3 Seed dispersal and plant-animal interactions

3.1 Directed endozoochory: a hitchhiker’s guide for clonal ericaceous plants to successful sexual reproduction

Arnberg, M.1; Eycott, A. E.1; Larsen, O.1; Bruun, L,1; Steyaert, S.1

1Nord University, Norway

Many plant populations are both seed and microsite limited. Microsites are often spatially unpredictable and if they are also short-lived, they are called Recruitment Windows of Opportunity (RWO). Sexual reproduction then depends on the arrival of enough seeds at the right time. When endozoochorous dispersal vector behaviour helps seeds reach such suitable microsites, this is known as directed dispersal and can be distinctly advantageous. Vaccinium species are clonal, berry-producing ericaceous species for which both seed-supply and microsite limitation have been demonstrated, despite the fact that they produce copious amounts of berries. Seedlings must have suitable abiotic conditions for growth but also avoid competition from the standing vegetation. We hypothesized that directed endozoochorous seed dispersal by birds towards decomposing stumps facilitates seedling recruitment in Vaccinium species which utilize RWOs for their sexual reproduction. We tested this in a boreal forest ecosystem where Vaccinium dominates the forest floor. Bird scats and seedlings were both more likely to occur on stumps than on the forest floor. Scats contained viable Vaccinium seeds. Not all stumps were used by birds nor were they equally effective as recruitment windows, highlighting the dependence of seeds arriving at the right stump at the right time. Scats were more common in forest with heterogeneous vertical structure and on stumps with moderate amounts of bare wood. Seedlings were more likely on larger stumps with established bryophytes or alternatively on smaller stumps with available bare wood. Directed endozoochory appears to be a vital component in the life cycle of berry-producing ericaceous plants. Bird-mediated dispersal towards decomposing stumps allows ericaceous plants to arrive at spatially unpredictable microsites within the temporal window of suitable conditions. Seedling establishment and distribution is thus related as much to the activity of endozoochorous dispersers (i.e. getting to the right place) as it is to microsite availability.

3.2 Climate and microhabitat effects on the importance of endozoochory along an elevational gradient in southern Ecuador

Acosta-Rojas, D.C.1,2, Barzcyk, M.1,2, Espinosa, C.I.3, Neuschulz, E.1, Schleuning, M.1

1Senckenberg Biodiversity and Climate Research Center, Germany; 2Goethe Universität, Germany; 3Technical University of Loja, Ecuador

Seed dispersal is a key process shaping the distribution of plant species. Particularly in tropical rainforests, endozoochory, the dispersal of seeds by frugivores, is the most dominant mode of seed dispersal. Understanding how abiotic factors shape the degree of endozoochory in tree communities is, however, largely understudied. Here, we investigated the effects of elevation, climate and microhabitat conditions on seed dispersal modes of plant communities located along an elevational gradient in the tropical Andes in southern Ecuador. Over one year, we quantitatively measured seed rain with 162 seed traps on nine 1-ha forest plots located at 1000 m, 2000 m, and 3000 m asl. We also recorded climatic conditions (i.e., temperature, rainfall) and microhabitat conditions (i.e., leaf area index, soil moisture, soil properties) to test how abiotic factors influence the dominance of endozoochory in the tree community. We recorded around 330,000 seeds belonging to 329 plant species. An average of 82.1% of species in the community was endozoochorous while 17.9% had other seed dispersal modes. Elevation had significant effects on the proportion of endozoochory in the tree community. Variation in the biomass of endozoochorous seeds was associated with variation in rainfall. In turn, the number of endozoochorous plant species decreased with decreasing temperature and simpler canopy structure (i.e., low leaf area index). Our analyses suggest that changes in climatic conditions and canopy structure may potentially alter the dispersal modes in plant communities and thus, the distribution of plant species in these mountains.

3.3 Role of seed dispersal by animals on secondary succession in Cantabrian mountains: implications for rewilding and forest restoration.

García, D.1

1University of Oviedo, Spain

Rewilding of Cantabrian montane forests involves the recolonization of open anthropogenic habitats (pastures with variable cover of rocks and shrubs) by tree species. This ecological succession process depends, at a large extent, on the dispersal of tree seeds by wild vertebrates and on the facilitation of tree seedling recruitment by shrubs. Frugivorous birds (thrushes, warblers and jays) and mammals (carnivores) establish, through seed dispersal, the early template of forest regeneration at the landscape scale. Animal diversity impacts positively in the magnitude of seed dispersal service, due to the between-species trophic and spatial complementarity that leads to the deposition of different seed species on different sites across the landscape. Forest loss and fragmentation condition largely the activity of seed dispersers, hampering seed deposition in deforested areas. Nevertheless, the occurrence of isolated remnant trees within pastures buffers this dispersal limitation, by anchoring seed dispersers and promoting nucleation foci for recruitment. When established under shrubs, tree seedlings and saplings frequently avoid browsing and trampling by cattle and wild ungulates, overcoming the regeneration bottleneck. Rewilding of Cantabrian montane forests depends, thus, on three functional components: (1) remnant forest patches, by acting as seed sources; (2) isolated trees and shrubs in pastures, by nucleating seedling establishment and fostering long-term recruitment; and (3) animal seed dispersers, by moving seeds from source areas to deforested habitats. The interconnection between these three components represents, therefore, a systemic mechanism of resilience which should be considered a tool of passive restoration of Cantabrian forests.

3.4 Are large vertebrates redundant in seed dispersal functions and dung beetle attraction in the Atlantic forest?

Fuzessy, L.1,2, Culot, L.2

1Center for Ecological Research and Forestry Applications, Spain; 2São Paulo State University, Brazil

Understanding the extent to which vertebrates play equivalent roles within communities, known as functional redundancy, is underlying to estimate the potential to offset ecological functions previously played by a disappearing species. The services provided by threatened species are broad, and include forest regeneration through primary seed dispersal processes, and also the influence on secondary seed dispersal by defining associations with invertebrates, such as dung beetles, with their feces. Based on the potential of megafrugivores to overlap in functions, we present a snapshot of a complex of tri-trophic interacting partners within a conserved scenario of the Brazilian Atlantic forest (AF). Using empirical field observations of seed dispersal by vertebrates and dung beetles attracted to their feces, we present the first documented food web encompassing plants, vertebrates and dung beetles. We (a) described patterns of interactions among plants and three large fruit-consuming vertebrates still inhabiting conserved remnants of the AF: tapirs (Tapirus terrestris), muriquis (Brachyteles arachnoides), and howlers (Alouatta guariba); (b) described patterns of interactions between dung beetles and feces; (c) evaluated vertebrate’s redundancy in terms of plants dispersed, and as dung resource for beetles; (d) delineated the food web of interacting partners; and (e) evaluated the stability of the food web facing a potential scenario of vertebrate loss. We found: (1) moderate redundancy in terms of primary seed dispersal; (2) low redundancy in terms of the potential influence on secondary dispersal; (3) the tri-trophic food web was characterized by low connectance, linkage density and modularity; (4) as a consequence, the loss of a single vertebrate potentially harmed the whole community structure.

3.5 Drivers and functional consequences of an individual-based seed-dispersal network along a natural regeneration gradient

Isla-Escudero, J.1, Jácome-Flores, M.2, Arroyo-Correa, B.1, Arroyo, J.M1, Jordano, P.1,3

1Doñana Biological Station, CSIC, Spain; 2Global Change and Sustainability Center, México; 3University of Seville, Spain

Plant-animal interactions are shaped and reconfigured by the ecological context where they happen, with impact on their functional consequences. Of current interest is the role of mutualistic interactions in plant range shifts due to the rapid changes that natural and human systems are currently facing. Interactions with seed-dispersing frugivores are key to the colonization process of many plant species. Understanding how seed dispersal interactions are shaped at the intra-population level across a natural regeneration gradient and their functional outcomes are key to comprehend the underlying colonization processes and range shift drivers. We analyzed the individual-based frugivory network of Juniperus phoenicea along a natural expansion gradient in Doñana National Park, SW Spain. We combined molecular analysis (DNA-Barcoding feces identification) with camera-trap surveys to sample frugivore visits at 105 focal junipers over two seasons. We used a modularity network metric to analyze the configuration of frugivory interactions along the regeneration gradient. Finally, we estimated the propagule contribution of each individual plant taking into account frugivore features (feeding rates/visit and seed treatment), and dispersal traits of individual plants (seeds/cone and seed viability). We found an individual interaction network structure concordant with the expansion gradient. We identified both modules composed of frugivore species and individual plants dominating the mature part of the gradient, as well as modules of plants and frugivores belonging to the colonization front. In addition, the individual context of each plant (both its intrinsic and extrinsic attributes) affected module composition, confirming the relevance of this individual-based approach. The contribution of individual junipers to the seed rain was found to be maximal at the colonization front, and strongly determined by the number of animal visits. Our results provide empirical support for plant expansion processes being actually favored by interactions with seed dispersers at the colonization front.

3.6 Dense herbivore populations influence the spatial patterns of seed dispersal and seed predation in the Mediterranean dwarf palm

Muñoz-Gallego, R.1, Traveset, A.1, Wiegand, W.2, Moreno, M.3, Fedriani, J.M.3,4

1Mediterranean Institute of Advanced Studies, CSIC-UIB, Spain; 2Helmholtz Center for Environmental Research, Germany; 3Desertification Research Center, CSIC, Spain; 4Doñana Biological Station, CSIC, Spain

The spatial distribution of adult plants and their seed dispersal pattern provides significant information about the underlying processes of plant-frugivore interactions. Thus, the frugivores’ assemblage (among other factors) could determine these spatial patterns and influence other plant-animal interactions, such as post-dispersal seed predation. We used spatial data of Chamaerops humilis adult palms and their dispersed seeds (Seed Dispersal Units, SDUs), collected during 2019 and 2020 in two different plots in Mallorca (Balearic Islands). These plots differed in the frugivores’ assemblage since feral goats were absent in one of them (the “defaunated” plot), but they were highly abundant in the other (the “overfaunated” plot). Moreover, we recorded whether SDUs were predated by insects and the intensity of predation. We addressed, using spatial point pattern analysis (SPPA), the following objectives: 1) to compare the spatial distribution of adult palms and SDUs between the “defaunated” and the “overfaunated” plots, 2) to assess the spatial relationship between the distribution of adult trees and the seed rain generated, 3) to describe the spatial patterns of seed predation by insects and, 4) to find out whether insect-predated seeds tended to be aggregated around adult palms. Adult palms and SDUs showed a double-clustered distribution with more isolated points than expected under null model in both the “defaunated” and the “overfaunated” plots. However, the bivariate analyses revealed a strong spatial association between adult palms and SDUs only in the “defaunated” plot. Interestingly, seed predation showed significant spatial patterns, but only in the “defaunated” plot. Seed predation happened more frequently and intensely within aggregated SDUs, and predated SDUs tended to be associated to adult palms. Our research disentangles for the first time the spatial patterns of seed predation by insects, and it calls for future studies on the effect of dense herbivore populations on plant spatial ecology.

3.7 Seed-dispersal limitation as a driver of biodiversity deficits in chronically fragmented landscapes

Acevedo-Limón, L.1, Rumeu, B.1, González-Varo, J.P.1

1University of Cádiz, Spain

Human-induced landscape changes have transformed forest ecosystems into fragments of woodland remnants embedded in a matrix of anthropogenic habitats. Both habitat fragmentation and habitat disturbance within fragments can lead to local extinctions and, therefore, to biodiversity deficits. For most plant species, seed dispersal constitutes a key process for the (re)colonization of woodland fragments once disturbance regimes have ceased. However, seed dispersal might be limiting because the distances from source populations to unoccupied fragments can be higher (several kilometers) than those at which most plant species disperse their seeds. Thus, dispersal limitation may explain contemporary ‘dark diversity’, that is, the set of species that are absent from a particular fragment but present in the surrounding region under similar ecological conditions. Previous studies have used seed sowing experiments to assess dispersal limitation, showing that it is a widespread phenomenon across forest ecosystems. Yet, we know little about its prevalence in chronically fragmented Mediterranean woodlands. In this study, we used sowing experiments to infer dispersal limitation for ten Mediterranean woody species (five barochorous and five vertebrate-dispersed species) in woodland fragments using the following rationale: if seedling recruitment and establishment from sown seeds are similar between fragments where species are present and those where they are absent, we infer that dark diversity (i.e. species’ absences) is mainly explained by dispersal limitation. Conversely, if recruitment and establishment are higher in fragments where the species is present than in those where it is absent, we infer that dark diversity is mainly due to environmental filtering driven by abiotic (e.g. water and soil conditions) or biotic factors (e.g. natural enemies). The results from this study have direct implications for management because local biodiversity could be enhanced by direct restoration actions assisting (re)colonization, like sowings or plantings, whenever dark diversity is explained by seed-dispersal limitation.

3.8 Understanding long-distance seed dispersal by sea currents: first results of experiments on Juniperus, Daucus, Ferula and Pancratium spp. from the Mediterranean Basin

Cuena-Lombraña, A.1, Bacchetta, G.1, Fois M.1

1University of Cagliari, Italy

To increase their evolutionary success, plants developed several adaptations to spread as widely and quickly as possible. Among them, the dispersal by water or hydrochory is a widely recognized but often overlooked effective syndrome; if propagules are also saltwater resistant, these can be dispersed through sea currents and break the barriers of insularity. The Mediterranean Basin, and especially islands, are natural laboratories of sea hydrochory (thalassochory) as main or complementary syndrome. We performed experiments with dispersal units of four genera native to the Mediterranean (Juniperus, Daucus, Ferula and Pancratium) including species differing in their distribution and possible dispersal ability: the coastal Juniperus macrocarpa, Daucus rouyi, Ferula arrigonii and Pancratium maritimum vs. the preferably inland J. turbinata and J. oxycedrus, F. communis and D. carota; and the endemic inland P. illyricum. We tested their period of dispersal units’ buoyancy and seed viability after floating to hypothesize their colonization distances. Our preliminary results suggest that some species show specific thalassochory syndrome while others could be dispersed by sea, although they probably evolved primarily for other dispersal types. Pancratium maritimum shows synchrony in floatability and vitality, suggesting a strong interconnection between the two traits. The congeneric P. illyricum shows poor floating ability and resistance to saltwater, which might explain its limited distribution. The genera Daucus and Ferula showed as well poor floating ability, but they can germinate after seawater exposition. Differently, all Juniperus species –all spread through insular and continental Mediterranean territories– show a less floatability than P. maritimum, while their viability remains high even after sinking, confirming that Juniperus species are particularly adapted to other dispersal types, such as endozoochory, although they are occasionally or stochastically able to be long dispersed by sea. This study contributes to explaining the overlooked but potentially crucial ability of vascular plants to colonize Mediterranean coastal ecosystems.

3.9 Variation among plant species in seed retention time inside frugivores’ gut: relevance and underlying traits

Bracho-Estévanez, C.A.1, Cuadrado, M.2, Sánchez, I.2, González-Varo, J.P.1

1University of Cádiz, Spain; 2Jerez City Council, Spain

Endozoochorous seed-dispersal by frugivorous animals is a mutualistic interaction that plays a pivotal role in the configuration of plant communities across most terrestrial ecosystems. In this mutualism, animals obtain food resources from the nutritive pulp of fleshy fruits, while plants benefit from the movement of their seeds away from the mother plant. That is, a reduction in competition together with a potential expansion to suitable habitats. The process consists of three major phases: initiation, transport, and seed deposition. Once fruits have been ingested, the movement patterns of animals and the retention time of seeds inside their guts will determine seed-dispersal distances. Thus, information on gut retention times (GRT) is essential to estimate the dispersal capacity of fleshy-fruited species. Experimental studies of GRT have been conducted in mammals, birds and reptiles, and multiple analyses have revealed positive allometric relationships between frugivore size and GRT: the larger the body size of the frugivore, the longer the retention time of the dispersed seeds; thereby, the higher the capacity for long-distance seed-dispersal. However, the potential effect of plant traits, as seed size and pulp nutrient content, on GRT has been largely overlooked despite these are highly variable among plant species and can influence the speed of seed ejection. In this study, we focused on variation in GRT among plant species when they are dispersed by a given disperser species. To do so, we conducted a set of experiments in which we measured GRT for more than 30 fleshy-fruited species dispersed by the song thrush (a key migratory seed-disperser in the Palearctic). Our results unveil substantial differences among plant species in GRT and a major role of seed and fruit traits in determining such variability. Thus, our findings can be interpreted in terms of variation among plant species in their intrinsic potential for long-distance seed-dispersal.

3.10 Plants on the ride: tracking the research diversity globally on endozoochory

Yadav, H.1,2, Phartyal, S.S.1

1Nalanda University, India; 2Yokohama National University, Japan

Animal-mediated seed dispersal (zoochory) is one of the essential ecosystem services for plants that help them find new habitats. Considering this, studying zoochory has become an important research area among ecologists for several decades. However, we have no comprehensive information about the diversity of zoochory studies, particularly on endozoochory at the global level. Here, we assessed when, where, and which taxon of plants or animals endozoochory was studied. We specifically aimed to find disparities/biases related to studied taxon, ecosystems, and geography. A systematic literature survey narrowed 162 peer-reviewed studies on endozoochory published in the last five decades. Our result highlights a continuous growth in endozoochory studies from 1971 onwards with considerable imbalances at the geographical and ecosystem level; >80% of studies were conducted only in the temperate regions with a prominent focus on the forest ecosystem (37%). Among animals, 91% of the study focused on wild animal species. Poaceae (covering 90 genera/226 species) reported the most endozoochorously dispersed plant taxa. Birds and antelopes were the most studied animal groups, covering 60 and 36% of studies. Although studies targeting domestic animals were low in number, they were found to disperse more plant species than wild animals. Despite the growth in endozoochory studies, considerable knowledge gaps still exist, mainly in the global south, where natural and human-altered landscapes still harbor a high diversity and abundance of wild and domestic herbivores without any grazing restrictions. Thus, the study suggests the need for more research from the global south having complex human- and animal-populated fragile ecosystems to generate more in-depth knowledge on endozoochorous seed dispersal.

3.11 Are seeds of wind-dispersed species really more oily? - The revised relationship between dispersal syndromes and seed nutrients.

Mašková, T.1

1University of Regensburg, Germany

Dispersal of all living organisms is a heterogeneous but, at the same time, very complex process that is driven by a combination of individual characteristics and environmental effects. In plants, seed dispersal is one of the main mechanisms of gene flow within but mainly between populations. Understanding the dispersal mechanism is crucial for answering the questions related to plant invasions and/or restoration processes. Different seed traits are considered to be connected with the dispersal spectra, but the evidence is usually not convincing. A relationship between dispersal spectra and seed mass was hypothesized, but found connection is weak. It was emphasized that not seed mass per se but the ratio of weight to the surface area of seeds is more important for dispersal, especially in the case of wind-dispersed species. It is thought that switching between carbohydrates and oils storage is the way how to manipulate this weight to surface area ratio because oils are more energy-rich compared to carbohydrates. On the other hand, oils are more energy demanding for their synthesis than carbohydrates. Therefore, there should be a balance between the costs of oils synthesis and the benefits of lighter seeds. Nevertheless, the existing evidence for higher seed oil content for wind-dispersed species in the literature suffers from unbalanced design, absence of phylogenetic correction, rough dispersal classification, and not distinguishing between a structural and non-structural part of seeds. Therefore, we used dispersal syndromes from the D3 database, which indicate a species-specific potential for a given dispersal vector instead of strict categorical classification. Further, we used seed oil and non-structural carbohydrate content data to distinguish the energy storage part of seeds that serve as nutrition and the structural part that mainly serves for embryo protection. We investigate the connection between the oil/carbohydrates ratio in seeds reserves and dispersal syndromes more precisely.

3.12 The evolution of plant dispersal syndromes and seed traits: evolutionary cues and diversification

Di Musciano, M.1,2, Berrilli, E.1, Frattaroli, A.R.1, Ricci, L.1, Di Cecco, V.3, Di Martino, L.3, Kaliontzopoulou, A.4

1University of L’Aquila, Italy; 2University of Bologna, Italy; 3Maiella National Park, Italy; 4University of Barcelona, Spain

Seed dispersal is a key trait for the reproductive success of plant species affecting the distribution and evolution of species across space and time. Different evolutionary pressures on plant movement have resulted in an enormous variety of seed dispersal mechanisms in seed plants. The broad range of dispersal syndromes (DS) can be summarized into four main groups: zoochory, anemochory, anemo-zoochory, and unspecialized. As expression of selective pressures, exerted by dispersal agents, we hypothesized a directional change from less specialized to more specialized syndromes. Moreover, we asked how dispersal ability affects species diversification rates in seed plants. Lastly, as seed traits play a specific role in each DS, we hypothesized that seed mass, terminal velocity, and floating capacity should show distinct evolution in each syndrome. We used stochastic character mapping (SIMMAP) to infer the ancestral state of DS and investigate their evolution in seed plants. We used the multistate speciation and extinction model (MuSSE) to test how DS influenced net diversification rates. The effect of dispersal ability on species diversification was assessed through quantitative state speciation‐extinction models (QuaSSE). Lastly, we fit different evolutionary models (OUwie) to each seed phenotypic trait using 100 randomly sampled DS histories obtained through SIMMAP. The results show how the most specialized DS (anemo-zoochory) exhibit the highest speciation and diversification rates, confirming that the increase of possible disperser spectrum is an evolutionary advantage. Species with mean dispersal ability have the highest diversification rates, which may be explained by two main reasons: high dispersal ability could inhibit speciation events and colonization ability in plants is not strictly correlated with dispersal ability. Contrasting evolutionary rates in seed mass and floating capacity and different optima in terminal velocity were observed, suggesting that these traits play a distinct role in each dispersal syndrome.

3.13 Unmasking the perching effect of the pioneer Mediterranean palm Chamaerops humilis L.

González-García, V.1, Garrote, P.J.2, Fedriani, J.M.3

1University of Oviedo, Spain; 2Center for Applied Ecology “Prof. Baeta Neves”, Portugal; 3Desertification Research Center CIDE, Spain

Seed arrival is a crucial necessary ecological process during the (re)colonization that can be enhanced by the use of the so-called “perch plants”. Little is known about how spatial aspects of “perching” affect their effectiveness in disturbed habitats. To evaluate several spatial aspects of “perching” effect, including whether the seed arrival via frugivorous birds is associated to the spatial distribution of the perch plants, we used a spatially explicit approach in two disturbed plots within the Doñana National Park (SW Spain). Specifically, we chose as study system the pioneer Mediterranean dwarf palm Chamaerops humilis L., which is often used as perch by a variety of frugivorous bird species. A total of 289 C. humilis individuals were sampled in search of bird feces (N = 2998) and dispersed seeds (N = 529). Recorded seeds belonged to six different woody species from five different families. GLMs analyses indicated that taller males C. humilis with high richness of beneficiary woody species received more dispersed seeds. We detected a random spatial structure of bird feces and dispersed seeds in one study plot, while a nonrandom spatial structure was found in the other one, where isolated C. humilis received a higher number of bird feces and dispersed seeds than expected under spatial null models. The difference in spatial patterns between both study plots could relate, among other factors, to their different state of development in the ecological succession. Most of dispersed seeds were concentrated in a small number of C. humilis individuals that acted as “hotspots” of seed arrival. The fact that frugivorous birds visited most often isolated C. humilis questions the aggregated spatial structure of revegetation designs typically used in restoration projects. This study reveals novel spatial aspects of the “perching” effect which could be helpful in the restoration of human-disturbed habitats worldwide.

3.14 Seed dispersal by ungulates – from seed traits to landscape level

Lepková, B.1, Mašková, T.2, Herben T.1,3

1Charles University, Czech Republic; 2University of Regensburg, Germany, 3Institute of Botany, Czech Republic

Free-ranging wild herbivores are a potential dispersal vector which can move seeds and fruits from mother plants to new localities connecting fragmented habitats. However, different species of herbivores provide dispersal for a different set of plant species due to the variability in animals’ foraging strategies, digestive tracts and body size. Furthermore, not all plant species are equal when it comes to survival in the guts. We conducted a thorough experiment with almost forty plant species and four herbivores to test for the survival of seeds after passage through the herbivore digestive system. Furthermore, we compared the survival of tested species with their frequency in the dung samples and in the landscape. We ask: (i) which seed traits and other characteristics influence the survival of seeds in the digestive tract? (ii) How does the survival of species from the feeding experiment correspond to germination rates from field-collected dung samples? (iii) How does it correspond to the frequency in the landscape?