Estimating fitness consequences of dispersal: a road to 'know-where'? Non-random dispersal and the underestimation of dispersers' fitness

1. Many studies investigating fitness correlates of dispersal in vertebrates report dispersers to have lower fitness than philopatric individuals. However, if dispersers are more likely to produce dispersing young or are more likely to disperse again in the next year(s) than philopatric individuals, there is a risk that fitness estimates based on local adult survival and local recruitment will be underestimated for dispersers. 2. We review the available empirical evidence on parent-offspring resemblance and individual lifelong consistency in dispersal behaviour, and relate these studies to recent studies of fitness correlates of dispersal in vertebrates. 3. Of the 12 studies testing directly for parent-offspring resemblance in dispersal propensity, five report a significant resemblance. The average effect size (r) of parent-offspring resemblance in dispersal was 0.15 [95% confidence interval (CI) = 0.07-0.22], with no difference between the sexes (average weighted effect size of 0.12 (0.08-0.16) and 0.16 (0.11-0.20) for females and males, respectively). Only three studies report data on within-individual consistency in dispersal propensity, of which two suggest dispersers to be more likely to disperse again. 4. To assess the magnitude of fitness underestimation expected for dispersing individuals depending on the heritability of dispersal distance and study area size, we used a simulation approach. Even when study area size is 10 times the mean dispersal distance, local recruitment per breeding event may be underestimated by 4-10%, generating a potential difference of 4-60% in average lifetime production of recruits between dispersing and philopatric individuals, with larger differences in long-lived species. 5. Estimates of both fitness correlates of dispersal and parent-offspring resemblance or within-individual consistency in dispersal behaviour have been reported for 11 species. Although some comparisons suggest genuine differences in fitness components between philopatric and dispersing individuals, others, based on adult and juvenile survival, are open to the alternative explanation of biased fitness estimates. 6. We list three potential ways of reducing the risk of making wrong inferences on biased fitness estimates due to such non-random dispersal behaviour between dispersing and philopatric individuals: (a) diagnosing effects of non-random dispersal, (b) reducing the effects of spatially limited study area and (c) performing controlled experiments.     

Birthplace‐dependent dispersal: are directions of natal dispersal determined a priori?

Sib–sib or, more generally, family resemblance for dispersal seems a widespread characteristic of vertebrates, and the birthplace has the potential to shape the dynamics and features of animal populations. Dispersal studies have often stressed the fundamental link between the fate of dispersers and population dynamics, but few have focused on the dispersal directions of individuals, despite the profound implications that this may have on population distribution, structure, dynamics and viability. We investigated the directions followed by 72 radio‐tagged dispersers (43 males and 29 females from 14 nest sites) in an eagle owl Bubo bubo population, and assessed their a) inter‐individual distances during dispersal and b) age at dispersal departure. For siblings, as well as potential‐siblings (i.e. individuals born in the same nest in different years), the birthplace influenced inter‐individual distances and dispersal directions, i.e. dispersers from the same nest moved to similar locations during the study; moreover, in each year, individuals from the same birthplace moved across the same areas in a short time period. Finally, siblings and potential‐siblings born in the same nest in different years started dispersal at similar ages. Based on the movement patterns of dispersers we discuss: a) the potential implications of the birthplace‐dependent dispersal on the ideal free distribution theory, as well as in terms of kin competition, inbreeding avoidance and population dynamics; and, more generally, b) the effect of the temporal features of the natal dispersal on the concept of habitat suitability vs density of individuals developed by the ideal free distribution theory.     

Seed dispersal of East Asian coastal dune plants via seawater – short and long distance dispersal

Coastal plants provide precious and irreplaceable services to human and coastal ecosystems, but people are still rather unaware how coastal plants relate with sea tides. We assumed that their seeds may reflect some relationships with tides. Our objective was to understand seed dispersal of plants living in the upper coastal regions, not reached by normal tides, but inundated by storm surges. For this purpose, we observed seed characteristics, especially seed buoyancy, of coastal and non-inundated plants of the Shandong Peninsula, north China. Through field simulation, we studied how buoyancy affected the dispersal during tides, using twig segments as retrievable dummies of seeds, in order to collect evidences with concern, how seed dispersal could occur during storm surges, which are extremes of tides. Coastal plants had predominantly buoyant seeds, while inland-growing plants had largely non-buoyant seeds. Ninety percent of buoyant twig segments (mimicking seeds) were recaptured after tides on experimentally used coastal areas; only 1% of non-buoyant ones of such dummies were recaptured, whereas the rest probably had been swept away by wave action to deposit at the sea bottom. Buoyant twig segments (mimicking seeds) dispersed along the coastlines as tides surged towards the coast. About 10% of these buoyant twigs were swept away with off-shore currents, but they might land elsewhere, similar as it might happen with long-distance dispersal of seeds.     

Coevolution of dispersal in a parasitoid–host system

Interspecific interactions and the evolution of dispersal are both of interest when considering the potential impact of habitat fragmentation on community ecology, but the interaction between these processes is not well studied. We address this by considering the coevolution of dispersal strategies in a host–parasitoid system. An individual-based host–parasitoid metapopulation model was constructed for a patchy environment, allowing for evolution in dispersal rates of both species. Highly rarefied environments with few suitable patches selected against dispersal in both species, as did relatively static environments. Provided that parasitoids persist, all the variables studied led to stable equilibria in dispersal rates for both species. There was a tendency toward higher dispersal rates in parasitoids because of the asymmetric relationships of the two species to the patches: vacant patches are most valuable for hosts, but unsuitable for parasitoids, which require an established host population to reproduce. High host dispersal rate was favoured by high host population growth rate, and in the parasitoid by high growth rates in both species. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Geographic distributions of homosporous ferns: does dispersal obscure evidence of vicariance?

The central problem in biogeography is that interactions between different processes result in the formation of historical patterns, such that it is difficult to discriminate the relative roles of vicariance and dispersal. Ferns are distributed by small wind-dispersed propagules that are produced in very large numbers and capable of dispersing thousands of kilometers. Thus, most taxon distributions in ferns are assumed to be a function of dispersal rather than vicariance. Here, we review some case examples that provide good evidence for vicariance and dispersal in ferns. We then ask whether dispersal is so extensive in ferns that vicariance is no longer detectable in most cases. Although we think that too few studies have been carried out to make generalizations at this stage, we outline the criteria for an effective research programme that can address this issue. Phylogenetic and distributional data are needed, not only because they are lacking in an evolutionarily important group of organisms, but also because data from ferns and other cryptogams are likely to be crucial in making broad biogeographic statements.     

When is dispersal for dispersal? Unifying marine and terrestrial perspectives

Recent syntheses on the evolutionary causes of dispersal have focused on dispersal as a direct adaptation, but many traits that influence dispersal have other functions, raising the question: when is dispersal ‘for’ dispersal? We review and critically evaluate the ecological causes of selection on traits that give rise to dispersal in marine and terrestrial organisms. In the sea, passive dispersal is relatively easy and specific morphological, behavioural, and physiological adaptations for dispersal are rare. Instead, there may often be selection to limit dispersal. On land, dispersal is relatively difficult without specific adaptations, which are relatively common. Although selection for dispersal is expected in both systems and traits leading to dispersal are often linked to fitness, systems may differ in the extent to which dispersal in nature arises from direct selection for dispersal or as a by‐product of selection on traits with other functions. Our analysis highlights incompleteness of theories that assume a simple and direct relationship between dispersal and fitness, not just insofar as they ignore a vast array of taxa in the marine realm, but also because they may be missing critically important effects of traits influencing dispersal in all realms.     

Are red imported fire ants facilitators of native seed dispersal?

Invasive ants threaten native communities, in part, through their potential to disrupt mutualisms, yet invasive species may also facilitate native species. The red imported fire ant (Solenopsis invicta) is one of the most conspicuous invasive ants in North America and its high densities, combined with its potential to displace native ants, have led to concerns that it may disrupt ant-plant seed dispersal mutualisms. We examined the potential of fire ants to disperse seeds in the longleaf pine ecosystem by comparing the removal of elaiosome-bearing seeds by fire ants versus native ants. A total of 14 ant species were observed removing seeds, with fire ants responsible for more than half of all removals. While fire ants were the dominant seed remover in this system, they did not remove significantly more seeds than would be expected based on their population density (46% of ground-dwelling ants). Moreover, red imported fire ants were similar to native ants with respect to distance of seed movement and frequency of moving seeds back to the nest. Areas of higher fire ant densities were found to have greater rates of seed removal by ants without a subsequent drop in seed dispersal by native ants, suggesting that fire ant-invaded areas may experience overall higher levels of seed dispersal. Thus, fire ants may actually facilitate dispersal of elaiosome-bearing plant species in the longleaf pine ecosystem.     

Is farther seed dispersal better? Spatial patterns of offspring mortality in three rainforest tree species with different dispersal abilities

The paradigm that tropical trees with farther seed dispersal experience lower offspring mortality is currently based on within-species studies documenting higher survival of offspring located farther from conspecific adults and/or closer to light gaps. We determined whether the paradigm also holds among species by comparing spatial patterns of offspring mortality among three sympatric Neotropical rainforest tree species with the same seed dispersers but with different dispersal abilities. First, we assessed spatially non-random mortality for each species by measuring spatial shifts of the population recruitment curve (PRC) with respect to conspecific adults and light gaps across three early life stages: dispersed seeds, young seedlings and old seedlings. Then, we determined whether PRC shifts were greater for the species with short dispersal distances than for the species with greater dispersal distances. We found that the PRC shifted away from conspecific adults consistently across life stages, but we found no consistent PRC shifts towards gaps, suggesting that mortality was related more to the proximity of conspecifics than to absence of light gaps. PRC shifts away from adults were greatest in the species with the lowest dispersal ability, supporting the paradigm. Differential PRC shifts caused the spatial distribution of offspring to become almost independent with respect to adult trees and gaps in all three species, despite large differences in seed dispersal distance among these species. Our results provide direct empirical support for the paradigm that among tropical trees, species with farther seed dispersal are less impacted by spatially non-random mortality than are similar species with shorter dispersal distances. Thus, greater dispersal effectiveness merits extra investments of trees in seed dispersal ability, even at the cost of fecundity.     

How much is a lot? Seed dispersal by white-faced capuchins and implications for disperser-based studies of seed dispersal systems

The quantity of seeds dispersed is considered one of several means to determine the dispersal effectiveness of an animal. However, there is little consistency in the manner in which quantities are measured or presented. Here, we quantify seed dispersal by white-faced capuchin monkeys (Cebus capucinus) in Santa Rosa National Park, Costa Rica by measuring: degree of frugivory, number of plant species consumed, the number of seeds consumed per unit time, the number of seeds dispersed intact per unit time, and the number of seeds dispersed intact per unit space. Forty-nine percent of C. capucinus diet is composed of the fruit of 39 species, 4 of which constitute 82% of the frugivory. Seventy-four percent of consumed fruits contain seeds that pass intact through the capuchin digestive system. Capuchins pass a mean of 15.7 seeds of a mean of 1.3 species per defecation, and defecate 25.4 times per 12-h day. These numbers are compared with extant data for C. capucinus, and possible reasons for discrepancies among results between studies are discussed. We propose a standardization of quantitative measures of seed dispersal so that quantifications of seed dispersal can be compared within species, and eventually across species.     

A ‘Goldilocks’ hypothesis for dispersal of biological control agents

The rate at which biological control agents disperse from release sites has important implications for their establishment and spread. Low rates of dispersal can yield spread that is too slow and may necessitate redistribution efforts for importation biological control and a high density of release sites for augmentation. Low dispersal rates may also lead to inbreeding at the site of release. On the other hand, high rates of dispersal can lead to Allee effects at the leading edge of the invasion front, potentially reducing the likelihood of establishment. Given these disadvantages associated with both low and high dispersal rates, we argue that intermediate rates of dispersal are likely to maximize the probability of establishment and appropriate spread for biological control agents released in the context of either importation or augmentative biological control. We consider this putative relationship a ‘Goldilocks hypothesis’ since it posits an optimum at intermediate values. In this review paper we begin by discussing the rationale for the Goldilocks hypothesis and then provide a case study from our work on importation biological control of the soybean aphid, Aphis glycines. Work on the soybean aphid parasitoid Binodoxys communis has shown that long-distance dispersal of immature parasitoids within winged migrating aphids is unlikely. This is likely good news for importation biological control because parasitoids dispersed in this manner would likely encounter crippling Allee effects. On the other hand, results from a field release study also suggest that female B. communis females (but not males) disperse actively from release sites. This female-biased dispersal may lead to strong mate-finding Allee effects and therefore may make establishment less likely.     

Does availability of potassium affect cold hardening of Scots pine through polyamine metabolism?

The effect of different potassium availability on the polyamines and frost resistance of Scots pine seedlings ( Pinus sylvestris L.) during cold hardening was studied. Scots pine seedlings were grown applying different rates of potassium by using the relative addition rate technique followed by a 2- or 9-week hardening period with decreased light intensity, day length and temperature. After 2 weeks of treatment the seedlings were not hardened (LT₅₀, =−11°C) and showed no differences in frost resistance, although differences in the polyamine levels between the K levels were observed. After 9 weeks of hardening the seedlings at the low, medium and high K levels showed a mean frost resistance (LTs.₅₀) of −81, −63, and −47°C, respectively. A negative effect of K on the frost resistance of the needles was also found in adult trees in September. The results indicate that at the early stage of cold hardening, potassium or free polyamine levels do not affect the frost resistance of Scots pine needles. However, in hardened seedlings and adult trees potassium displays a negative and putrescine a positive correlation with frost resistance, whereas spermidine and spermine show no correlation.     

Do plant-community-based grazing regimes lead to epizoochorous dispersal of high proportions of target species?

The contribution of large-herbivore epizoochory to the transfer of seeds within and between areas is thought to be significant. But often seeds of ubiquitous species are dispersed, which may enhance ruderalization processes. In order to study the dispersal of target species by sheep, we employed a community-based grazing approach followed by intra- and inter-area sheep transfers (maximum transfer distance 3 km). In case of inter-area transfers, well-developed target communities of an open inland sand ecosystem are used as “source”, linked to less-developed sand habitats (“sink”) via sheep. Also other factors determining which species become dispersed under field conditions were tested: seed surface structure, seed mass, plant seed-releasing height and animal behaviour. Finally the influence of animal movement on seed detachment and the actual arrival of seeds within a “sink” were studied.

Sheep transfers resulted in the dispersal of 56 seed species, dominated by Red List (seven species) and other target species. Quantitatively, most transported seeds belonged to target species, whereas graminoid competitors were highly under-represented. Morphological traits enhance the attachment probability regardless of seed mass. But for seeds without these epizoochory-facilitating traits, mass seems to affect attachment negatively. Plant height affected the number of species present in sheep coats but not the seed quantities. Probably certain species in the vegetation produced large numbers of seeds, e.g. low-growing Medicago minima with seed surface structures and high-growing species Verbascum phlomoides without seed surface structures. Also, although transfer half-times were three times lower than grazing half-times, naturally attached Stipa capillata and Agrimonia procera seeds showed no significant detachment rates during transfer, whereas considerable losses were found during grazing. Other 3-km sheep transfers did not result in significant losses of either epizoochorously transported seed or species quantities. Our study shows that community-based grazing can lead to the dispersal of especially target species. Besides that, different habitat fragments can be connected to each other via sheep without significant seed losses along the way.     

A practical approximation of pollen dispersal–deposition for calculation of pollen productivity and quantification of vegetation

We compared simple mathematical pollen dispersal–deposition models with Gaussian plume models. The simple mathematical models proved equal or better approximations of real world pollen dispersal–deposition. We concluded that for most standard applications, such as estimating pollen productivity or quantitative vegetation reconstructions, simple mathematical models would perform satisfactory. Such easy-to-use models may lower the threshold to employ quantitative tools to palaeoecological questions.     

Can we determine the biological availability of sediment-bound trace elements?

It is clear from available data that the susceptibility of biological communities to trace element contamination differs among aquatic environments. One important reason is that the bioavailability of metals in sediments appears to be altered by variations in sediment geochemistry. However, methods for explaining or predicting the effect of sediment geochemistry upon metal bioavailability are poorly developed. Experimental studies demonstrate that ingestion of sediments and uptake from solution may both be important pathways of metal bioaccumulation in deposit/detritus feeding species. Relative importance between the two is geochemistry dependent. Geochemical characteristics of sediments also affect metal concentrations in the tissues of organisms collected from nature, but the specific mechanisms by which these characteristics influence metal bioavailability have not been rigorously demonstrated. Several prerequisites are necessary to better understand the processes that control metal bioavailability from sediments. 1) improved computational or analytical methods for analyzing distribution of metals among components of the sediments; 2) improved computational methods for assessing the influences of metal form in sediments on sediment-water metal exchange; and 3) a better understanding of the processes controlling bioaccumulation of metals from solution and food by metazoan species directly exposed to the sediments. Such capabilities would allow mechanistic explanations essential to the development of practical tools sought for determining sediment quality criteria for metals.     

Does nitrogen availability control rates of litter decomposition in forests?

The effects of increased exogenous N availability on rates of litter decomposition were assessed in several field fertilization trials. In a jack pine (Pinus banksiana Lamb.) forest, needle litter decomposed at the same rate in control plots and in plots fertilized with urea and ammonium nitrate (1350 kg N ha^-1) with or without P and K. Mixed needle litter of western hemlock (Tsuga heterophylla (Raf.) Sarg.), western red cedar (Thuja plicata Donn) and Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) incubated in plots recently amended with sewage sludge (500 kg N ha^-1) lost less weight during 3 years than did litter in control plots. Forest floor material also decomposed more slowly in plots amended with sewage sludge. Paper birch (Betula papyrifera Marsh.) leaf litter placed on sewage sludge (1000 kg N ha^-1), pulp sludge, or sewage-pulp sludge mixtures decomposed at the same rate as leaf litter in control plots. These experiments demonstrate little effect of exogenous N availability on rates of litter decomposition.The influence of endogenous N availability on rates of litter decomposition was examined in a microcosm experiment. Lodgepole pine (Pinus contorta var. latifolia Engelm.) needle litter collected from N-fertilized trees (525 kg N ha^-1 in ammonium nitrate) were 5 times richer in N than needles from control trees (1.56% N versus 0.33% N in control trees), but decomposed at the same rate. Green needles from fertilized trees contained twice as much N as needles from control trees (1.91% N versus 0.88% N), but decomposed at the same rate. These experiments suggest that N availability alone, either exogenous or endogenous, does not control rates of litter decomposition. Increased N availability, through fertilization or deposition, in the absence of changes in vegetation composition, will not alter rates of litter decomposition in forests.     

Enhanced seed dispersal of Prunus africana in fragmented and disturbed forests?

Forest destruction and disturbance can have long-term consequences for species diversity and ecosystem processes such as seed dispersal. Understanding these consequences is a crucial component of conserving vulnerable ecosystems. In the heavily fragmented and disturbed Kakamega Forest, western Kenya, we studied seed dispersal of Prunus africana (Rosaceae). In the main forest, five forest fragments, and differently disturbed sites, we quantified the overall frugivore community as an indicator for species diversity. Furthermore, we determined the frugivores on 28 fruiting P. africana trees, estimated seed dispersal, crop size and the general fruit availability of surrounding trees. During the overall frugivore census we recorded 49 frugivorous species; 36 of them were observed visiting P. africana trees and feeding on their fruits. Although overall frugivore species richness was 1.1 times lower in fragments than in main forest sites and 1.02 times higher in highly disturbed than in less disturbed sites, P. africana experienced 1.1 times higher numbers of frugivores in fragments than in main forest sites and 1.5 times higher numbers of frugivores in highly disturbed than in less disturbed sites. Correspondingly, seed dispersal was 1.5 times higher in fragments than in main forest sites and 1.5 times higher in more disturbed than less disturbed sites. Fruit availability of surrounding trees and crop size influenced the number of visitors to some degree. Thus, the number of dispersed seeds seemed to be slightly higher in fragmented and highly disturbed sites. This indicates that loss of single species does not necessarily lead to a decrease of ecosystem services. However, loss of diversity could be a problem in the long term, as a multitude of species might act as buffer against future environmental change.     

Identifying ‘firebreaks’ to fragment dispersal networks of a marine parasite

Marine ecosystems are beset by disease outbreaks, and efficient strategies to control dispersal of pathogens are scarce. We tested whether introducing no-farming areas or ‘firebreaks’ could disconnect dispersal networks of a parasitic disease affecting the world’s largest marine fish farming industry (～1000 farms). Larval salmon lice (Lepeophtheirus salmonis) are released from and transported among salmon farms by ocean currents, creating inter-farm networks of louse dispersal. We used a state-of-the-art biophysical model to predict louse movement along the Norwegian coastline and network analysis to identify firebreaks to dispersal. At least one firebreak that fragmented the network into two large unconnected groups of farms was identified for all seasons. During spring, when wild salmon migrate out into the ocean, and louse levels per fish at farms must be minimised, two effective firebreaks were created by removing 13 and 21 farms (1.3% and 2.2% of all farms in the system) at ～61°N and 67°N, respectively. We have demonstrated that dispersal models coupled with network analysis can identify no-farming zones that fragment dispersal networks. Reduced dispersal pathways should lower infection pressure at farms, slow the evolution of resistance to parasite control measures, and alleviate infection pressure on wild salmon populations.     

Does seed dispersal limit initiation of primary succession in desert playas?

To investigate the initiation of primary succession in a cold-desert playa-dune complex, we studied the large-scale (2000 m) seed (diaspore) dispersal patterns at Mono Lake, California. Seeds of seven of the ten species reaching the barren playa had wind-dispersal adaptations. Rates of dispersal (numbers of seeds per square metre per day) were as much as three orders of magnitude lower on the playa than in the diverse dune vegetation. However, seed input appeared sufficient to reach potential safe sites on the playa, with a peak input of 66 ± 8 total seeds·m·d. The smooth playa surface, the virtual absence of aboveground barriers, and the high windspeed environment promote the long-distance dispersal of seeds (at least 1300 m for Chrysothamnus spp. and at least 700 m for Sarcobatus vermiculatus). The large spatial scale of sampling revealed a relatively high seed input onto the playa by the dominant pioneer species S. vermiculatus, despite the low abundance of parent vegetation in this region. All of these results implicate low rates of seed entrapment as an obstacle to establishment on this desert playa, rather than a lack of seed input.     

Evolution of conditional dispersal: a reaction–diffusion–advection model

To study evolution of conditional dispersal, a Lotka-Volterra reaction-diffusion-advection model for two competing species in a heterogeneous environment is proposed and investigated. The two species are assumed to be identical except their dispersal strategies: both species disperse by random diffusion and advection along environmental gradients, but one species has stronger biased movement (i.e., advection along the environmental gradients) than the other one. It is shown that at least two scenarios can occur: if only one species has a strong tendency to move upward the environmental gradients, the two species can coexist since one species mainly pursues resources at places of locally most favorable environments while the other relies on resources from other parts of the habitat; if both species have such strong biased movements, it can lead to overcrowding of the whole population at places of locally most favorable environments, which causes the extinction of the species with stronger biased movement. These results provide a new mechanism for the coexistence of competing species, and they also imply that selection is against excessive advection along environmental gradients, and an intermediate biased movement rate may evolve.     

Origins of the Hawaiian flora: Phylogenies and biogeography reveal patterns of long‐distance dispersal

Botanists have long considered the origins of the Hawaiian flora in terms of long‐distance dispersal from particular source areas. We extensively reviewed phylogenetic studies of the Hawaiian angiosperm flora to determine the most likely region of origin for each lineage from a defined set of source areas. We also evaluated dispersal modes of each lineage to assess whether certain dispersal modes are associated with a given source area. The largest source category was Widespread (involving related taxa that extend across more than one region), although many of these comprised native non‐endemic species, and accounted for little of the total species diversity (after accounting for in situ speciation). The next largest source regions were Indo‐Malayan and Neotropical. Comparatively few lineages originated from the East Asian region, although these include the single largest lineage. Lineages originating in the Indo‐Malayan region predominantly arrived via Pacific Islands, whereas dispersal from all other regions appears to have been mostly direct. Compared with previous analyses, we found a higher proportion of lineages originating in the Neotropics and temperate North America. Widespread origins were positively associated with dispersal via flotation on water, whereas other origins were associated with dispersal by birds, either through internal transport or external adhesion. We identified thirty‐one potential cases of dispersal out of Hawaii to other islands. Our assessment is complicated by lineages with ancient origins, with further complications likely stemming from hybridization events. Overall, numerous lineages including some distinctive endemic genera have not had sufficient phylogenetic study to determine an origin.