Methods for estimating long-distance dispersal

Long-distance dispersal (LDD) includes events in which propagules arrive, but do not necessarily establish, at a site far removed from their origin. Although important in a variety of ecological contexts, the system-specific nature of LDD makes "far removed" difficult to quantify, partly, but not exclusively, because of inherent uncertainty typically involved with the highly stochastic LDD processes. We critically review the main methods employed in studies of dispersal, in order to facilitate the evaluation of their pertinence to specific aspects of LDD research. Using a novel classification framework, we identify six main methodological groups: biogeographical; Eulerian and Lagrangian movement/redistributional; short-term and long-term genetic analyses; and modeling. We briefly discuss the strengths and weaknesses of the most promising methods available for estimation of LDD, illustrating them with examples from current studies.
The rarity of LDD events will continue to make collecting, analyzing, and interpreting the necessary data difficult, and a simple and comprehensive definition of LDD will remain elusive. However, considerable advances have been made in some methodological areas, such as miniaturization of tracking devices, elaboration of stable isotope and genetic analyses, and refinement of mechanistic models. Combinations of methods are increasingly used to provide improved insight on LDD from multiple angles. However, human activities substantially increase the variety of long-distance transport avenues, making the estimation of LDD even more challenging.     

Emus as non-standard seed dispersers and their potential for long-distance dispersal

Long-distance seed dispersal may have important consequences for species range, migration rates, metapopulation dynamics, and gene flow. Plants have evolved various adaptations for seed dispersal by standard agents, with typical dispersal distances associated with them. Seeds may also be dispersed by non-standard agents for which they do not show any apparent adaptation and may reach long distances. By sampling the droppings of emus Dromaius novaehollandiae at three localities in Western Australia, we investigated their potential to act as long-distance dispersers of seeds with adaptations for dispersal modes other than endozoochory, such as unassisted, ant, wind and exozoochory, for which they act as non-standard agents. Seventy-seven plant species with five types of dispersal syndromes were found in the 112 droppings analysed, with at least 68 having viable seeds. Although endozoochory was the most frequent syndrome, the presence of other syndromes was important in terms of number of species (61%) and seeds (50%). Estimates of species richness indicated that an increase in sampling effort would increase the number of species observed, especially among non-endozoochores. As a consequence of their long gut retention times and high mobility, emus can provide long-distance dispersal opportunities that may be especially relevant for species with dispersal modes of typically short distances (unassisted, ant).
Our results suggest that the role of emus as non-standard agents for long-distance dispersal should be taken into account for understanding current geographic ranges, gene flow and metapopulation dynamics of some plant species, as well as for predicting their future responses to climate change and fragmentation.     

Marking live conifer pollen for long-distance dispersal experiments

Long-distance dispersal (LDD) theory requires a method for marking live LDD pollen. Such a method must complement more intensive sampling methods inclusive of molecular cytogenetics, proteomics and genomics. We developed a new method for marking live Pinus taeda pollen using two dyes, rhodamine 123 and aniline blue, dissolved in a sucrose solution. Marked and unmarked pollen were compared with respect to in vitro germination, storage, terminal velocity, and in vivo pollen tube penetration of ovules. We found that: (1) both types of marked pollen retained their capacity for germination, (2) both types of marked pollen had similar aerodynamic properties when compared to unmarked pollen controls, (3) marked pollen retained its germination capacity for 48 h, and (4) of the marked pollen, only the aniline-marked pollen penetrated ovules during pollination. Germination declined rapidly for both types of marked pollen after 48 h and before 37 days at -20°C storage, while unmarked pollen lots retained 93% germination at all stages. This method for marking live P. taeda pollen is feasible for tracing LDD pollen only if released and deposited within 48 h of dye treatment.     

Mechanistic analytical models for long-distance seed dispersal by wind

We introduce an analytical model, the Wald analytical long-distance dispersal (WALD) model, for estimating dispersal kernels of wind-dispersed seeds and their escape probability from the canopy. The model is based on simplifications to well-established three-dimensional Lagrangian stochastic approaches for turbulent scalar transport resulting in a two-parameter Wald (or inverse Gaussian) distribution. Unlike commonly used phenomenological models, WALD's parameters can be estimated from the key factors affecting wind dispersal--wind statistics, seed release height, and seed terminal velocity--determined independently of dispersal data. WALD's asymptotic power-law tail has an exponent of -3/2, a limiting value verified by a meta-analysis for a wide variety of measured dispersal kernels and larger than the exponent of the bivariate Student t-test (2Dt). We tested WALD using three dispersal data sets on forest trees, heathland shrubs, and grassland forbs and compared WALD's performance with that of other analytical mechanistic models (revised versions of the tilted Gaussian Plume model and the advection-diffusion equation), revealing fairest agreement between WALD predictions and measurements. Analytical mechanistic models, such as WALD, combine the advantages of simplicity and mechanistic understanding and are valuable tools for modeling large-scale, long-term plant population dynamics.     

Benthic macroalgae as a dispersal mechanism for fauna: influence of a marine tumbleweed

Effective dispersal is problematic for benthic organisms without planktonic larvae; rafting and vertical migrations are mechanisms that can potentially be employed by such fauna, but these strategies entail considerable predation risk as well as other disadvantages. Unattached, but non-floating, “drift” algae harbor large numbers of fauna and may serve as an alternative dispersal mechanism in some systems. This paper reports field manipulations in Florida Bay, Florida, USA designed to determine (1) if such algae can disperse benthic animals, and (2) if dispersal efficiency varies as a function of two common substrata types: seagrass and bare sediment. A live immersion stain was used to mark faunal associates of Laurencia spp. algal clumps in situ. The fidelity of molluscs, decapods, ophiuroids, and fishes to stationary algal clumps was then compared with the fidelity of these animals to clumps that were forced to tumble over a given distance with a blower apparatus; these experiments were performed over both sand and seagrass substrata. Measurements of frequency, spatial extent, and rate of algal drift were made to aid in assessing the potential importance of benthic algae as a dispersal mechanism.

Algal clumps often rolled in a manner similar to that of terrestrial tumbleweeds; mark-recapture work showed that algal clumps can move up to 0.5 km/day and that algal drift is a frequent phenomenon. The algal masses were effective transporters of benthic fauna, including mobile shrimps and fishes; dispersal was more efficient over sand than over seagrass. Dispersal of fauna via this mobile habitat should entail lower risk than other adult dispersal stratagems such as vertical migration or rafting; this mechanism would be most advantageous for brooding species or those with limited planktonic phases. Differential fidelity to clumps tumbling across seagrass versus sand suggests that the algae could facilitate exchange of fauna between isolated seagrass patches.     

Alpine plant species have limited capacity for long-distance seed dispersal

Seed dispersal will be essential for plants to track future climate space, but dispersal capacity is rarely measured or incorporated into species distribution models. Using the entire alpine flora of the Snowy Mountains, south-eastern Australia, as a case study, we modelled the dispersal capacity of 198 species (93.4% of the flora) using the plant traits dispersal syndrome, seed mass, seed release height and growth form. The modelled maximum dispersal distances were mostly affected by dispersal syndrome of each species. The models reveal that 75% of species disperse up to 10 m, whilst 20% may disperse >100 m. Most species in this flora do not have any specific dispersal strategy, hence their inability to disperse >10 m. However, those species with longer modelled distances were dispersed by animals or wind (>600 and >140 m, respectively). This alpine flora has a low capacity for long-distance seed dispersal and is likely to suffer from migration lag as the local climate undergoes rapid changes.     

Small-scale variability as a mechanism for large-scale stability in mountain grasslands

Abstract. Data from a 7-yr permanent plot study of grassland dynamics were used to address the relationship between processes at two levels of resolution (3.3 cm x 3.3 cm, 50 cm x 50 cm). Grasslands mown and manured in the traditional way in the Krkonose Mts. (Riesengebirge) were used as a model system. Spatial dynamics at the finest scale were very high, as demonstrated by turnover of individual species in 3.3 cm x 3.3 cm subplots and year-to-year transition matrices of the same subplots. The direction of these dynamics was not correlated with grassland treatment, although there was some correlation within years. An extrapolation of such year-to-year dynamics to larger time scales would result in big large-scale changes on the community level, and large shifts in species composition of the whole sward. However, dynamics at larger spatial or temporal scales were generally small. Some directional change occurred in manured plots, whereas little change occurred in unmanured plots. Large-scale dynamics were not correlated with small-scale dynamics in plots without manuring, but some correlation was detectable in manured plots. There are probably several processes that drive small-scale dynamics, such as non-linear interactions and environmental fluctuations. We argue that within certain limits these forces act on species composition so as to make small-scale dynamics non-directional. This results in both large-scale species diversity and apparent large-scale stability of these grasslands. However, if these forces are beyond these limits, the small-scale dynamics may become directional, resulting in rapid changes at larger spatial scales.     

Genetic traces of recent long-distance dispersal in a predominantly self-recruiting coral

Background

Understanding of the magnitude and direction of the exchange of individuals among geographically separated subpopulations that comprise a metapopulation (connectivity) can lead to an improved ability to forecast how fast coral reef organisms are likely to recover from disturbance events that cause extensive mortality. Reef corals that brood their larvae internally and release mature larvae are believed to show little exchange of larvae over ecological times scales and are therefore expected to recover extremely slowly from large-scale perturbations.

Methodology/Principal Findings

Using analysis of ten DNA microsatellite loci, we show that although Great Barrier Reef (GBR) populations of the brooding coral, Seriatopora hystrix, are mostly self-seeded and some populations are highly isolated, a considerable amount of sexual larvae (up to ∼4%) has been exchanged among several reefs 10 s to 100 s km apart over the past few generations. Our results further indicate that S. hystrix is capable of producing asexual propagules with similar long-distance dispersal abilities (∼1.4% of the sampled colonies had a multilocus genotype that also occurred at another sampling location), which may aid in recovery from environmental disturbances.

Conclusions/Significance

Patterns of connectivity in this and probably other GBR corals are complex and need to be resolved in greater detail through genetic characterisation of different cohorts and linkage of genetic data with fine-scale hydrodynamic models.     

Evidence for long-distance dispersal in a sedentary passerine, Gymnorhina tibicen (Artamidae)

Australian magpies (Gymnorhina tibicen) are group-living birds found across much of mainland Australia. Adults commonly remain in a breeding territory until death. Young of the year either remain on the natal (birth) site or are forced by their parents to disperse. Observational studies in south-eastern Australia suggest that most dispersing juveniles settle within 7 km of their natal territory. Therefore, despite potential for considerable gene flow (via flight), social organization predisposes magpies towards local population structuring. In this study, we measured genetic variation at both nuclear (allozyme) and mitochondrial loci and found evidence of substantial gene flow over very large distances (up to 1599 km). Thus, some juvenile magpies may disperse much greater distances than was previously thought. For mtDNA, geographic and genetic distance were strongly correlated, consistent with a pattern of isolation by distance. Therefore, although female gene flow is substantial it is apparently geographically restricted over large distances, in approximately a stepping-stone fashion. We conclude that a strong relationship between gene flow and geographic distance can develop even over large distances if populations have experienced no major historical disturbances to gene flow.     

Molecular evidence for long-distance dispersal in the New Zealand pteridophyte flora

Aim To examine the relative importance of long‐distance dispersal in shaping the New Zealand pteridophyte (ferns and lycophytes) flora and its relationships with other floras, with the null hypothesis that the extant New Zealand pteridophyte flora has been isolated since New Zealand’s separation from Gondwana. Location New Zealand. Methods rbcL DNA sequences were assembled for 31 New Zealand pteridophyte genera, with each genus represented by one New Zealand species and the most closely related non‐New Zealand species for which data were available. Maximum‐likelihood, maximum‐parsimony, and Bayesian analysis phylograms were constructed and used as input for r 8s molecular dating, along with 23 fossil calibrations. Divergence estimates less than conservatively recent ages for New Zealand’s geological isolation, namely H_o > 30 Ma for pairs involving New Caledonian and Norfolk Island species and H_o > 55 Ma for all others, were taken as rejection of the null hypothesis. Results The null hypothesis was rejected for all pairs except, under some parameter conditions, for those involving the New Zealand species Cardiomanes reniforme, Lindsaea trichomanoides, Loxsoma cunninghamii, Lygodium articulatum, Marattia salicina, and Pteris comans. However, the Lindsaea and Pteris results probably reflect the absence in the analyses of closely related non‐New Zealand samples, while the Marattia divergence was highly contingent on which fossil calibrations were used. Main conclusions Rejection of the null hypothesis for the majority of pairs implies that the extant New Zealand lineage has undergone long‐distance dispersal either into or out of New Zealand. The notion of a long isolation since geological separation can, therefore, be dismissed for much of New Zealand’s pteridophyte flora. The analyses do not identify the direction of the long‐distance dispersal, and these New Zealand lineages could have had vicariant origins with subsequent long‐distance emigration. However, the alternative that many extant New Zealand pteridophyte lineages only arrived by long‐distance immigration after geological isolation seems likely.     

Adaptations for animal dispersal of one-seed juniper seeds

Summary Distributional patterns of one-seed juniper seeds and seedlings show that most seeds are found directly beneath source trees but most seedlings are found away from the source trees. Thus, seeds dispersed away from source trees seem to have a better chance of germination and growth than seeds beneath source trees. Seed distribution patterns indicate haphazard animal dispersal rather than directional dispersal by water runoff or gravity. One-seed juniper appears to have adaptations favoring zoochory over other types of dispersal methods. Seeds are not well protected from animals but are presented in an attractive, abundant, easily accessible and nutritious fruit. Fruit ripening occurs just before the arrival of avian winter residents in the piñon-juniper woodlands. Several of these species are potential dispersal agents. Seeds passed through the intestines of Townsend's Solitaires showed lowered germination compared to untreated seeds but these birds are probably good dispersers.     

A novel preference for an invasive plant as a mechanism for animal hybrid speciation

Homoploid hybrid speciation--speciation via hybridization without a change in chromosome number--is rarely documented and poorly understood in animals. In particular, the mechanisms by which animal homoploid hybrid species become ecologically and reproductively isolated from their parents are hypothetical and remain largely untested by experiments. For the many host-specific parasites that mate on their host, choosing the right host is the most important ecological and reproductive barrier between these species. One example of a host-specific parasite is the Lonicera fly, a population of tephritid fruit flies that evolved within the last 250 years likely by hybridization between two native Rhagoletis species following a host shift to invasive honeysuckle. We studied the host preference of the Lonicera fly and its putative parent species in laboratory experiments. The Lonicera fly prefers its new host, introduced honeysuckle, over the hosts of both parental species, demonstrating the rapid acquisition of preference for a new host as a means of behavioral isolation from the parent species. The parent taxa discriminate against each other's native hosts, but both accept honeysuckle fruit, leaving the potential for asymmetric gene flow from the parent species. Importantly, this pattern allows us to formulate hypotheses about the initial formation of the Lonicera fly. As mating partners from the two parent taxa are more likely to meet on invasive honeysuckle than on their respective native hosts, independent acceptance of honeysuckle by both parents likely preceded hybridization. We propose that invasive honeysuckle served as a catalyst for the local breakdown of reproductive isolation between the native parent species, a novel consequence of the introduction of an exotic weed. We describe behavioral mechanisms that explain the initial hybridization and subsequent reproductive isolation of the hybrid Lonicera fly. These results provide experimental support for a combination of host shift and hybridization as a model for hybrid speciation in parasitic animals.     

Sex, isolation and fidelity: unbiased long-distance dispersal in a terrestrial amphibian

Amphibians in general are considered poor dispersers and thus their dispersal curve should be dominated by short movements. Additionally, as male toads do not compete for females and sexual selection is by female choice, dispersal should be male-biased. Furthermore, since adults are site-loyal and polygynous, juveniles should move farther and faster than adults. We tested the hypotheses that dispersal would be limited and both sex- and age-biased in a population of Fowler's toads Bufo fowleri at Lake Erie, Ontario, Canada. Based on a mark-recapture study of 2816 toads, 1326 recaptured at least once, we found that although the toads did show high site fidelity, the dispersal curve was highly skewed with a significant "tail" where the maximum distance moved by an adult was 34 km. Dispersal was neither sex-biased nor age-biased despite clear theoretical predictions that dispersal should be biased towards males and juveniles. We conclude that the resource competition hypothesis of sex-biased dispersal does not predict dispersal tendencies as readily for amphibians as for mammals and birds. Toad dispersal only appears to be juvenile-biased because the juveniles are more abundant than the adults, not because they are the more active dispersers.     

Contrasting geographical distributions as a result of thermal tolerance and long-distance dispersal in two allegedly widespread tropical brown algae

Background

Many tropical marine macroalgae are reported from all three ocean basins, though these very wide distributions may simply be an artifact resulting from inadequate taxonomy that fails to take into account cryptic diversity. Alternatively, pantropical distributions challenge the belief of limited intrinsic dispersal capacity of marine seaweeds and the effectiveness of the north-south oriented continents as dispersal barriers. We aimed to re-assess the distribution of two allegedly circumtropical brown algae, Dictyota ciliolata and D. crenulata, and interpret the realized geographical range of the respective species in relation to their thermal tolerance and major tectonic and climatic events during the Cenozoic.

Methodology/Principal Findings

Species delimitation was based on 184 chloroplast encoded psbA sequences, using a Generalized Mixed Yule Coalescent method. Phylogenetic relationships were inferred by analyzing a six-gene dataset. Divergence times were estimated using relaxed molecular clock methods and published calibration data. Distribution ranges of the species were inferred from DNA-confirmed records, complemented with credible literature data and herbarium vouchers. Temperature tolerances of the species were determined by correlating distribution records with local SST values. We found considerable conflict between traditional and DNA-based species definitions. Dictyota crenulata consists of several pseudocryptic species, which have restricted distributions in the Atlantic Ocean and Pacific Central America. In contrast, the pantropical distribution of D. ciliolata is confirmed and linked to its significantly wider temperature tolerance.

Conclusions/Significance

Tectonically driven rearrangements of physical barriers left an unequivocal imprint on the current diversity patterns of marine macroalgae, as witnessed by the D. crenulata–complex. The nearly circumglobal tropical distribution of D. ciliolata, however, demonstrates that the north-south oriented continents do not present absolute dispersal barriers for species characterized by wide temperature tolerances.     

Evidence of long-distance dispersal of a gray wolf from the Chernobyl Exclusion Zone

The Chernobyl Exclusion Zone (CEZ) is a ~?4300 km² area in Belarus and Ukraine that remains heavily contaminated with radiation from the nuclear accident of 1986. Long standing controversy persists on the fate of wildlife within the CEZ following human abandonment of the area. Human residency remains extremely sparse, and the CEZ has become a refuge for some populations of wildlife, including gray wolves (Canis lupus). Using GPS telemetry, we documented the first long-distance movements of a young (1–2 years) male wolf from the CEZ into the surrounding landscape. The wolf traveled 369 km from its home range center over a 21-day period in February 2015. In the 95 days prior to dispersal, the wolf maintained a home range of ~?28 km², with daily displacements rarely exceeding 5 km. With the onset of dispersal, daily displacement increased to a mean of 16.8 km. The dispersal of a young wolf is an important observation because it suggests that the CEZ may serve as a source for some wildlife populations outside of the CEZ, and raises questions about the potential spread of radiation-induced genetic mutations to populations in uncontaminated areas.     

A model for long-distance dispersal of boll weevils (Coleoptera: Curculionidae)

The boll weevil, Anthonomus grandis (Boheman), has been a major insect pest of cotton production in the US, accounting for yield losses and control costs on the order of several billion US dollars since the introduction of the pest in 1892. Boll weevil eradication programs have eliminated reproducing populations in nearly 94%, and progressed toward eradication within the remaining 6%, of cotton production areas. However, the ability of weevils to disperse and reinfest eradicated zones threatens to undermine the previous investment toward eradication of this pest. In this study, the HYSPLIT atmospheric dispersion model was used to simulate daily wind-aided dispersal of weevils from the Lower Rio Grande Valley (LRGV) of southern Texas and northeastern Mexico. Simulated weevil dispersal was compared with weekly capture of weevils in pheromone traps along highway trap lines between the LRGV and the South Texas / Winter Garden zone of the Texas Boll Weevil Eradication Program. A logistic regression model was fit to the probability of capturing at least one weevil in individual pheromone traps relative to specific values of simulated weevil dispersal, which resulted in 60.4% concordance, 21.3% discordance, and 18.3% ties in estimating captures and non-captures. During the first full year of active eradication with widespread insecticide applications in 2006, the dispersal model accurately estimated 71.8%, erroneously estimated 12.5%, and tied 15.7% of capture and non-capture events. Model simulations provide a temporal risk assessment over large areas of weevil reinfestation resulting from dispersal by prevailing winds. Eradication program managers can use the model risk assessment information to effectively schedule and target enhanced trapping, crop scouting, and insecticide applications.     

Extensive long-distance pollen dispersal in a fragmented landscape maintains genetic diversity in white spruce

Conifers are among the most genetically diverse plants but show the lowest levels of genetic differentiation, even among geographically distant populations. High gene flow among populations may be one of the most important factors in maintaining these genetic patterns. Here, we provide empirical evidence for extensive pollen-mediated gene dispersal between natural stands of a widespread northern temperate/boreal conifer, Picea glauca. We used 6 polymorphic allozyme loci to quantify the proportion of seeds sired by pollen originating from different sources in a landscape fragmented by agriculture in North Central Ontario, Canada. In 7 stands, a small proportion of seeds were sired by self-pollen or neighboring trees but 87.1% (+/-1.7% standard error [SE]) of seeds were sired by pollen from at least 250 to 3000 m away. In 4 single isolated trees, self-fertilization rates were low and more than 96% (+/-1.3% SE) of seeds were sired by immigrant pollen. The average minimum pollen dispersal distance in outcrossed matings was 619 m. These results provide strong evidence that extensive long-distance pollen dispersal plays a primary role in maintaining low genetic differentiation among natural populations of P. glauca and helps maintain genetic diversity and minimize inbreeding in small stands in a fragmented landscape.