analyses compared to controlled experiments can impede drawing conclusions about gut passage survival of seeds. The large variability in diet composition among individuals and over time indicates high endozoochorous dispersal potential for a wide range of plant species by wild mallard in aquatic and wetland, as well as surrounding terrestrial habitats.
Background
Propagule retention time is a key factor in determining propagule dispersal distance and the shape of “seed shadows”. Propagules dispersed by animal vectors are either ingested and retained in the gut until defecation or attached externally to the body until detachment. Retention time is a continuous variable, but it is commonly measured at discrete time points, according to pre-established sampling time-intervals. Although parametric continuous distributions have been widely fitted to these interval-censored data, the performance of different fitting methods has not been evaluated. To investigate the performance of five different fitting methods, we fitted parametric probability distributions to typical discretized retention-time data with known distribution using as data-points either the lower, mid or upper bounds of sampling intervals, as well as the cumulative distribution of observed values (using either maximum likelihood or non-linear least squares for parameter estimation); then compared the estimated and original distributions to assess the accuracy of each method. We also assessed the robustness of these methods to variations in the sampling procedure (sample size and length of sampling time-intervals).
Results
Fittings to the cumulative distribution performed better for all types of parametric distributions (lognormal, gamma and Weibull distributions) and were more robust to variations in sample size and sampling time-intervals. These estimated distributions had negligible deviations of up to 0.045 in cumulative probability of retention times (according to the Kolmogorov–Smirnov statistic) in relation to original distributions from which propagule retention time was simulated, supporting the overall accuracy of this fitting method. In contrast, fitting the sampling-interval bounds resulted in greater deviations that ranged from 0.058 to 0.273 in cumulative probability of retention times, which may introduce considerable biases in parameter estimates.
Conclusions
We recommend the use of cumulative probability to fit parametric probability distributions to propagule retention time, specifically using maximum likelihood for parameter estimation. Furthermore, the experimental design for an optimal characterization of unimodal propagule retention time should contemplate at least 500 recovered propagules and sampling time-intervals not larger than the time peak of propagule retrieval, except in the tail of the distribution where broader sampling time-intervals may also produce accurate fits.
1. Dabbling ducks (Anatinae) are omnivorous birds that are widespread, numerous, highly mobile and often migratory, and therefore have great potential for (long-distance) dispersal of other organisms, including plants. However, their ability to act as plant dispersal vectors has received little attention compared to frugivores, and is often assumed to be relevant only for wetland species.
2. To evaluate the potential for plant dispersal by dabbling ducks, we collated and analysed existing data. We identified all plant species whose seeds have been recorded in the diets of the seven dabbling duck (Anas) species in the Western Palearctic, as reported from gut content analyses. We then analysed the habitats and traits of these plant species to identify general patterns, and related these to data on gut passage survival and duck movements.
3. A large number of plant species (>445 species of 189 genera and 57 families) have been recorded in the diet of dabbling ducks. These plant species represent a very wide range of habitats, including almost the full range of site fertility, moisture and light conditions, excluding only very dry and deeply shaded habitats. The ducks prefer seeds of intermediate sizes (1-10 mm3), which have good chances to survive gut passage, but also ingest smaller and larger seeds. Ingested seeds represent a wide range of dispersal syndromes, including fleshy fruits. Many species (62%) were not previously considered animal-dispersed in plant databases, and 66% were not identified as bird-dispersed. Rarefaction analyses suggest that our analysis still greatly underestimates the total number of plant species ingested.
4. Synthesis. Dabbling ducks do not exclusively ingest seeds of wetland plants, which make up only 40% of the ingested species. Rather, they feed opportunistically on a wide cross-section of plant species available across the landscapes they inhabit. Given the millions of ducks, the hundreds-to-thousands of seeds ingested per individual on a daily basis, and known gut passage survival rates, this results in vast numbers of seeds dispersed by ducks per day. Internal seed dispersal by dabbling ducks appears to be a major dispersal pathway for a far broader spectrum of plant species than previously considered.
Description Fit linear and generalized linear mixed-effects models. The models and their components are represented using S4 classes and methods. The core computational algorithms are implemented using the 'Eigen' C++ library for numerical linear algebra and 'RcppEigen' ``glue''.
Digestion is a process which takes place in resting conditions. Exercise is characterised by a shift in blood flow away from the gastrointestinal (GI) tract towards the active muscle and the lungs. Changes in nervous activity, in circulating hormones, peptides and metabolic end products lead to changes in GI motility, blood flow, absorption and secretion.
In exhausting endurance events, 30 to 50% of participants may suffer from 1 or more GI symptoms, which have often been interpreted as being a result of maldigestion, malabsorption, changes in small intestinal transit, and improper food and fluid intake. Results of field and laboratory studies show that pre-exercise ingestion of foods rich in dietary fibre, fat and protein, as well as strongly hypertonic drinks, may cause upper GI symptoms such as stomach ache, vomiting and reflux or heartburn. There is no evidence that the ingestion of nonhypertonic drinks during exercise induces GI distress and diarrhoea. In contrast, dehydration because of insufficient fluid replacement has been shown to increase the frequency of GI symptoms. Lower GI symptoms, such as intestinal cramps, diarrhoea — sometimes bloody — and urge to defecate seem to be more related to changes in gut motility and tone, as well as a secretion. These symptoms are to a large extent induced by the degree of decrease in GI blood flow and the secretion of secretory substances such as vasoactive intestinal peptide, secretin and peptide-histidine-methionine. Intensive exercise causes considerable reflux, delays small intestinal transit, reduces absorption and tends to increase colonic transit. The latter may reduce whole gut transit time. The gut is not an athletic organ in the sense that it adapts to increased exercise-induced physiological stress. However, adequate training leads to a less dramatic decrease of GI blood flow at submaximal exercise intensities and is important in the prevention of GI symptoms.
Long distance dispersal (LDD) of propagules is an important determinant of population dynamics, community structuring and biodiversity distribution at landscape, and sometimes continental, scale. Although migratory animals are potential LDD vectors, migratory movement data have never been integrated in estimates of propagule dispersal distances and LDD probability. Here we integrated migratory movement data of two waterbird species (mallard and teal) over two continents (Europe and North America) and gut retention time of different propagules to build a simple mechanistic model of passive dispersal of aquatic plants and zooplankton. Distance and frequency of migratory movements differed both between waterbird species and continents, which in turn resulted in changes in the shapes of propagule dispersal curves. Dispersal distances and the frequency of LDD events (generated by migratory movements) were mainly determined by the disperser species and, to a lesser extent, by the continent. The gut retention time of propagules also exerted a significant effect, which was mediated by the propagule characteristics (e.g. seeds were dispersed farther than Artemia cysts). All estimated dispersal curves were skewed towards local-scale dispersal and, although dispersal distances were lower than previous estimates based only on the vector flight speed, had fat tails produced by LDD events that ranged from 230 to 1209 km. Our results suggest that propagule dispersal curves are determined by the migratory strategy of the disperser species, the region (or flyway) through which the disperser population moves, and the propagule characteristics. Waterbirds in particular may frequently link wetlands separated by hundreds of kilometres, contributing to the maintenance of biodiversity and, given the large geographic scale of the dispersal events, to the readjustment of species distributions in the face of climate change.
Animal migrations span the globe, involving immense numbers of individuals from a wide range of taxa. Migrants transport nutrients,
energy, and other organisms as they forage and are preyed upon throughout their journeys. These highly predictable, pulsed
movements across large spatial scales render migration a potentially powerful yet underappreciated dimension of biodiversity
that is intimately embedded within resident communities. We review examples from across the animal kingdom to distill fundamental
processes by which migratory animals influence communities and ecosystems, demonstrating that they can uniquely alter energy
flow, food-web topology and stability, trophic cascades, and the structure of metacommunities. Given the potential for migration
to alter ecological networks worldwide, we suggest an integrative framework through which community dynamics and ecosystem
functioning may explicitly consider animal migrations.
Fruits and seeds are critical food sources for many European passerines during the autumn migration, which in turn contribute to disperse seeds either internally, i.e. after ingestion (endozoochory), or externally, when seeds adhere to the body surface (epizoochory). Despite the recognized importance of birds as seed dispersers, the vast majority of studies focused on endozoochory while the external transport of seeds is frequently invoked as being potentially important, but remains largely unexplored. This is particularly important during the post-breeding migration of passerines, the most ubiquitous and diverse movement of potential seed carriers across Europe and into Africa, which coincides with the fruiting peak of many plant species (August–October). Our aim was to evaluate the role of migrating birds as potential long-distance seed dispersers, and comparing the prevalence of epizoochory and endozoochory during post-breeding migration. We sampled 926 wild birds in nine locations in Portugal, and retrieved 1833 seeds of 19 plant species dispersed internally and only three seeds externally attached to three birds (Serinus serinus, Locustella naevia and Turdus merula), showing an endozoochory prevalence 85 times higher than that of epizoochory. Migrating and non-migrating passerines dispersed seeds equally. While two of the seeds transported externally had specific adaptations to epizoochory, namely spines (Torilis arvensis) and hooks (Galium aparine), the third is a large seed from a fleshy-fruited plant, Frangula alnus (i.e. typical endozoochorous syndrome). These seeds were found on bird species with different diets, but similar behaviour (ground foragers) and in similar habitats (open agro-ecosystems). Our results highlight the strong role of migrating passerines as potentially long-distance seed dispersers and show that, at least in the autumn, the prevalence of epizoochory is several orders of magnitude lower than that of endozoochory.
Common and widespread species often show a large variability in behaviour and habitat use. Such variability at the species level may result from individuals themselves being very variable or, alternatively, variability may arise from differences between individuals. The aim of this study was to explore land use in general and between-subject variability in the local movements and daily activity patterns of Mallards Anas platyrhynchos in central Switzerland during the winter. The Mallard is a common duck species and can be found on almost all types of water bodies. We equipped 24 ducks with VHF radio tags and searched for these ducks 1–3 times per day. We also used nine tags that automatically recorded their location every 30 min as well as acceleration in three dimensions every 2–5 min. These methods yielded information on the activity of the duck with a high temporal resolution both day and night. The 24 ducks were strongly linked to water, and 97% of all localisations were within 50 m of a water body. An affinity to settlements was only observed in the vicinity of the main lake in the area, but not for those ducks on smaller water bodies or fields. Some individuals were very stationary, using only a small area during the study period; others made daily commuting flights between two sites about 8 km apart while still others moved around similar distances but in varying directions. Rain and increasing wind speed correlated with decreasing movement activity. However, the effect of these weather parameters, and especially that of temperature, varied between individuals. Activity was strongly influenced by the sun’s movement, with general activity and flight activity being highest around sunrise and sunset. This daily pattern was similar for all individuals. Hence, while the activity pattern was similar for all individuals, the resulting degree of local movements and the response to changing weather parameters were very variable among individuals.
Ecosystem services are ecosystem processes that directly or indirectly benefit human well-being. There has been much recent literature identifying different services and the communities and species that provide them. This is a vital first step towards management and maintenance of these services. In this review, we specifically address the waterbirds, which play key functional roles in many aquatic ecosystems, including as predators, herbivores and vectors of seeds, invertebrates and nutrients, although these roles have often been overlooked. Waterbirds can maintain the diversity of other organisms, control pests, be effective bioindicators of ecological conditions, and act as sentinels of potential disease outbreaks. They also provide important provisioning (meat, feathers, eggs, etc.) and cultural services to both indigenous and westernized societies. We identify key gaps in the understanding of ecosystem services provided by waterbirds and areas for future research required to clarify their functional role in ecosystems and the services they provide. We consider how the economic value of these services could be calculated, giving some examples. Such valuation will provide powerful arguments for waterbird conservation.
Abstract Migratory birds are often suggested to be important vectors for long-distance dispersal (LDD) of plant and animal propagules. The scale of such dispersal events (hundreds to thousands of kilometers) can influence landscape-level biological processes and species distributions. However, the few vector species studied and the lack of proper integration of their migratory movement in models of LDD has precluded the study of their potential as long-distance biotic dispersers. By means of a mechanistic model parameterized with empirical data, we first investigated the properties of seed dispersal curves generated by migratory birds and then analyzed the effect of bird size on model parameters and consequent seed dispersal patterns. Seed dispersal curves showed in most cases large and heavy tails, resulting in relatively frequent LDD (up to 3.5% of dispersal distances longer than 100 km). Bird size mediated trade-offs between bird movement and seed retention time that, in turn, determined seed dispersal patterns and the potential of each bird species as an LDD vector. Our modeling framework builds on a mechanistic understanding of seed dispersal by migratory birds and may thus be a useful tool to estimate the scale and frequency of bird-mediated, large-scale transport of native, invasive, and pathogenic organisms.
Aim
Patterns of high biodiversity among less mobile organisms throughout isolated locations suggest that passive dispersal importantly contributes to biodiversity. We examined the contribution of waterbirds to the dispersal of plant seeds and macroinvertebrates between aquatic wetlands. Birds are renowned vectors for seeds of terrestrial plants, but less is known about their role in more dispersal‐dependent aquatic systems. We therefore performed a meta‐analysis on bird‐mediated endozoochorous dispersal of aquatic species.
Location
Our review included studies that collected data world‐wide.
Methods
We analysed data from 81 peer‐reviewed publications on endozoochorous dispersal of aquatic plant seeds and macroinvertebrates by waterbirds.
Results
In total, 36% of 1581 waterbird droppings collected in the field contained one or more intact propagules, with macroinvertebrates found almost as frequently as plant seeds. Positive droppings contained on average 3.3 intact propagules, of which one‐third were viable. In 728 trials from 17 published feeding experiments 24% of the ingested propagules were retrieved intact, with c . 6.5% both viable and intact. As many as 17 species of Anatidae and Rallidae were involved in the dispersal of at least 39 species of macroinvertebrates and seeds from 97 species of plants across a wide taxonomic range. Smaller propagules seemed less affected by digestion than larger ones. We provide a first quantitative model that can be used to estimate waterbird‐mediated dispersal of propagules between wetlands. This model indicates that an average waterbird has the potential to disperse five viable propagules after flying more than 100 km, and one additional propagule after flying 300 km.
Main conclusions
We demonstrate that waterbirds have the potential to transport a wide variety of aquatic plants and animals over several hundreds of kilometres. High survival of propagules might be explained by propagule adaptations or by the digestive adaptations of birds, whereby energy absorption is thought to be maximized rather than assimilation efficiency. Our meta‐analysis suggests that waterbirds might contribute significantly to wetland biodiversity around the world, despite several limitations to our current knowledge. We outline avenues for future research to address these knowledge gaps.
1. The directed‐dispersal (DrD) hypothesis constitutes one of the main explanations for the adaptive value of seed dispersal in spatially heterogeneous environments. Traditionally, the DrD hypothesis asserts non‐random arrival to specific sites where establishment conditions are independently favourable. Yet, enhanced arrival might negatively affect the establishment in otherwise favourable sites through enhanced density‐dependent mortality (DDM). Since both density effects and habitat suitability might differ among establishment phases, assessment of habitat suitability should encompass the entire establishment process.
2. Here, we test the DrD hypothesis against a null model of random dispersal (RD) in an arid ecosystem where fleshy‐fruited perennial Ochradenus baccatus shrubs are dispersed by two resident passerines. Acacia trees were predicted to present the favourable habitat in our system through the nurse‐plant effect facilitating O. baccatus early establishment.
3. We determined expected seed arrival by monitoring the dispersers’ time allocation among the different habitats and assessed habitat quality for different establishment phases: seed‐phase survival (post‐dispersal survival and germination) was determined by line transects, while early seedling survival was estimated by monitoring seedlings throughout the first dry season. Additionally, subsequent recruitment success was assessed by comparing the distribution of adult shrubs to that expected from the observed germination patterns.
4. When considering the expected seed arrival and early establishment (seed‐phase and early seedling survival), the DrD hypothesis is supported: birds preferentially deposited seeds in habitats where conditions are favourable (e.g. under Acacia trees). Yet, considering recruitment success during later phases, the dispersal service provided by the birds was less beneficial than RD.
5. Effective density was indexed using the zone‐of‐influence approach in which densities are corrected by phase‐specific sizes. We suggest that intense seed deposition into favourable habitats has led to strong DDM (presumably through competition) in those habitats during late establishment phases and was responsible, at least partially, for changes in habitat suitability across the recruitment phases.
6. Synthesis . Our results show that assessment of the DrD hypothesis depends on the context of the study (in terms of recruitment phases) since sites of enhanced seed arrival and high seed‐to‐seedling survival can ultimately prove unfavourable to the plant if density‐dependent or other effects might increase mortality in these sites during later recruitment phases.
Dispersal-viewed as the departure of a diaspore (eg. seed or fruit) from the parent plant-is examined in terms of mechanisms, advantages (eg. in connection with escape from parental influence, and colonization), and patterns of production (eg. geographical aspects, seasonality, and intraspecific variation).-P.J.Jarvis
Vertebrates are important seed dispersers for many plants. In addition to transport of seeds, ingestion often affects the proportion or rate of seed germination. We present one of the first studies comparing the effects of different waterbird species on the seeds of a subcosmopolitan pondweed, Potamogeton pectinatus. We also present the first comparison of the effects of digestion by ducks (mallard Anas platyrhynchos, shoveler A. clypeata and wigeon A. penelope) and physical-chemical "simulation of digestion" on pondweed seed germination. In two experiments differing in the length of the preceding stratification period, two to three individuals per duck species were force-fed 150 seeds each. Average retrieval, total germination and germination rate did not differ significantly between duck species. Germination rate was higher for duck ingested seeds, intermediate for scarified seeds (i.e. after mechanical removal of the epicarp+mesocarp) and lowest for the controls and acid treated seeds, independently of the length of the stratification period. Total germination, however, did not differ significantly among duck-ingested, scarified, control and acid treated seeds. Consequently the changes in germination rate after ingestion by ducks seem related to the grinding treatment in the gut and unrelated to exposure to acidic conditions. The co-existence of ingested and uningested seeds within a given seed cohort will increase the diversification of seed germination patterns, which can favour the colonisation of habitats characterised by unpredictable environmental conditions.
1. Inland wetlands constitute ecological islands of aquatic habitat often isolated by huge areas of non-suitable terrestrial habitats. Although most aquatic organisms lack the capacity to disperse by themselves to neighbouring catchments, many species present widespread distributions consistent with frequent dispersal by migratory waterbirds.
2. A literature review indicates that bird-mediated passive transport of propagules of aquatic invertebrates and plants is a frequent process in the field, at least at a local scale. Both endozoochory (internal transport) and ectozoochory (external transport) are important processes.
3. The characteristics of the dispersed and the disperser species that facilitate such transport remain largely uninvestigated, but a small propagule size tends to favour dispersal by both internal and external transport.
4. We review the information currently available on the processes of waterbird-mediated dispersal, establishing the limits of current knowledge and highlighting problems with research methods used in previous studies. We also identify studies required in the future to further our understanding of the role of such dispersal in aquatic ecology.
The spatial distribution of plants (and other primarily sessile organisms) depends on the interplay between their ecological requirements and the spatial template set before, during, and after the dispersal process. In the case of animal-dispersed plants, the spatial characteristics of animal behaviour during the seed dispersal process are likely to leave a lasting imprint on plant distribution. Here, we hypothesize that the activity patterns of the frugivorous lizard Podarcis lilfordi directly influence the spatial distribution of the fleshy-fruited shrub Daphne rodriguezii. To evaluate this hypothesis, we first analysed lizard activity, following radio-tracked lizards during the plant's fruiting period, and identified its main determinants at several spatial scales of habitat aggregation (from 12.5 to 150 m). We hypothesised that lizard activity depends on differential habitat features explaining its territory use plus habitat preferences associated with each movement bout. In a second step, the most important determinants of lizard activity plus the variables describing habitat structure were used to predict the presence of adult and juvenile plants. Predictability of lizard activity (based on AUC and Pearson regression coefficients) was higher at broad spatial-scales of habitat aggregation (75 m). The two best predictors of lizard activity were the habitat features of and the distance to the core area (defined as the area enclosing the 0.50 cumulative probability of lizard locations). Plant presence was best predicted by models based on a combination of lizard activity and habitat features at local spatial scales (1.5 m). Best models included habitat features and lizard activity for adult plants, and local-scale habitat features, the proximity of adult plants and lizard activity for juveniles. In both cases, most plants (50–60%) were located at ‘optimal sites’ (both favourable for lizards and with adequate habitat features), whereas a small fraction of them (3–10%) were located at dispersal-limited sites (i.e. with adequate habitat features but suboptimal for lizards). Our results thus suggest that the interplay between lizard activity and local habitat features determines the spatial patterns of juvenile-plant presence and leaves a lasting signature on adult-plant distribution.
1. Over the past centuries, European streams have been heavily influenced by humans through pollution and regulation. As a result, the quality and diversity of freshwater riparian habitats have declined strongly, and the diversity of riparian flora and fauna has decreased. Recent restoration measures have resulted in stream habitat improvements, but biodiversity improvements have failed to follow in fragmented streams. It has been suggested that dispersal limitation could play an important role in the lack of biodiversity improvement in restored streams, but to date, there is no conclusive evidence for this assumption.
2. In this study, we investigated whether colonization of restored streams by plants and macroinvertebrates is limited by dispersal. We hypothesized that colonization success increases with increasing availability of (nearby) source populations and with increasing ability of species to disperse over long distances. We related species composition in seven restored stream sections to species’ abundances in the surroundings and to species’ dispersal abilities.
3. For both plants and macroinvertebrates, colonization success is strongly related to the abundance of species in the local and regional species pools.
4. For plants, dispersal strategy has an additional influence on colonization success: short‐lived plants with high production of small, well‐dispersed seeds colonized best within the 3‐ to 5‐year period after restoration.
5. The existence of dispersal strategy constraints could not be confirmed in macroinvertebrates, possibly because these are limited by a lack of connectivity on larger spatial scales. On the landscape scale, beneficial effects of increased plant diversity might further improve habitat suitability for macroinvertebrates.
6. Synthesis and applications. Dispersal appears to be a limiting factor for successful (re)colonization of restored streams in fragmented landscapes. In plants, this is attributed to limitations in seed dispersal abilities and likely to a lack of nearby source populations as well. In macroinvertebrates, lack of nearby source populations may also be a limiting factor. Hence, we suggest restoring landscape connectivity at larger spatial scales and optimizing the availability of near‐natural ‘source’ areas in the vicinity of restoration projects, at least for plants, to improve the success of biodiversity restoration in fragmented habitats.
Vertebrates are important seed dispersers for many plants, particularly those inhabiting naturally fragmented habitats such as lakes and wetlands. Such dispersal often takes place through the transport of ingested seeds (endozoochory).
Endozoochorous passage of seeds is likely to vary among both disperser and dispersed species. We hypothesized that seed retention time and survival of gut passage varies among disperser species (here Anas ducks) and is influenced by intraspecific differences in seed size.
Wigeongrass ( Ruppia maritima ) seeds were ingested by five duck species; Teal, Wigeon, Shoveler, Pintail and Mallard. Defecated seeds were recovered and germinated.
Total retrieval and germination of seeds, patterns of retrieval over time and seed weight before and after gut passage did not differ among duck species. Hence interspecific differences among Anas ducks and intraspecific differences in seed weight do not affect seed retention time or the response of seeds to gut passage.
Germination of retrieved seeds was influenced by the retention time in the gut, with seeds voided earlier more likely to germinate than those voided later.
The probability of dispersal at different retention times by any given duck was low. However, when considering the thousands of ducks moving among wetlands, the dispersal probabilities of seeds become significant.
Estimation of seed dispersal distance as a function of retention time suggested higher dispersal probabilities for seeds voided earlier. Based on average flight speeds ranging from 10 to 70 km h ⁻¹ , most probable dispersal distances range from 40 to 280 km. Dispersal over greater distances is possible, but less likely.
The consequences of plastic responses of the avian digestive tract for the potential of birds to disperse other organisms remain largely uninvestigated.
To explore how a seasonal diet switch in Mallard ( Anas platyrhynchos L.) influences their potential to disperse plants and invertebrates, we recorded the retention time of markers, following exposure to two diets of contrasting digestibility (trout chow vs seeds).
We then recorded the retrieval and germination of Fennel Pondweed ( Potamogeton pectinatus L.) seeds and Brine Shrimp ( Artemia franciscana Kellogg) cysts ingested by the same birds.
Gut passage rates of markers were increasingly longer in birds on the seed‐based, high‐fibre diet and shorter in birds on the animal‐based, low‐fibre one.
Propagule digestibility, and thus survival to gut passage, differed between diet groups, with more seeds and fewer cysts retrieved from ducks on the animal‐based diet. Germination decreased with retention time, but was not affected by diet.
Differences in passage rates of markers but not of seeds and cysts suggest no change in dispersal distances of plants and invertebrates between seasons, while differences in digestibility would affect the numbers of propagules dispersed.
1. Migratory waterbirds are major vectors for the dispersal of aquatic plants. However, quantitative field studies of the frequency of transport are scarce, and the relative importance of internal and external transport remains unclear.
2. We quantified and compared the rates of internal and external transport of aquatic plant propagules by teal ( Anas crecca ) in the Camargue (southern France), inspecting the lower gut contents of birds that had been shot ( n = 366) and washing birds that had been live‐trapped ( n = 68) during the winters of 2006–2007 and 2007–2008.
3. Intact propagules ( n = 902) of 21 plant taxa were recorded in the rectum of teal, of which 16 germinated or were shown to be viable. Intact propagules were recorded in the rectum of 20% of teal, with up to 171 propagules per individual bird. Chara oogonia were most abundant (60% of intact propagules), suggesting that small size favours internal transport. Eleocharis palustris , Juncus spp. and Potamogeton pusillus (17, 7 and 6% of intact propagules, respectively) were also very abundant.
4. Intact propagules ( n = 12) of 10 plant taxa were found on the outside of live teal, and four of these taxa later germinated. Intact propagules were found on 18% of teal. No teal was found to carry more than one propagule externally. There was no difference in size between propagules transported internally and externally.
5. Teal are major dispersers of plants within the Camargue, despite being highly granivorous. Contrary to widespread assumptions in the literature, endozoochory by ducks appears to be a much more important mode of dispersal for aquatic plants than exozoochory. We found no evidence of changes in the probability of plant propagule dispersal at a landscape scale over the course of the winter, so propagule production and zoochory appear to be decoupled over time in aquatic systems.
Seed dispersal is an important process for plants, but may be particularly important for plants occurring in spatially isolated
habitats like wetlands. Variation in the geographic distribution of wetland plant species may be strongly influenced by their
ability to use waterbirds, particularly waterfowl to enhance dispersal. We used controlled feeding and germination experiments
to investigate recovery, retention time, and germination for the seeds of 10 wetland plant species (Chenopodium album, Digitaria ischaemum, Echinochloa colonum, Echinochloa crusgalli, Eleocharis palustris, Panicum dichotomiflorum, Polygonum lapathifolium, Polygonum pensylvanicum, Rumex crispus, and Scheonoplectus maritimus) and compared how these metrics varied with seed characteristics. We fed a known number of seeds to captive raised mallards
(Anas platyrhynchos) and collected fecal samples every 4 hours for 48 hours; all recovered seeds were planted in seedling trays and watched for
60 days to monitor germination. We conducted 10 trials and fed each seed species in each trial, and included germination controls
of non-consumed seeds. Overall, 19.0 ± 1.8% (mean ± SE) of seeds were recovered and of recovered seeds 7.6 ± 1.2% germinated.
Recovery ranged from 1.9 ± 0.6% in D. ischaemum to 51.0 ± 4.7% in S. maritimus and germination ranged from < 0.5% in D. ischaemum to 28.5 ± 5.7% in R. crispus. Recovery and germination were not related to seed size or mass (p > 0.5) but recovery was positively correlated with seed
fiber content (r2 = 0.44, p = 0.04). Control seeds germinated better than fed seeds for all species except S. maritimus, where fed seeds germinated better. Germination percentage declined with gut retention time for four of seven species. We
suggest despite the large differences in viable seeds recovered, mallards may be important dispersers for the seeds of most
species we studied and hypothesize that observed variation may be attributable to different plant strategies that relate to
reproductive tactics and habitat type.
Despite a long historical record of radio-tracking analyses, basic home-range information is still lacking for most common
waterfowl species, especially during the winter. We investigated how dabbling duck home ranges and daily foraging movements
are influenced by extrinsic (site, temperature, date) and intrinsic factors (species, sex, age). We radio-tagged and monitored
125 individuals of three duck species (mallard Anas platyrhynchos, Eurasian teal A. crecca crecca and northern pintail A. acuta) in three French wetlands over four winters. Home-range sizes for a given species varied greatly among our study sites. Moreover,
species differed according to home-range structure and distance traveled to reach their foraging grounds (teal had a more
patchy home range and traveled farther distances than mallards). Foraging distances increased with temperature and time (over
the winter season), but this effect differed among species, suggesting that they behave differently in response to food depletion
and/or cold weather. The commuting behavior (i.e., the decision to leave the roost at night for foraging) differed among species
and season. Teals were more risk-prone because they were more likely to leave the roost at night. In our study, ducks foraged
at distances of 1–2km from roosts, whereas distances of 2–48km have been recorded in North America. We suggest that food
supply, hunting pressure or population density may account for these inter-continental differences.
It is commonly assumed that waterbirds act as dispersal vectors of aquatic organisms. In this paper we review experimental work focusing on the endozoochorous transport of propagules by waterbirds with the aim to determine what aspects of this mechanism have been investigated. We discuss (i) the main issues addressed in propagule feeding experiments, (ii) aspects of the gut structure that affect the retrieval, retention time and viability of propagules, and (iii) the importance of assessing propagule retention time in the gut. A total of 26 experimental studies exist, which represent a very low number when compared to studies of seed dispersal in terrestrial systems. The diversity of questions dealt with in these articles was low, with the majority focusing exclusively on whether propagules survive gut passage. More comparative studies involving batches of disperser and dispersed species should be carried out, also to establish whether they possess characteristics that favour endozoochorous transport. It is important to assess the effect of intra- and inter-specific variation in the different sections of the waterbird gut on the fate of propagules. Additionally, experimental work dealing with the mechanism of endozoochorous dispersal can be separated into a sequence of events. Each event is characterised by its own probability of occurrence. In most studies, complete data sets relating to every step of the process have not been collected. In order to quantify dispersal probabilities of propagules such data are necessary.
Many small organisms in various life stages can be transported in the digestive system of larger vertebrates, a process known as endozoochory. Potential dispersal distances of these “propagules” are generally calculated after monitoring retrieval in experiments with resting vector animals. We argue that vectors in natural situations will be actively moving during effective transport rather than resting. We here test for the first time how physical activity of a vector animal might affect its dispersal efficiency. We compared digestive characteristics between swimming, wading (i.e. resting in water) and isolation (i.e. resting in a cage) mallards (Anas platyrhynchos). We fed plastic markers and aquatic gastropods, and monitored retrieval and survival of these propagules in the droppings over 24 h. Over a period of 5 h of swimming, mallards excreted 1.5 times more markers than when wading and 2.3 times more markers than isolation birds, the pattern being reversed over the subsequent period of monitoring where all birds were resting. Retention times of markers were shortened for approximately 1 h for swimming, and 0.5 h for wading birds. Shorter retention times imply higher survival of propagules at increased vector activity. However, digestive intensity measured directly by retrieval of snail shells was not a straightforward function of level of activity. Increased marker size had a negative effect on discharge rate. Our experiment indicates that previous estimates of propagule dispersal distances based on resting animals are overestimated, while propagule survival seems underestimated. These findings have implications for the dispersal of invasive species, meta-population structures and long distance colonization events.
Electronic supplementary material
The online version of this article (doi:10.1007/s00442-012-2293-0) contains supplementary material, which is available to authorized users.
Long-distance dispersal (LDD) events, although rare for most plant species, can strongly influence population and community dynamics. Animals function as a key biotic vector of seeds and thus, a mechanistic and quantitative understanding of how individual animal behaviors scale to dispersal patterns at different spatial scales is a question of critical importance from both basic and applied perspectives. Using a diffusion-theory based analytical approach for a wide range of animal movement and seed transportation patterns, we show that the scale (a measure of local dispersal) of the seed dispersal kernel increases with the organisms' rate of movement and mean seed retention time. We reveal that variations in seed retention time is a key determinant of various measures of LDD such as kurtosis (or shape) of the kernel, thinkness of tails and the absolute number of seeds falling beyond a threshold distance. Using empirical data sets of frugivores, we illustrate the importance of variability in retention times for predicting the key disperser species that influence LDD. Our study makes testable predictions linking animal movement behaviors and gut retention times to dispersal patterns and, more generally, highlights the potential importance of animal behavioral variability for the LDD of seeds.
Exercise and digestive processes are known to elevate the metabolic rate of organisms independently. In this study, the effects of simultaneous exercise and digestion were examined in the graceful crab Cancer gracilis. This species exhibited resting oxygen uptake levels between 29 and 42 mg O(2) kg(-1) h(-1). In postprandial crabs, oxygen uptake was approximately double that of unfed crabs. During exercise, oxygen uptake increased three- to fourfold, reaching maximal levels of more than 130 mg O(2) kg(-1 ) h(-1). However, there was no difference in oxygen uptake during activity between unfed and postprandial animals. There was also no difference in exercise endurance levels between unfed and postprandial animals; both sets of animals were unable to right themselves after being turned on their backs, reaching exhaustion after 13-15 attempts. To determine whether increased activity affected gastric processes, the passage of a meal through the digestive system was followed using a fluoroscope. Passage of digesta through the gut system was slower in active animals than in resting crabs. Resting crabs cleared the foregut after approximately 18 h, which was significantly faster than the 34.5 h for constantly active animals. Likewise, the midgut region of resting animals was cleared at a faster rate than that of active animals. Because of residual amounts of digesta remaining in the hindgut, no difference in clearance rates of this section of the gut was evident. The slower clearance times of the foregut were due to a significantly slower rate of mastication of food, as evidenced by a lower cardiac stomach contraction rate. Contraction of the pyloric region of the foregut functions to move the digesta along the midgut, and there was a direct correlation between slower contraction rates of this region and the increased time of passage for digesta through the midgut of active animals. Because increased activity levels affected gastric processing, the crabs exhibited a behavioral response. During a 24-h period after feeding, there was a significant reduction in locomotor activity. The findings of this study suggest a prioritization of metabolic responses toward activity at the expense of digestion. This is discussed in relation to the ability of the crabs to balance the demands of competing physiological systems.
Growth in seed dispersal studies has been fast-paced since the seed disperser effectiveness (SDE) framework was developed 17 yr ago. Thus, the time is ripe to revisit the framework in light of accumulated new insight. Here, we first present an overview of the framework, how it has been applied, and what we know and do not know. We then introduce the SDE landscape as the two-dimensional representation of the possible combinations of the quantity and the quality of dispersal and with elevational contours representing isoclines of SDE. We discuss the structure of disperser assemblages on such landscapes. Following this we discuss recent advances and ideas in seed dispersal in the context of their impacts on SDE. Finally, we highlight a number of emerging issues that provide insight into SDE. Overall, the SDE framework successfully captures the complexities of seed dispersal. We advocate an expanded use of the term dispersal encompassing the multiple recruitment stages from fruit to adult. While this entails difficulties in estimating SDE, it is a necessary expansion if we are to understand the central relevance of seed dispersal in plant ecology and evolution.
The metabolic cost of swimming was studied in mallard ducks (Anas platy-rhynchos) which had been trained to swim steadily in a variable-speed water channel. At speeds of from 0·35 to 0·50 m/sec the oxygen consumption remained relatively constant at approximately 2·2 times the resting level. At speeds of 0·55 m/sec and higher the oxygen consumption increased rapidly and reached 4·1 times resting at the maximum sustainable speed of 0·70 m/sec.. The maximum sustainable swimming speed of the ducks coincided with the limit predicted from hydrodynamic considerations of the water resistance of a displacement-hulled ship of the same hull length as a duck (0·33 m). The cost of transport (metabolic rate/speed) reached a minimum of 5·77 kcal/ kg km at a swimming speed of 0·50 m/sec. Ducks swimming freely on a pond were observed to swim at the speed calculated in experimental trials to give minimum cost of transport. Drag measurements made with model ducks indicated a maximum overall efficiency (power output/power input) for the swimming ducks of about 5%. Ships typically have maximum efficiencies of 20–30%. Because of the difficulty in delimiting the cost of swimming activity alone from the other bodily functions of the duck, overall efficiency may present an incorrect description of the swimming performance of the duck relative to that of a ship. An hydrodynamic parameter such as speed/length ratio whereby a duck excels conventional ships may present a more appropriate comparison.
Digestion is a process which takes place in resting conditions. Exercise is characterised by a shift in blood flow away from the gastrointestinal (GI) tract towards the active muscle and the lungs. Changes in nervous activity, in circulating hormones, peptides and metabolic end products lead to changes in GI motility, blood flow, absorption and secretion. In exhausting endurance events, 30 to 50% of participants may suffer from 1 or more GI symptoms, which have often been interpreted as being a result of maldigestion, malabsorption, changes in small intestinal transit, and improper food and fluid intake. Results of field and laboratory studies show that pre-exercise ingestion of foods rich in dietary fibre, fat and protein, as well as strongly hypertonic drinks, may cause upper GI symptoms such as stomach ache, vomiting and reflux or heartburn. There is no evidence that the ingestion of nonhypertonic drinks during exercise induces GI distress and diarrhoea. In contrast, dehydration because of insufficient fluid replacement has been shown to increase the frequency of GI symptoms. Lower GI symptoms, such as intestinal cramps, diarrhoea--sometimes bloody--and urge to defecate seem to be more related to changes in gut motility and tone, as well as a secretion. These symptoms are to a large extent induced by the degree of decrease in GI blood flow and the secretion of secretory substances such as vasoactive intestinal peptide, secretin and peptide-histidine-methionine. Intensive exercise causes considerable reflux, delays small intestinal transit, reduces absorption and tends to increase colonic transit. The latter may reduce whole gut transit time. The gut is not an athletic organ in the sense that it adapts to increased exercise-induced physiological stress. However, adequate training leads to a less dramatic decrease of GI blood flow at submaximal exercise intensities and is important in the prevention of GI symptoms.
The development of Charles Darwin's views on evolution by natural selection has fascinated biologists since the 1859 publication of his landmark text On The Origin of Species. His experiences, observations and reflections during and after his pivotal journey on the Beagle during 1831-36 were of critical importance. Darwin was not, however, a man to be rushed. While his autobiography claims that the framework of his theory was laid down by 1839, its first outline sketch did not emerge until 1842. That essay was heavily edited, with many insertions and erasures. It formed the vital kernel of his more expansive but also unpolished and unpublished essay of 1844. Following careful editing by his son Francis, both essays were published in 1909, and are reproduced here. Reading these side by side, and together with the Origin, permits us to scrutinise selection and evolution truly in action.
Ecologists, both practical and theoretical, now appreciate that to understand biological systems they must consider the spatial dimension. Consequently, dispersal has become one of the hottest topics in plant ecology. However, in the midst of so much research output on dispersal, there is a need for a stock-take to determine the needs of future research: what has been achieved to date, where do current studies fit in, and what still needs to be determined? What are the implications of dispersal for those engaged in managing plant populations and communities? This is the first book for many years to present a synthesis of research on dispersal and its implications for plant population dynamics. The book consists of three sections: Section A reviews information on the biological and environmental processes that determine the path of an individual dispersing propagule, usually a seed, and the theory that has been developed to predict these trajectories; Section B discusses the distributions of seeds resulting from dispersal from an entire plant, theoretical research predicting the shapes of these distributions and design issues for future dispersal studies; Section C explores the implications of dispersal for expansion of populations, structure within existing populations and communities, and the evolution of dispersal traits.
We trained white-crowned sparrows to locomote (normal mixed gait) on the wiremesh substrate of a circular treadmill while we measured steady-state , evaporative water loss (), and intraperitoneal temperature () at several treadmill speeds (0, 0.30, 0.35, 0.41, 0.46 km h⁻¹) and air temperatures (, 10, 0, 12, and 25 C) at each speed. In birds at rest, increased as diminished, but was independent of when birds were locomoting. At any , increased linearly with treadmill speed (to a maximum of 44.1 C). At or lower, was a linear function of at all treadmill speeds but did not conform to this regression at ( at 0.35-0.46 km h⁻¹ was lower than expected). We hypothesize that is not a reliable index of thermal environment in this zone and should be replaced by the "operative temperature," . At all , was a linear function of treadmill speed, with a progressively diminishing slope that became zero at . The percentage of total heat lost by latent transfer increased with increasing but was independent of treadmill speed. From these data, we propose that the heat increment of locomotion progressively substitutes for the thermostatic requirement. At , is independent of treadmill speed, and it costs a white-crowned sparrow no more energy to move about and forage than it costs it just to sit still and shiver to produce thermostatic heat. This has important implications for the interpretation of ecological theories of optimal foraging.
1 A metapopulation approach considers the ecology and genetics of populations as a product of local dynamics and the regional processes of migration, extinction and colonization. While conventional metapopulation theory involves species with frequent population turnover, limited migration and random extinction, it is likely that metapopulation dynamics, broadly defined as the product of local population dynamics and dispersal, is a feature of all species. 2 Theoretical metapopulation models of single species make three critical insights. First, metapopulations will consist of a shifting mosaic of local populations linked through migration with only a fraction of the available habitat patches occupied at one time. Secondly, there is a threshold number of habitats available, below which the species cannot persist because extinction exceeds colonization. Thirdly, the antagonism between selective forces acting during recolonization and population growth can influence the evolution of phenotypic traits. Unfortunately, little empirical data is available to evaluate these ideas for plants or to address the broader issue of whether processes at a regional scale add anything to our understanding of population dynamics. 3 Plants may seem particularly appropriate for metapopulation analyses as a result of their immobility, strong spatial structure and restricted dispersal. However, a review of the literature revealed a paucity of studies that explicitly adopted a metapopulation approach, particularly in terms of testing theoretical models. We argue that this is because of the difficulty of measuring parameters such as extinction, colonization and migration that are central to most metapopulation models. 4 Plants possess a number of special features that present both challenges and opportunities for the development of new insights into the biology of metapopulations. Three particular characteristics, seed dormancy, restricted dispersal and local adaptation, need to be incorporated into existing theoretical models so they more accurately reflect the dynamics of plant metapopulations. Finally, more effort is needed to incorporate the explicit spatial structure of individuals within metapopulations and to investigate the effect that dispersion has on their growth and reproduction.
Metapopulation biology is concerned with the dynamic consequences of
migration among local populations and the conditions of regional
persistence of species with unstable local populations. Well established
effects of habitat patch area and isolation on migration, colonization
and population extinction have now become integrated with classic
metapopulation dynamics. This has led to models that can be used to
predict the movement patterns of individuals, the dynamics of species,
and the distributional patterns in multispecies communities in real
fragmented landscapes.
Within the paradigm of resource-limited competition-structured communities,
dabbling ducks (Anas spp.) have been used as a textbook example of how morphological
differences, notably bill lamellar density and body length, may allow
sympatric species to partition food and hence coexist. We reviewed all accessible
diet studies from the Western Palearctic for three closely related dabbling duck
species, mallard (Anas platyrhynchos), pintail (A. acuta) and teal (A. crecca), and
present a comprehensive list of the food items (invertebrates, seeds, vegetative
parts of plants) ingested. To assess the circumannual perspective of niche separation,
we evaluated size distribution of ingested seeds among seasons and duck
species. There was a significant difference among duck species in mean size and
mass of ingested seeds, as well as in diet composition, with the largest seeds
consumed by the largest species (mallard) with the coarsest bill filter apparatus
(lamellae), and the smallest seeds by the smallest species (teal) with the finest bill
lamellae. However, no effect of season was found, suggesting consistent diet
segregation among species throughout the annual cycle of ducks and over large
geographical areas. We argue that the patterns of food size separation between
the three species are compatible with the idea of coexistence under interspecific
competition.
We investigated whether daily O₂ consumption ( ) could be predicted from heart rate ( ) in five exercising barnacle geese (Branta leucopsis) and compared the accuracy of this method with that of the doubly labeled water (DLW) method. The regressions of on , based on incremental speed tests, differed among individual birds. The O₂ pulse (i. e., ) progressively increased with exercise level from 0.22 mL O₂ heartbeat⁻¹ during resting to an estimated 0.47 mL O₂ heartbeat⁻¹ during flight. Daily , was generally underestimated (-3.9%) by (individual) resting O₂, pulses but overestimated (+8.4%) by linear regressions of on . However, it was wellpredicted (+0.8%) by the O₂ pulses appropriate for each exercise level When using relationships derived from the group of birds, the estimations were generally improved (-3.3% for resting O₂, pulse, -0.03% for appropriate O₂ pulse) but poorer (+13.6%) for the group linear regression. Some of these predictions were better than the estimation of daily CO₂ production ( ) by the two-compartment model of the DLW method (average algebraic error of +0.9%). We conclude that can be used to estimate daily energy expenditure in birds accuratelyprovided that (1) its application is limited to the range of exercise levels in which has been calibrated against and (2a) relationships are determined for each individual bird or (2b) the measurements of several free-ranging birds are averaged. Heart rate can also be used to indicate within-day variation in energy expenditure.
Long‐distance dispersal (LDD) is important in plants of dynamic and ephemeral habitats. For plants of dynamic wetland habitats, waterfowl are generally considered to be important LDD vectors. However, in comparison to the internal (endozoochorous) dispersal of terrestrial plants by birds, endozoochorous dispersal of wetland plants by waterfowl has received little attention. We quantified the capacity for endozoochorous dispersal of wetland plants by waterfowl and identified the mechanisms underlying successful dispersal, by comparing the dispersal capacities of a large number of wetland plant species.
We selected 23 common plant species from dynamic wetland habitats and measured their seed characteristics. We fed seeds of all species to mallards ( Anas platyrhynchos ), a common and highly omnivorous duck species, and quantified seed gut survival, gut passage speed and subsequent germination. We then used a simple model to calculate seed dispersal distances.
In total 21 of the 23 species can be dispersed by mallards, with intact seed retrieval and subsequent successful germination of up to 32% of the ingested seeds. The species that pass fastest through the digestive tract of the mallards are retrieved in the greatest numbers (up to 54%) and germinate best (up to 87%). These are the species with the smallest seeds. Seed coat thickness plays only a minor role in determining intact passage through the mallard gut, but determines if ingestion enhances or reduces germination in comparison to control seeds.
Model calculations estimate that whereas the largest seeds can hardly be dispersed by mallards, most seeds can be dispersed up to 780 km, and the smallest seeds up to 3000 km, by mallards during migration.
Synthesis . This study demonstrates the mechanism underlying successful endozoochorous dispersal of wetland plant seeds by mallards: small seed size promotes rapid, and hence intact and viable, passage through the mallard gut. Mallards can disperse wetland plant seeds of all but the largest‐seeded species successfully in relatively large numbers (up to 32% of ingested seeds) over long distances (up to thousands of kilometres) and are therefore important dispersal vectors.
Summary 1. Nature conservation and restoration traditionally focus on protecting individual sites. In parts of the world where the natural landscape has been severely altered for agricultural or urban use, individual patches are too small and isolated to ensure effective nature protection. Spatial proc- esses, such as metapopulation dynamics, are disrupted and natural linkages in the landscape, such as water flows, are severed by modifications in the landscape and hydrology. 2. We propose the identification of Operational Landscape Units (OLUs), which are defined as combinations of landscape patches with their hydrogeological and biotic connections, as a tool to facilitate wetland restoration in catchments with a high degree of fragmentation and strongly altered hydrology. The combined consideration of biotic (i.e. dispersal, transports of organisms) and hydrological connections (flooding events, groundwater flowpaths) is a new approach. 3. We developed criteria for the delineation of OLUs in regional wetland restoration initiatives. The key elements for delineation are definition of the restoration objectives, identification of spatial landscape mechanisms and information on historic and present land uses and hydrologic management. 4. As a case study, we delineated an OLU by applying these criteria in a restoration initiative for a large agricultural area that used to be a floodplain until the early 1950s in N.E. Twente, The Netherlands. The OLU encompassed not only the floodplain area to be restored but also a relatively remote nature reserve upstream as well as the stream connecting both areas. By restoring the historic water regime, flooding events would become a regular feature in the two areas and organisms including seeds would flow from the nature reserve to the restored floodplain. 5. Synthesis and applications. Discussions of the proposed Operational Landscape Units with stakeholders (water authorities, nature conservation agencies, farmers) resulted in shared insights which will lead to modifications of the original management plan for the area. We believe the OLU approach will make natural resource managers aware of the importance of spatial processes and connectivity in landscapes and, if properly applied, will lead to more natural and more successful restoration projects.
Little is known about the role of migratory waterfowl in the long-distance dispersal (LDD) of seeds. We studied the gut contents of 42 teals Anas crecca collected in the Camargue, southern France, and found intact seeds of 16 species. There was no relationship between the probability that a given seed species was found intact in the lower gut, and the seed hardness or size. The number of seeds found in the oesophagus and gizzard (a measure of ingestion rate) was the only significant predictor of the occurrence of intact seeds in the lower gut, so studies of waterfowl diet can be used as surrogates of dispersal potential. In a literature review, we identified 223 seed species recorded in 25 diet studies of teal, pintail Anas acuta, wigeon A. penelope or mallard A. platyrhynchos in Europe. We considered whether limited species distribution reduces the chances that a seed can be carried to suitable habitat following LDD. Overall, 72% of plant species recorded in duck diets in southern Europe (36 of 50) were also recorded in the north, whereas 97% of species recorded in duck diets in the north (137 of 141) were also recorded in the south. This suggests a great potential for LDD, since most dispersed plants species occur throughout the migratory range of ducks. Migratory ducks are important vectors for both terrestrial and aquatic plant species, even those lacking the fleshy fruits or hooks typically used to identify seeds dispersed by birds. Finally, we show ducks are important vectors of exotic plant species. We identified 14 alien to Europe and 44 native to Europe but introduced to some European countries whose seeds have been recorded in duck diet.
We review whether migratory Anatidae, i.e., swans, geese and ducks, could be acting as vectors for dispersal of Zostera, Ruppia and Potamogeton propagules by endozoochory (carrying seeds in their guts). We list six prerequisites that must all be fulfilled, if successful dispersal should occur. Several Anatidae species feed on these macrophytes, and undertake rapid long-distance movements, making dispersal possible. We identify four problems, which in combination leads us to conclude that long-distance dispersal events are likely to be rare. (i) Most long-distance movements are out of phase with the reproductive efforts of the plants, and if birds arrive at sites when plants still bear seeds, they are likely to depart well after seed stocks have been depleted. (ii) Seed transport by birds will usually be uni-directional, from north to south on autumn migrations. (iii) Most of the gut contents of migratory birds are likely to have been discarded within 300 km of departure. (iv) In many cases, birds will arrive in habitats seriously different from those they departed, i.e., any seeds carried along will have low chances of surviving in their new site. We suggest that northbound dispersal by endozoochory can only occur during spring if waterbirds feed on seeds that have not been depleted and remained frozen down or buried in sediments, or during moult- or post-moult migrations. Moult migration takes place in summer in phase with the reproductive efforts of the plants. Also epizoochorous dispersal (external attachment) is subject to restrictions i, ii and iv.
To test whether the effects of water oxygen concentration ([O(2)]) on the metabolic interaction between locomotion and digestion differ between fish species with different locomotive and digestive behaviours in normoxia, we investigated the swimming performance of fasted and fed fish at water [O(2)] of 1, 2 and 8 (normoxia) mg L(-1) (2.5, 5 and 20 kPa) at 25°C in three juvenile Cyprinidae fish species: goldfish (Carassius auratus), common carp (Cyprinus carpio) and qingbo (Spinibarbus sinensis). Digestion, taxon and water [O(2)] all had significant effects on the pre-exercise oxygen consumption rate [Formula: see text] and the swimming performance (P < 0.05). Among the three fishes, qingbo showed the highest swimming performance and the lowest feeding [Formula: see text] at the saturated water [O(2)], and its active oxygen consumption rate [Formula: see text] and critical swimming speed (U (crit)) decreased the most with decreases in water [O(2)]. Qingbo exhibited a locomotion-priority metabolic mode at all three water [O(2)]. Digestion was sacrificed to locomotion in a postprandial swimming situation, but fed qingbo could not maintain their U (crit) at water [O(2)] of 2 and 1 mg L(-1). Goldfish showed the lowest swimming performance and the highest feeding [Formula: see text] at the saturated water [O(2)]. They exhibited a digestion-priority metabolic mode at high water [O(2)]. However, with a decrease in water [O(2)], the feeding [Formula: see text] decreased more acutely than the respiratory capacity; thus, digestion and locomotion performed independently in a postprandial swimming situation (i.e., an additive metabolic mode) at a water [O(2)] of 1 mg L(-1). The common carp showed moderate and balanced swimming performance and feeding [Formula: see text] at the saturated water [O(2)], and exhibited an additive metabolic mode at all 3 water [O(2)], because digestion, swimming and respiratory capacities decreased in parallel with the decrease in water [O(2)].
The prevalence of exercise-induced gastrointestinal (GI) symptoms has been reported up to 70%. The pathophysiology largely remains unknown.
To review the physiological and pathophysiological changes of the GI-tract during physical exercise and the management of the most common gastrointestinal symptoms.
Search of the literature published in the English and Dutch languages using the Pubmed database to review the literature that focused on the relation between splanchnic blood flow (SBF), development of ischaemia, postischaemic endotoxinemia and motility.
During physical exercise, the increased activity of the sympathetic nervous system (SNS) redistributes blood flow from the splanchnic organs to the working muscles. With prolonged duration and/or intensity, the SBF may be decreased by 80% or more. Most studies point in the direction of increased SNS-activity as central driving force for reduction in SBF. A severely reduced SBF may frequently cause GI ischaemia. GI-ischaemia combined with reduced vagal activity probably triggers changes in GI-motility and GI absorption derangements. GI-symptoms during physical exercise may be prevented by lowering the exercise intensity, preventing dehydration and avoiding the ingestion of hypertonic fluids.
Literature on the pathophysiology of exercise-induced GI-symptoms is scarce. Increased sympathetic nervous system activity and decreased splanchnic blood flow during physical exercise seems to be the key factor in the pathogenesis of exercise-induced GI-symptoms, and this should be the target for symptom reduction.
• In considering the Origin of Species, it is quite conceivable that a naturalist, reflecting on the mutual affinities of organic beings, on their embryological relations, their geographical distribution, geological succession, and other such facts, might come to the conclusion that each species had not been independently created, but had descended, like varieties, from other species. Nevertheless, such a conclusion, even if well founded, would be unsatisfactory, until it could be shown how the innumerable species inhabiting this world have been modified, so as to acquire that perfection of structure and coadaptation which most justly excites our admiration. Naturalists continually refer to external conditions, such as climate, food, &c, as the only possible cause of variation. In one very limited sense, as we shall hereafter see, this may be true; but it is preposterous to attribute to mere external conditions, the structure, for instance, of the woodpecker, with its feet, tail, beak, and tongue, so admirably adapted to catch insects under the bark of trees. In the case of the misseltoe, which draws its nourishment from certain trees, which has seeds that must be transported by certain birds, and which has flowers with separate sexes absolutely requiring the agency of certain insects to bring pollen from one flower to the other, it is equally preposterous to account for the structure of this parasite, with its relations to several distinct organic beings, by the effects of external conditions, or of habit, or of the volition of the plant itself. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
• In considering the Origin of Species, it is quite conceivable that a naturalist, reflecting on the mutual affinities of organic beings, on their embryological relations, their geographical distribution, geological succession, and other such facts, might come to the conclusion that each species had not been independently created, but had descended, like varieties, from other species. Nevertheless, such a conclusion, even if well founded, would be unsatisfactory, until it could be shown how the innumerable species inhabiting this world have been modified, so as to acquire that perfection of structure and coadaptation which most justly excites our admiration. Naturalists continually refer to external conditions, such as climate, food, &c, as the only possible cause of variation. In one very limited sense, as we shall hereafter see, this may be true; but it is preposterous to attribute to mere external conditions, the structure, for instance, of the woodpecker, with its feet, tail, beak, and tongue, so admirably adapted to catch insects under the bark of trees. In the case of the misseltoe, which draws its nourishment from certain trees, which has seeds that must be transported by certain birds, and which has flowers with separate sexes absolutely requiring the agency of certain insects to bring pollen from one flower to the other, it is equally preposterous to account for the structure of this parasite, with its relations to several distinct organic beings, by the effects of external conditions, or of habit, or of the volition of the plant itself. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Grazing mammals are regarded as major vectors in seed dispersal of grassland plants, through seed ingestion and subsequent excretion (endozoochory). The (evolutionary) ecology underlying this dispersal mode is relatively poorly understood because there are limited data, among others, on how seed attributes perform in this process (and could thus be selected for). For seed mortality following ingestion, contrasting patterns described for the role of simple seed traits seem partly due to inadequate comparative analytical methods. We conducted a feeding experiment in which controlled seed quantities from 48 grassland herb and grass species were fed to cattle. Seed mass, length and shape measurements were related to seed mortality rate using phylogenetically independent contrasts, which account for taxonomic interdependence. The proportion of seeds surviving the digestive tract was generally low, but it reached 100%, with increased germination for some species. Neither seed size nor shape correlated significantly with mortality. Structural traits are likely to overrule these simple seed traits, as illustrated by high survival of species having water-impermeable seeds. As this trait has interesting properties with respect to intraspecific variation and genetics, it could provide opportunities for inference on evolutionary consequences for this type of dispersal.
An examination was performed on 20 healthy men, who had a specific diet, to test the influence of moderate physical activity on bowel transit. During a 3-day pause and a 3-day phase of easy sports activity (jogging), oro-anal transit was measured with the help of radiopaque markers (Hinton method). While the subject was under exertion, the entire weight of stool rose significantly (743 vs. 600 g), whereas we found no significant influence on the oro-anal transit time (39 vs. 48 h) or on stool frequency (1.3 vs. 1.3 per day). Moderate physical activity had no effect on bowel transit time of healthy men under a constant diet. The effect of the so often recommended increase of physical activity on constipation remains to be elucidated.
Ten healthy volunteers (six men and four women, aged 22-41 years) were studied in a crossover trial. The study was divided into three one week periods. During each period the subjects either ran on a treadmill, cycled on a bicycle ergometer, or rested in a chair for 1 hour every day. The exercise was performed at two thirds predicted maximum heart rate (equivalent to 50% VO2 max). The sequences were rotated; no studies were performed in the perimenstrual period. Transit was measured by the method of measuring the excretion of a single dose of radio-opaque markers; all stools were collected, weighed, and x rayed after the ingestion of radio-opaque markers. Dietary fibre and fluid intake were measured on the fourth day of each test period by 24 hour record. Lifestyle was otherwise unchanged. Transit time was dramatically accelerated by moderate exercise (both jogging and cycling); however, stool weight, defecation frequency, dietary fibre intake, and fluid intake did not change significantly. Whole gut transit changed from 51.2 hours (95% confidence intervals 41.9 to 60.5) at rest to 36.6 hours (31.6 to 39.2) when riding and 34.0 hours (28.8 to 39.2) when jogging. Riding and running both differed significantly from resting (p less than 0.01); the difference between riding and running was not significant.
Although exercise is often recommended as therapy for constipation, almost nothing is known of the effects of exercise on rates of movement of material in the gastrointestinal tract. In this study we investigated the influence of mild exercise on transit of a liquid meal from the mouth to the large intestine. Orocecal transit time was determined by a consistent elevation of H2 concentration in a rebreathing apparatus after ingestion of 30 g lactulose; the lactulose was part of a 360-kcal, 350-ml liquid meal. Comparison of transit time was made, in 12 young healthy subjects, between seated rest and a treadmill walk at 5.6 km/h up a 2% grade. The walk elevated heart rate from 64 +/- 4 to 109 +/- 5 beats/min, O2 uptake (VO2) from 0.29 +/- 0.02 to 1.20 +/- 0.07 l/min STPD, and final rectal temperature from 37.0 +/- 0.1 to 38.3 +/- 0.1 degrees C (all P less than 0.01). Exercise speeded transit of the liquid meal, with mean rises in H2 concentration taking place 66 +/- 10 min after ingestion at rest, compared with 44 +/- 6 min after food intake during exercise (P less than 0.02). H2 concentrations in the rebreathing apparatus showed similar base lines in the two experiments, and quantitative increases in H2 concentration, although shifted in time by exercise, were otherwise identical. Subjects with the slowest resting transit rates showed the largest exercise effects (r = 0.79, P less than 0.05). These results indicate that mouth-to-cecum transit of at least the first portion of a liquid meal-based nonabsorbable carbohydrate marker is significantly accelerated during mild exercise.
To examine how moderate exercise affects the blood flow in the gastrointestinal tract.
Twelve miniature swine weighing 38-43 kg were used. All animals were trained on a cardiac exercise treadmill. Blood flow measurements were done on conscious animals using labeled microspheres with a diameter of 16.5 +/- 0.1 (SD) microm. The first flow was measured while the animal was awake and resting, the second flow after 15 min of exercise, the third flow after 30 min of rest.
Flow in the oesophagus at rest was 19.5 +/- 1.3 (SEM) ml/min/100 g. During exercise the flow decreased to 13.3 +/- 1.2 (SEM) ml/min/100 g (ns). After 30 min of rest the flow was 9.9 +/- 1.2 (SEM) ml/min/100 g (p < 0.05 when comparing the flow before and after exercise). Flow in the cardia at rest was 23.1 +/- 1.3 (SEM) ml/min/100 g. During exercise the flow decreased to 14.0 +/- 1.2 (SEM) ml/min/100 g (p < 0.05). After 30 min of rest the flow was 15.0 +/- 1.2 (SEM) ml/min/100 g. Flow in the pylorus at rest was 38.9 +/- 1.1 (SEM) ml/min/100 g. During exercise the flow decreased to 24.6 +/- 1.1 (SEM) ml/min/100 g (p < 0.01). After 30 min of rest the flow was 26.9 +/- 1.2 (SEM) ml/min/100 g. Blood flow in the small and large intestine was mainly unaffected by moderate exercise.
Under moderate exercise, blood flow in the upper part of the gastrointestinal tract declines while it is mainly unaffected in the duodenum, small and large intestine.