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Regurgitation by waterfowl: An overlooked mechanism for long-distance dispersal of wetland plant seeds
... For birds, deliberate regurgitation may be induced for various reasons including for feeding chicks, by allowing adults to carry prey over long distances, removal by predators of indigestible prey remains in pellets, and the removal of seeds from fruit by frugivorous birds in order to accelerate the process of digestion. Of particular importance is that bird regurgitation requires a suffocate movement which is not possible during flight, making this kind of response more likely to occur after landing at a suitable habitat (Kleyheeg and Van Leeuwen, 2015). ...
... Although it remains poorly studied, for waterbirds regurgitation may either occur only an hour or two after a meal in response to overfeeding or not for more than 10 h. Rapid regurgitation will reduce the potential distance for dispersal but will increase the chances of even the most delicate of propagules being 116 successfully transported (Kleyheeg and Van Leeuwen, 2015). Similarly, regurgitation mechanisms in relation to parasites have also received only limited attention, although a small number of studies do provide some important pointers as to the relevance of this mechanism. ...
The last decades have brought important insight and updates in the diagnosis, management and immunopathology of female genital schistosomiasis (FGS) and male genital schistosomiasis (MGS). Despite sharing a common parasitic aetiological agent, FGS and MGS have typically been studied separately. Infection with Schistosoma haematobium manifests with gender-specific clinical manifestations and consequences of infection, albeit having a similar pathogenesis within the human genital tract. Schistosoma haematobium is a known urinary bladder carcinogen, but its potential causative role in other types of neoplasia, such as cervical cancer, is not fully understood. Furthermore, the impact of praziquantel treatment on clinical outcomes remains largely underexplored, as is the interplay of FGS/MGS with relevant reproductive tract infections such as HIV and Human Papillomavirus. In non-endemic settings, travel and immigrant health clinics need better guidance to correctly identify and treat FGS and MGS. Our review outlines the latest advances and remaining knowledge gaps in FGS and MGS research. We aim to pave a way forward to formulate more effective control measures and discuss elimination targets. With a growing community awareness in health practitioners, scientists and epidemiologists, alongside the sufferers from these diseases, we aspire to witness a new generation of young women and men free from the downstream disabling manifestations of disease.
... Endozoochory is the system by which animals disperse seeds through the direct consumption of fruits. The seeds contained in the fruits pass through the digestive tract to subsequently be defecated or regurgitated and dispersed (Cypher & Cypher, 1999;Kleyheeg & van Leeuwen, 2015). In this context, terrestrial mammals such as rabbits (Lezama-Delgado et al., 2016;Malo & Suárez, 1995), foxes (Escribano-Ávila et al., 2014), and even larger herbivores (Campos-Arceiz & Blake, 2011) act as the dispersers of different fruit species. ...
Carnivorous mammals disperse seeds through endozoochory and diploendozoochory. The former consists of ingestion of the fruit, passage through the digestive tract, and expulsion of the seeds, a process that allows scarification and dispersal of the seeds over long or short distances. The latter is typical of predators that expel seeds that were contained in the prey and the effects of which may differ from those of endozoochory with respect to the retention time of the seeds in the tracts, as well as their scarification and viability. The objective of this study was to conduct an experimental evaluation comparing the capacity of each mammal species in terms of the dispersal of Juniperus deppeana seeds and, at the same time, to compare this capacity through the two dispersal systems: endozoochory and diploendozoochory. We measured dispersal capacity using indices of recovery, viability, changes in testas, and retention time of seeds in the digestive tract. Juniperus deppeana fruits were collected in the Sierra Fría Protected Natural Area in Aguascalientes, Mexico, and were administered in the diet of captive mammals: gray fox (Urocyon cinereoargenteus), coati (Nasua narica) and domestic rabbits (Oryctolagus cuniculus). These three mammals represented the endozoochoric dispersers. For the diploendozoochoric treatment, seeds excreted by rabbits were incorporated into the diets of captive mammals: bobcat (Lynx rufus) and cougar (Puma concolor), in a local zoo. Seeds present in the scats were then collected, and recovery rates and retention times were estimated. Viability was estimated by X-ray optical densitometry and testa thicknesses were measured and surfaces checked using scanning electron microscopy. The results showed a recovery of seeds greater than 70% in all the animals. The retention time was <24 h in the endozoochory but longer at 24-96 h in the diploendozoochory (p < .05). Seed viability (x¯ ± SD) was decreased in rabbits (74.0 ± 11.5%), compared to fruits obtained directly from the canopy (89.7 ± 2.0%), while gray fox, coati, bobcat, and cougar did not affect seed viability (p < .05). An increase in the thickness of the testas was also observed in seeds excreted from all mammals (p < .05). Through evaluation, our results suggest that mammalian endozoochory and diploendozoochory contribute to the dispersal of J. deppeana by maintaining viable seeds with adaptive characteristics in the testa to promote forest regeneration and restoration. In particular, feline predators can provide an ecosystem service through scarification and seed dispersal.
... Actually, relatively bigger and softer seeds can be also excreted by regurgitation, which represents another important spreading way in endozoochory. This behavior has been reported especially in birds (Balgooyen & Moe, 1973;Kleyheeg & van Leeuwen, 2015). Even though the most well-known route of endozoochorous seed dispersal by ungulates is faeces, some recent studies conducted on goats (Delibes et al., 2017) and red deer (Castañeda et al., 2018) have revealed that spitting viable seeds from the cud during rumination is also important, at least for the seeds of some plant species. ...
... It could also reflect differences in the amount of food regurgitated by the birds among studies, which would decrease the amount of food assimilated. However, this would mainly concern the mallard, as the northern bobwhite is not prone to regurgitation (Kleyheeg and van Leeuwen, 2015;Malone, 1966;OECD, 2016a). In that respect, the re-estimation of parameter κ x was sufficient to compensate for the differences in food ingestion rates among studies. ...
Mechanistic effect models are increasingly recommended as tools for refining evaluations of risk from exposure to pesticides. In the context of bird and mammal risk assessments, DEB-TKTD models have been recommended for characterizing sublethal effects at lower tiers. However, there are currently no such models. Currently, chronic, multi-generational studies are performed to characterize potential effects of pesticides on avian reproduction, but it is has not been established to what extent results from these studies can inform effect models. Here, a standard Dynamic Energy Budget (DEB) model was extended to account for the avian toxicity endpoints observed in regulatory studies. We linked this new implementation to a toxicological module to capture observed pesticide effects on reproduction via a decreased efficiency of egg production. We analysed ten reproduction studies with five different pesticides conducted with the mallard (Anas platyrhynchos) and the northern bobwhite (Colinus virginianus). The new model implementation accurately distinguished between effects on egg production from direct mechanism of toxicity and from food avoidance. Due to the specific nature of regulatory studies, model applicability for risk refinement is currently limited. We provide suggestions for next steps in model development.
... Specific traits of waterbird species that are known to influence the fate of propagules after ingestion include diet and gut morphology van Leeuwen, van der Velde, van Groenendael, et al., 2012). Some species can regurgitate propagules in pellets (Lovas-Kiss, Sánchez, et al., 2018;Navarro-Ramos et al., 2021) or otherwise (Kleyheeg & van Leeuwen, 2015), allowing larger propagules to disperse even if they cannot survive complete gut passage into faeces. There are complex interactions of propagules with other food ingested simultaneously. ...
1. We review progress in our understanding of the importance of waterbirds as dispersal vectors of other organisms, and identify priorities for further research.
2. Waterbirds are excellent for long-distance dispersal (LDD), whereas other vectors such as fish and mammals disperse similar propagules, but over shorter distances. Empirical studies of internal and external transport by waterbirds have shown that the former mechanism generally is more important. Internal transport is widely recognised for aquatic plants and aquatic invertebrates with resting eggs, but also is important for other organisms (e.g., terrestrial flowering plants not dispersed by frugivores, bryophytes, tardigrades, fish eggs).
3. Waterbird vectors also are important in terrestrial habitats, and provide con-nectivity across terrestrial-aquatic boundaries. There are important differences in the roles of different waterbird species, especially those using different habitats along the aquatic-terrestrial gradient. Early attempts to predict zoochory based on propagule morphology have been found wanting, and more research is needed into how the traits of vectors and vectored organisms (including life history , dormancy and growth traits) explain dispersal interactions. Experimental studies have focused on the potential of propagules to survive internal or external transport, and research into factors determining the establishment success of propagules after dispersal is lacking.
4. Recent spatially explicit models of seed dispersal by waterbirds should be expanded to include invertebrate dispersal, and to compare multiple bird species in the same landscape. Network approaches have been applied to plant-waterbird dispersal interactions, and these are needed for invertebrates. Genetic studies support effective LDD of plants and invertebrates along waterbird flyways, but there remains a lack of examples at a local scale. Next Generation Sequencing and genomics should be applied to waterbird-mediated dispersal across the landscape. More studies of biogeography, community ecology, or population genetics should integrate waterbird movements at the design stage.
... Many pond species possess life cycles and adaptive strategies enabling them to persist across the landscape in the face of disturbance, such as dormant and resistant propagules of aquatic invertebrates and plants (Alderton et al. 2017;Williams et al. 1997), and relatively long lifespans for amphibians and some invertebrates. Efficient dispersal mechanisms by many invertebrates allow rapid recolonization when favorable conditions return including endozoochary (Kleyheeg and van Leeuwen 2015), aerial dispersal (Bilton et al. 2001), and "hitch-hiking" (Okamura et al. 2019). Research focused on the life-history strategies that enable species and communities to persist after a disturbance will be especially valuable to conservation managers as manipulating and facilitating disturbance via active management or passively by rewilding may be key to the survival and protection of many pond species. ...
Ponds are among the most biodiverse and ecologically important freshwater habitats globally and may provide a significant opportunity to mitigate anthropogenic pressures and reverse the decline of aquatic biodiversity. Ponds also provide important contributions to society through the provision of ecosystem services. Despite the ecological and societal importance of ponds, freshwater research, policy, and conservation have historically focused on larger water bodies, with significant gaps remaining in our understanding and conservation of pond ecosystems. In May 2019, pond researchers and practitioners participated in a workshop to tackle several pond ecology, conservation, and management issues. Nine research themes and 30 research questions were identified during and following the workshop to address knowledge gaps around: (1) pond habitat definition; (2) global and long‐term data availability; (3) anthropogenic stressors; (4) aquatic–terrestrial interactions; (5) succession and disturbance; (6) freshwater connectivity; (7) pond monitoring and technological advances; (8) socio‐economic factors; and (9) conservation, management, and policy. Key areas for the future inclusion of ponds in environmental and conservation policy were also discussed. Addressing gaps in our fundamental understanding of pond ecosystems will facilitate more effective research‐led conservation and management of pondscapes, their inclusion in environmental policy, support the sustainability of ecosystem services, and help address many of the global threats driving the decline in freshwater biodiversity.
... (in this case Chara globularis Thuill.) and P. natans is likely due to resurrection of these plants from propagule banks disturbed by the restoration works as these species have long-lived (centennial timescales) oospores (Stobbe et al. 2014) and seeds (Alderton et al. 2017) respectively. It is likely, however, that several species found post-restoration are "new colonists" to the pond, potentially via passive dispersal mechanisms such as wildfowl-based endozoochory (Soons et al. 2008;Green et al. 2016) and regurgitation (Kleyheeg & van Leeuwen 2015). Some ancestral species did not return to Mystery Pit, including the submerged plant M. spicatum and the nationally rare O. fistulosa. ...
The restoration of highly terrestrialized farmland ponds that combines the removal of woody vegetation and pond sediment greatly enhances aquatic biodiversity. Nonetheless, questions remain regarding the historical precedent of pond restoration, and particularly if post‐restoration aquatic macrophyte communities resemble pre‐terrestrialization assemblages. We used a paleoecological approach to address these questions for a typical, recently restored farmland pond in Norfolk, eastern England. Plant and animal remains in pond sediment cores were used to infer decadal‐centennial scale changes to pond communities and to identify past pond management events. We then evaluated the resemblance of restored and historical assemblages by comparisons with contemporary post‐restoration vegetation data. Based on changes in the abundance of terrestrial leaf remains and other indicators (increases followed by declines of aquatic organisms), the study pond appears to have a long history (going back to the early‐1800s) of canopy management (at least three inferred management events), but after the mid‐1970s, steady and substantial increases in terrestrial indicators, suggest cessation of management resulting in uninterrupted terrestrialization. Aquatic macrophyte communities arising after restoration showed some similarities with historical assemblages, but also contained apparently new species. This study demonstrates how paleolimnological methods can improve understanding of pond ecological histories to better inform restoration targets and practices.
... Seeds naturally disperse across wetlands by water, wind, animals (particularly waterbirds), and gravity (Cronk and Fennessy, 2001;Kleyheeg and van Leeuwen, 2015;Reynolds and Cumming, 2016;Soons et al., 2016Soons et al., , 2017. Current restoration techniques that introduce seeds by hand or with machines are designed to overcome dispersal limitations, but do not necessarily mimic these natural dispersal mechanisms. ...
As we approach the Decade of Ecosystem Restoration (2021–2030), there is renewed focus on improving wetland restoration practices to reestablish the habitat and climate mitigation functions and services that wetlands provide. A first step in restoring these functions and services is to reestablish the native vegetation structure and composition through strategic seed-based approaches. These approaches should be driven by ecological, genetic, and evolutionary principles, along with consideration for economics, logistics, and other social constraints. Effective seed-based approaches must consider the chosen species, seed sourcing, dormancy break and germination requirements, seed enhancement technologies, potential invaders, seeding densities, and long-term monitoring. Choice of species should reflect historical plant communities and future environmental conditions, species that support functional goals including invasion resistance, and seed availability constraints. Furthermore, seeds should be sourced to ensure ample genetic diversity to support multifunctionality and evolutionary capacity while also considering the broad natural dispersal of many wetland species. The decision to collect wild seeds or purchase seeds will also impact species choice and genetic diversity, which can have cascading effects for functional goals. To ensure seedling establishment, seed dormancy should be addressed through dormancy breaking treatments and the potentially narrow germination requirements of some species will require targeted sowing timing and location to align with safe sites. Other seed enhancements such as priming and coatings are poorly developed for wetland restoration and their potential for improving establishment is unknown. Because wetlands are highly invasion prone, potential invaders and their legacies should be addressed. Seeding densities should strike a balance between outcompeting invaders and preserving valuable seed resources. Invader control and long-term monitoring is key to improving revegetation and restoration. Here, we review scientific advances to improve revegetation outcomes, and provide methods and recommendations to help achieve the desired goals. Gaps in knowledge about seed-based wetland restoration currently exist, however, and untested practices will certainly increase risks in future efforts. These efforts can be used to better understand the ecological, genetic, and evolutionary processes related to wetland seeds, which will bring us one step closer to seed-based restoration of functions and services needed for human and ecological communities.
... He also claimed that experiments conducted by Hesse (1924) revealed that the spawn of some anurans can remain out of the water for up to four days without losing their capacity for development. Kleyheeg and van Leeuwen (2015) studied the potential of regurgitation by birds as means of seed dispersal and suggested that, if regurgitation occurs only a few hours after ingestion, it could also facilitate dispersal of less resistant organisms, such as -in this case -fish eggs. Fahr (1993) and Measey et al. (2007) discussed bird carriage as a mechanism by which amphibians may have colonized the Gulf of Guinea islands. ...
Although the distribution patterns of major amphibian lineages are mainly explained by a Pangean origin with subsequent vicariant diversification, dispersal events have exerted a strong influence on present-day distributions. Long-distance dispersal (LDD) involves movements outside the standard geographic limits and outside the genetic neighbourhood area of individuals. Although considered ‘rare’, LDD is disproportionately important to amphibian populations, species and communities. To understand the role of LDD in shaping current biogeographic patterns in these tetrapods, we reviewed the cases reported in the literature. A systematic bibliographic search was performed to obtain information on how many studies have dealt with LDD in amphibians, which methods they used, which taxa and distances were involved, and when/where events had apparently occurred. In 41 studies, we recovered at least 90 LDD events (3 active, 87 passive) involving at least 56 extant species and 38 genera. Most events (73) involved the colonization of islands, with rafting being suggested as the most conceivable means of overwater passive dispersal for these vertebrates. In this review, we show that LDD events have played an important role in shaping current amphibian biogeographic patterns, especially the occurrence of disjunct distributions and the colonization of islands.
... In addition, the type of food ingested with the propagules can strongly influence the rate of passage through the digestive tract (Malone, 1965), and very short gut passage time might be expected if a predator is affected by some disease influencing the digestion processes. Furthermore, various waterbirds more or less regularly regurgitate their food (e.g., Kleyheeg & van Leeuwen, 2015;Proctor, 1968), which is a mechanism contributing to dispersal of aquatic plants and invertebrates. If a crayfish predator regurgitates, the prey pieces may spend substantially shorter time in its body than when passing through the whole digestive tract. ...
The crayfish plague pathogen (Aphanomyces astaci) can be transmitted through the digestive system of fish, but its dispersal through mammalian and bird digestive tracts has been considered unlikely, and direct experimental evidence remains scarce. We present a small‐scale transmission experiment with European otter and American mink fed with infected crayfish, and experiments testing survival of cultures of five A. astaci strains at temperatures corresponding to those inside mammal and bird bodies. The pathogen was neither isolated from predator excrements nor transmitted to susceptible crayfish exposed to excrements. In agar‐based artificial media, it occasionally survived for 15 min at 40.5°C and for 45 min at 37.5°C, but not so when incubated at those temperatures for 45 min and 75 min, respectively. The five tested strains differed in resistance to high temperatures, two (of genotype groups E and D) being more susceptible than other three (of groups A, B and D). Their survival to some extent varied when exposed to the same temperature after several weeks or months, suggesting that some yet‐unknown factors may influence A. astaci resistance to temperature stress. Overall, we support the notion that passage through the digestive tract of warm‐blooded predators makes A. astaci transmission unlikely.
... Van Leeuwen et al. (2012) provide a review of macroinvertebrate and macrophyte species transported by waterbirds via their faecal droppings, and although crustacean, insect, molluscan and bryozoan species were all recorded, no chelicerates were found. In a more recent study that focuses on the dispersal of wetland plant seeds, Kleyheeg and van Leeuwen (2015) highlight regurgitation as an overlooked dispersal mechanism. Given that this event can happen within a few hours, regurgitated organisms may potentially remain viable. ...
New findings of organismal dispersal by other organisms can help explain the distribution of species to remote places. In this work, I describe a male and a female of a new water mite species of the genus Arrenurus that were found in the crop of an Anas flavirostris duck near Cochabamba, Bolivia. Both specimens were complete; however, it is unknown if they were alive and, thus, potentially viable at the time of collection. This study also represents the first reported finding of water mites in a bird crop.
... We also consider whether the distributions of the dispersed plant species are consistent with LDD events that shorebirds are likely to provide, and whether current literature provides evidence that they are dispersed by other animal vectors. We also consider differences in seed size and quantity between pellets and faeces, since dispersal kernels and the potential for LDD are likely to differ between these forms of excreta (Proctor 1968, and regurgitation may be more likely for larger seeds (Kleyheeg and van Leeuwen, 2015). Finally, we explored potential seasonal differences between spring and autumn migration in the number of seeds in excreta, as this will influence the directionality of LDD events. ...
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.
... However, ectozoochory has been the topic of fewer studies, and its role has possibly been underestimated. Dispersal modes that are less commonly considered are regurgitation of intact propagules (Kleyheeg & van Leeuwen 2015) and propagules taken up as nest building materials (Dean, Milton & Siegfried 1990;Kristiansen 1996). ...
The White-headed Duck is a stifftail with a highly fragmented distribution in the central and southwestern Palearctic, from south of Lake Baikal in the east, to northwestern Africa and the Iberian Peninsula in the west. Populations in north-central Asia are migratory, and spend the winter in the Middle East, Türkiye, and southeastern Europe. There are sedentary populations in Spain and northwestern Africa. This charismatic bird is used as a flagship for wetland conservation in several countries in its range, and reintroductions have been attempted in Hungary, Italy, France, and Mallorca Island (Balearic Islands, Spain).
It is a highly aquatic species that is found in a variety of wetlands throughout the year, including natural and man-made habitats, and they exhibit seasonal variations in habitat use. The bulbous base of the bill contains large salt-excreting glands, which are considered an adaptation to brackish and saline habitats. It breeds in a variety of wetlands, including freshwater, brackish, alkaline, and eutrophic lakes with emergent vegetation used for nesting. Wintering sites generally have a larger surface area and lower cover of emergent vegetation compared to breeding sites, and include saline lakes in regions where freshwater ones freeze. The White-headed Duck shows adaptations for diving and the main food sources of adults and immatures are midge larvae (Diptera, Chironomidae) and seeds of aquatic plants.
The mating system of the White-headed Duck is characterized as male-dominance polygyny, in which males compete for females by sorting out positions of dominance. Courtship behaviors are increasingly intense, from relaxed flotilla-swimming to head–high–tail–cock, sideways hunch, kick–flap, and side–ways–piping. During the early breeding season, the males move to open water close to emergent vegetation selected for nesting. In these areas, fighting between males is common and dominance hierarchies are established. First breeding takes place when females are two years old. Females nest over water and their eggs are very large in relation to female size, which may be related to semi-parasitic nesting or to highly precocial ducklings that are tended by the female only for 1–3 weeks.
Considered globally Endangered, it is extinct as a breeder in Europe with the exception of Spain. It has undergone an estimated decline in numbers of 34.4% between 2005 and 2013, and is threatened by competition and hybridization with the introduced Ruddy Duck (Oxyura jamaicensis), habitat alteration, drainage, droughts, and competition with introduced populations of common carp (Cyprinus carpio) and other cyprinids. Other important threats are hunting, ingestion of lead shot, and drowning in fishing–nets.
There are numerous aspects of the natural history of White-headed Duck that are poorly known. The breeding success of males has not been analyzed by means of genetic studies of paternity. Another aspect that remains unstudied is mate selection by females. There are few data about parasitic nesting. Genetic studies of nest maternity would be important to understand nest parasitism. Studies on the effects of both parental and creching behavior on chick survival are needed. Future studies on dispersal and adult survival would be helpful. Migratory routes, stopover sites and destinations are not well-known, and more information is needed. Data on population sizes of this species are inadequate and coordinated censuses are required. The role of White-headed Duck as a dispersal vector for aquatic plants and invertebrates has not been studied.
Knowledge of the White-headed Duck was improved by the work of Amat and Sánchez (2) and the comparative studies of stifftail ducks made in captivity by Montserrat Carbonell (3), largely overlooked until their publication (4).
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.
The passive dispersal of non-mobile organisms by vertebrates (zoochory) is a common mechanism used to explain their often widespread distribution. Transport occurs either internally via the vertebrate digestive tract (endozoochory), or externally be adhering to skin, feathers or fur (ectozoochory), and its success is due to both physiological and ecological factors associated with the disseminating ‘hosting’ animal.
Helminth eggs and larvae are generally non-mobile stages that are largely dependent on the movement of another animal, typically a host, for geographical dissemination. Studies on the zoochory of helminths by vertebrates are extensive and particularly long-standing, stretching back to the 19th century, although this literature is often overlooked when considering the biogeography of parasites. This review assesses the potential of helminths to be dispersed passively by zoochory examining evidence from both laboratory and field studies. The physiological dynamics of the vertebrate intestines and skin surface as hostile environments, as well as the characteristics of eggs and larvae which may facilitate successful transport are evaluated. The various mechanisms of helminth endo- and ectozoochory are presented and the likelihood of long-distance dispersal determined. It is concluded that zoochory is a potentially important means of disseminating parasites.
Seagrass ecosystems exist throughout Pacific Island Countries and Territories (PICTs). Despite this area covering nearly 8% of the global ocean, information on seagrass distribution, biogeography, and status remains largely absent from the scientific literature. We confirm 16 seagrass species occur across 17 of the 22 PICTs with the highest number in Melanesia, followed by Micronesia and Polynesia respectively. The greatest diversity of seagrass occurs in Papua New Guinea (13 species), and attenuates eastward across the Pacific to two species in French Polynesia. We conservatively estimate seagrass extent to be 1446.2 km², with the greatest extent (84%) in Melanesia. We find seagrass condition in 65% of PICTs increasing or displaying no discernible trend since records began. Marine conservation across the region overwhelmingly focuses on coral reefs, with seagrass ecosystems marginalised in conservation legislation and policy. Traditional knowledge is playing a greater role in managing local seagrass resources and these approaches are having greater success than contemporary conservation approaches. In a world where the future of seagrass ecosystems is looking progressively dire, the Pacific Islands appears as a global bright spot, where pressures remain relatively low and seagrass more resilient.
Seagrass ecosystems provide critical contributions (goods and perceived benefits or detriments) for the livelihoods and wellbeing of Pacific Islander peoples. Through in-depth examination of the contributions provided by seagrass ecosystems across the Pacific Island Countries and Territories (PICTs), we find a greater quantity in the Near Oceania (New Guinea, the Bismarck Archipelago and the Solomon Islands) and western Micronesian (Palau and Northern Marianas) regions; indicating a stronger coupling between human society and seagrass ecosystems. We also find many non-material contributions historically have been overlooked and under-appreciated by decision-makers. Closer cultural connections likely motivate guardianship of seagrass ecosystems by Pacific communities to mitigate local anthropogenic pressures. Regional comparisons also shed light on general and specific aspects of the importance of seagrass ecosystems to Pacific Islanders, which are critical for forming evidence-based policy and management to ensure the long-term resilience of seagrass ecosystems and the contributions they provide.
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.
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.
Dabbling ducks are important quarry species, and as a result, they are relatively well studied. Over the last century, considerable effort has been made to describe their diet and food requirements. In this review, we compile present knowledge about the diet of four widespread dabbling ducks (wigeon, pintail, mallard and teal) in the Western Palearctic. Previous diet research has a spatio-temporal bias towards autumn/winter and the western parts of Europe. The limited number of studies from the breeding season reveals an increase in invertebrates in the diet compared to other seasons, but with some differences between adults and ducklings. Adult ducks eat a larger proportion of benthic invertebrates, whereas ducklings feed relatively more on emerging invertebrates. The most important plant species (seeds) based on frequency occurrence was found to vary with a geographic gradient. Carex spp., Hordeum vulgare and Hippuris vulgaris are common in the diet of birds at northern latitudes, whereas taxa such as Oryza sativa, Potamogeton pectinatus and Scirpus spp. are common in the south. The reviewed studies are based on the contents of different parts of the digestive system and on a variety of methods to quantify food items. The variations in sampling techniques and shortage of articles from the breeding season and some geographic regions highlight the need for future studies. In the future, it is important to standardize sampling techniques to improve the possibility to compare studies and to obtain a more representative view of the diet of dabbling ducks in Europe.
Whether a bird handles a fruit by crushing it with its bill or simply swallowing it whole has important ramifications for both the dispersal success of the plant and the feeding behavior of the bird. In cage experiments, birds that crushed fruits in their bills ("mashers") usually dropped many seeds without ingesting them. Large seeds were dropped more frequently than small seeds. The proportion of seeds dropped by five tanager species correlated negatively with their body weight. Birds that swallowed fruits whole ("gulpers") did not drop seeds before swallowing fruits. Gulpers regurgitated large seeds and defecated small seeds. Median regurgitation time was less than median defecation time. Gulpers had lower ingestion rates than mashers, probably because mashers did not ingest many seeds. Mashers spent more time than gulpers in handling fruits. Mashers may also be less restricted than gulpers of equivalent size in the sizes of fruits they can take. Plants may respond evolutionarily to the differences in the seed-dispersal probability of mashers and gulpers through different fruit presentation methods, shifted fruiting seasons, seed size, and pericarp texture.
Prey remains and regurgitated pellets collected from nests are the most common material for investigating the diet of birds of prey. Generally such data is thought to be biased with large prey overrepresented. However, there is no analysis investigating how systematic the error is in relation to prey size, abundance, species or method used. In this study we compared the diet composition of the Goshawk (Accipiter gentilis) and the Buzzards (the Common Buzzard Buteo buteo and the Rough-legged Buzzard B. lagopus) in northern Finland obtained indirectly (by collection of prey remains and pellets) and by direct methods (using a movie camera and a video recording system). In order to investigate the relationship between these two types of diet data more generally, we combined our own material and some published original data. Video and film images allowed us to identify according to class or family level most of the prey items delivered to the nests during the surveillance sessions, but identification according to genus or species level often was difficult. We found that small prey items were underestimated in remains as compared to large prey items. However, when none of the prey delivered to the nest is in large numbers, prey remains give fairly reliable idea of the real diet.
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.
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.
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.
Capsule: Redshank diet from southern Europe during migration shows spatial and seasonal variations. Aims: To assess seasonal variation in Redshank diet at a major passage site, and to compare data derived from analysing pellets or faeces. Methods: At the Odiel Marshes in 2001, pellets from spring migration (39), autumn migration (121) and midwinter (15) were analysed, together with faecal samples from autumn (84). Results: The abundance of different invertebrate groups in pellets varied between seasons. In spring, Chironomus salinarius pupae and larvae dominated by volume, followed by Ephydridae larvae and the beetle Paracymus aenus. Polychaetes and molluscs dominated in autumn, and isopods in midwinter. In autumn, chironomid larvae, Mesembryanthemum nodiflorum seeds and Artemia cysts were relatively more abundant in faeces, whereas polychaetes, isopods, molluscs and cestode cysticercoids were more abundant in pellets. Harder and/or larger items were thus relatively more abundant in pellets than faeces. Pellet analysis gave more emphasis to mudflat prey, and faeces to saltpan prey. Conclusion: Pellet and faecal analysis give different results for wader diet, and it is useful to combine the two methods. However, they show significant correlations both in diet range and rank abundance of prey items. Redshank diet shows much seasonal and spatial variation in southern Europe.
In Central Europe, many plant populations are patchily distributed in human‐modified landscapes and depend on animal vectors for seed dispersal. To predict seed‐dispersal distances and locations of seeds of wild cherry trees ( Prunus avium L.) in forest and farmland habitats in a human‐modified landscape, we integrate movement data and seed regurgitation times of the Common Blackbird ( Turdus merula L.) in a simulation model.
We performed feeding trials with Common Blackbirds and wild cherries to determine the distribution of regurgitation times. We captured 32 male blackbirds and equipped them with radio tags to follow their movements in forest and farmland habitats. To simulate the movement of cherry seeds through the landscape, we combined the distribution of regurgitation times with bird movement data and modelled seed‐dispersal distances and locations of seed deposition for forest and farmland birds.
According to our simulations, more cherry seeds were deposited under foraging trees in farmland (20.8%) than in forest populations (9.5%). Median seed‐dispersal distances (50.8 vs. 68.2 m) and the proportion of long‐distance dispersal events (distances > 100 m) were predicted to be lower in farmland (14.9%) than in forest populations (28.2%).
In the model, forest‐dwelling blackbirds dispersed more cherry seeds into suitable habitat (98.7%) than farmland blackbirds (85.4%). In both habitats, seed deposition in suitable habitat was much higher than expected from the proportion of suitable habitat within blackbirds' home ranges, indicating directed dispersal.
To test whether differences in seed‐dispersal locations were related to recruitment success, we recorded seedling densities in farmland and forest populations of P. avium and determined survival probabilities of seedlings. Seedling densities and survival were much lower in farmland than in forest populations, even accounting for strong environmental effects on seedling recruitment.
Synthesis : Our findings show that behavioural differences of animal seed dispersers between habitat types can result in substantial changes in seed‐dispersal distances and locations in human‐modified habitats. These changes in seed‐dispersal services for bird‐dispersed plant species may be related to reduced seedling recruitment in farmland populations making such populations prone to extinction in the long term.
This is the second edition of a multi-author book first published in 1992. It deals with all aspects of plant regeneration by seeds, including reproductive allocation, seed dispersal and predation, longevity, dormancy and germination. All chapters have been updated, and four new chapters added on seed size, seedling establishment, the role of gaps, and regeneration from seed after fire.
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 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.
Waders (Charadriiformes) undergo particularly long migratory flights, making them ideal vectors for long-distance dispersal. We present a study of dispersal of plant seeds by migratory waders in the Odiel saltworks in south-west Spain. This is the first field study to demonstrate excretion of viable seeds by waders. Viable seeds of Mesembryanthemum nodiflorum (Aizoaceae), Sonchus oleraceus (Asteraceae) and Arthrocnemum macrostachyum (Chenopodiaceae) were frequent in pellets and faeces of redshank Tringa totanus, spotted redshank Tringa erythropus, and black-tailed godwit Limosa limosa during spring and autumn migrations, but less frequent during winter. Another 11 seed types were recorded at low density. More intact M. nodiflorum seeds were present in redshank faeces than in their pellets, but seeds extracted from pellets were more likely to germinate. More S. oleraceus seeds were transported per redshank pellet in spring, but more redshank migrated through the area in autumn. The distributions of the plants transported are consistent with an important role for long-distance dispersal by waders. M. nodiflorum and S. oleraceus are introduced weeds in the Americas and Australasia, and dispersal by birds may contribute to their rapid spread. Although S. oleraceus is generally thought to be wind-dispersed, birds may be responsible for longer distance dispersal events.
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.
Many plant seeds and invertebrates can survive passage through the digestive system of birds, which may lead to long distance dispersal (endozoochory) in case of prolonged retention by moving vectors. Endozoochorous dispersal by waterbirds has nowadays been documented for many aquatic plant seeds, algae and dormant life stages of aquatic invertebrates. Anecdotal information indicates that endozoochory is also possible for fully functional, active aquatic organisms, a phenomenon that we here address experimentally using aquatic snails. We fed four species of aquatic snails to mallards (Anas platyrhynchos), and monitored snail retrieval and survival over time. One of the snail species tested was found to survive passage through the digestive tract of mallards as fully functional adults. Hydrobia (Peringia) ulvae survived up to five hours in the digestive tract. This suggests a maximum potential transport distance of up to 300 km may be possible if these snails are taken by flying birds, although the actual dispersal distance greatly depends on additional factors such as the behavior of the vectors. We put forward that more organisms that acquired traits for survival in stochastic environments such as wetlands, but not specifically adapted for endozoochory, may be sufficiently equipped to successfully pass a bird's digestive system. This may be explained by a digestive trade-off in birds, which maximize their net energy intake rate rather than digestive efficiency, since higher efficiency comes with the cost of prolonged retention times and hence reduces food intake. The resulting lower digestive efficiency allows species like aquatic snails, and potentially other fully functional organisms without obvious dispersal adaptations, to be transported internally. Adopting this view, endozoochorous dispersal may be more common than up to now thought.
Barrett, R. T., Camphuysen, C. J., Anker-Nilssen, T., Chardine, J. W., Furness, R. W., Garthe, S., Hüppop, O., Leopold, M.
F., Montevecchi, W. A., and Veit, R. R. 2007. Diet studies of seabirds: a review and recommendations. – ICES Journal of Marine
Science, 64.
We review the different methods that are used to collect dietary data from marine birds. We consider their limitations and
practicalities and emphasize critical data gaps in our knowledge of the feeding ecology of seabirds (na mely diets outside
breeding seasons). To enhance comparability of findings among studies, species, and oceanographic regions, we make recommendations
on standards for the reporting of results in the literature.
IN 41 bird species of mediterranean scrublands of S Spain, seed dispersers (feeding on whole fruits and voiding seeds unharmed) are indistinguishable from nonfrugivores and fruit predators (feeding on pulp or seeds and not performing dispersal) in the ratio of gizzard mass, liver mass, and intestine length to body mass, but differ significantly in bill morphology and average gut passage time (GPT). Seed dispersers tend to be flatter and broader billed than other groups, and have a wider mouth relative to bill width. GPT of seed dispersers is signficantly shorter than that of other groups. Morphological correlates of seed dispersers suggest that adaptations for insectivory serve as preadaptations for feeding on whole fruits. Shorter GPT's, in contrast, appear to be an adaptation indispensable to sustained, intense frugivory. seasonal frugivory imposes limits on commitments to permanent structural modifications, and more subtle functional adaptations of seed dispersers to plants are as relevant as the more conspicuous structural adaptations reported for year-round frugivores.-from Author
Although winter foods of mallards (Anas platyrhynchos) have been documented in several studies, the importance of ecological or biological factors on the consumption of specific food groups often was ignored. Consequently, we evaluated whether age, pair status, molt status, habitat, year, or season influenced foods consumed by male mallards in southeastern Missouri during winters 1983-86. Seeds of moist-soil plants composed 61.4 and 46.0% of the aggregate dry mass diet of ducks collected in 1983-84 and 1984-85. Agricultural grain made up 33.8% of the aggregate dry mass diet in 1984-85, and acorns accounted for 64.5% of the diet in 1985-86. Our analysis revealed that habitat where birds were collected (P < 0.01) and annual variation (P < 0.01) were predominate factors influencing male mallard diet during winter. We attribute annual differences in food consumption primarily to annual variation in mast production. Invertebrates were present in 82% of 156 food samples, but composed only 7.3% dry mass of all ducks collected. Invertebrate consumption was greater during mid-winter than during other portions of winter (P < 0.01), probably a result of population growth and life history strategies of invertebrate species. Consumption of food groups did not differ among adult and immature males (P = 0.75), paired and unpaired males (P = 0.15), or males of different molt status (P = 0.22). These results suggest that age and physiological factors are less important than environmental factors in determining food use by male mallards during winter. Providing a diversity of habitats and suitable foods may be the best management approach to compensate for annual variation in availability of individual food resources.
I report on handling methods and efficiencies of 26 species of Paraguayan birds feeding on fruits of Allophyllus edulis (Sapindaceae). A bird may swallow fruits whole (Type I: pluck and swallow feeders), hold a fruit and cut the pulp from the seed with the edge of the bill, swallowing the pulp but not the seed (Type II: cut or mash feeders), or take bites of pulp from a fruit that hangs from the tree or that is held and manipulated against a branch (Type III: push and bite feeders). In terms of absolute amount of pulp obtained from a fruit, and amount obtained per unit time, Type I species are far more efficient than Type II and III species. Bill morphology influences feeding methods but is not the only important factor. Diet breadth does not appear to be significant. Consideration of feeding efficiency relative to the needs of the birds indicates that these species need to spend relatively little time feeding to meet their estimated energetic needs, and that handling time has a relatively trivial effect on the time/energy budgets of the bird species observed.
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.
I/~.\tr.ac.t. Morphological and digestive correlates of seed dispersal were investigated in 41 bird species of mediterranean scrublands of southern Spain. Seed dispersers (feeding on whole fruits and voiding seeds unharmed) are indistinguishable from nonfrugivores and frult predators (feedlng on pulp or seeds and not performing dispersal) in the ratlo of glzzard mass. liver mass. and intestine length to body mass. but direr significantly in bill morphology and average gut passage time (GPT). Seed dispersers tend to be flatter and broader billed than other groups. and have a wider mouth relative to bill wldth. GPT of seed dispersers is significantly shorter than that of other groups. Morphological correlates of seed dispersers suggest that adaptatlons for insectivory serve as preadaptations for feeding on whole fru~ts. Shorter GPT's, in contrast. appear to be an adaptation indispensable to sustained. intense frugibory. Seasonal frugivon imposes limlts on commitments to permanent structural mod- ifications. and more subtle functional adaptatlons are to be expected. In the context of plant-disperser coevolution. unapparent adaptations ofseed dispersers to plants are as relevant as the more conspicuous structural adaptations reported for year-round fruglvores. In mediterranean scrublands they suffice to maintain a hlgh-efficiency seed dispersal system.
Data gathered on 70 bird species and 171 plant species in the lower montane forests of Monteverde, Costa Rica, suggest that fruit-eating birds face many of the constraints imposed on other gape-limited foragers, but have an unusual minimum-size relationship with their food because of the unique characteristics of fruits. Fruit-eating birds with broad gapes consumed more lauraceous fruit species and a larger mean and maximum size of fruits overall than narrow-gaped birds, but size of the smallest fruits eaten was not correlated with gape width; large-gaped species commonly fed on diminutive fruits. Birds effectively selected among individual fruits within a tree on the basis of fruit size, dropping bulky fruits beneath the tree. Effective size selectivity also occurred among trees of different species in the same family and among plant species in various families. The diet of broad-gaped birds was not composed differentially of large fruit species. Plants with large fruits attracted fewer species of birds than plants with small fruits. The broad-gaped bird species on which large-fruited plants specialized were those with the most generalized diets. -from Author
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.
1. Visual fields were determined in two species of dabbling ducks (Anatini): Shoveler Anas clypeata L. (planktivore whose foraging is guided mainly by tactile cues) and Wigeon A. penelope L. (herbivore whose foraging is guided mainly by visual cues).
2. The binocular fields of Shoveler and Wigeon are of similar maximum width (20°), but they differ in their position and vertical extent. The bill of the Shoveler lies in the very periphery of its frontal binocular field, which extends through 220° thus providing comprehensive visual coverage about the head. In Wigeon the bill is positioned more centrally in the frontal binocular field, which extends through 150° and results in the birds having a narrow blind area behind the head.
3. The vigilance behaviour of Shoveler and Wigeon when foraging simultaneously was studied using a focal observation procedure at sites where the two species winter in sympatry. Focal Wigeon almost only fed by grazing. Only Shoveler feeding by dabbling (filtering the first centimetres of water) were used in the analyses. Wigeon spent significantly more time in head-up vigilance than Shoveler (F1,75 = 14·70, P = 0·0003).
4. It is proposed that this interspecific difference in the proportion of time spent in vigilance behaviour may be an adaptive response to differences in the visual field topography of these species, particularly with respect to the presence/absence of a blind area to the rear of the head.
5. The ability of foragers to combine part of their vigilance behaviour with head-down feeding has recently been recognized as influencing the trade-offs related to vigilance while foraging. This study shows that this ability may vary significantly between species, even within the same genus, and that these variations are likely to be due to contrasted visual fields, themselves related to the type of feeding techniques employed by the different duck species.
1. Retention times of food in stomachs of breeding and non-breeding African pengiuns (Spheniscus demersus) were examined. 2. Rates of gastric emptying in non-breeding birds were linearly related to the mass of food in the stomach. 3. Breeding birds returned to the nest with more food in their stomachs when chicks were larger. The rate of regurgitation of food was linearly related to chick mass. 4. Retention times of food in the stomachs of breeding penguins can only be explain by cognisance of observed regurgitation rates and by assuming that there is no gastric emptying through the pyloric sphincter.
Viable seeds of Celtis , Convolvulus , Malva , and Rhus were regurgitated from the digestive tract of killdeer ( Charadrius vociferus ) after 160, 144, 152, and 340 hours, respectively; seeds were recovered in the same way, after long-time retention, from least sandpipers ( Erolia minutilla ). Most other birds do not retain seeds as long. There is evidence that seeds of many species can remain viable in the intestinal tract of some shorebirds long enough to be transported several thousand miles.
Seeds: The Ecology of Regeneration in Plant Communities. Cabi publishers
- P Jordano
Jordano, P., 2000. Fruits and frugivory. In: Fenner, M. (Ed.), Seeds: The Ecology of
Regeneration in Plant Communities. Cabi publishers, Wallingford, UK, pp.
125-166.