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Conditional genetic covariance among pollen pools for a Large non-fragmented remnant (LR), b two fragmented remnants within an urban landscape (FR1 and FR2), c Adjacent fragmented remnant 1 (AFR1) and Restored Site 1 (RS1) and d Adjacent fragmented remnant 2 (AFR2) and restored site 2 (RS2), depicted as pollination graphs overlaid on satellite images of sites. Nodes represent the population of pollen haplotypes sampled by each maternal family. Edges represent significant statistical covariance among pollen pools (colour figure online)
Source publication
Habitat fragmentation affects landscape connectivity, the extent of which is influenced by the movement capacity of the vectors of seed and pollen dispersal for plants. Negative impacts of reduced connectivity can include reduced fecundity, increased inbreeding, genetic erosion and decreased long-term viability. These are issues for not only old (r...
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Citations
... Therefore, our recommendation for land managers is that the pollination needs of self-incompatible plant species in restoration should be prioritised when concerned with restoring diverse functioning plant communities. Proximity of restored populations to natural populations, hostility of intervening landscapes to pollinator movements, and the mobility of pollinators, will influence how critical pollinator limitation might be (Ritchie et al., 2019(Ritchie et al., , 2021). In the current study, proximity to a large and relatively pristine nature reserve has apparently provided a source of pollinators for restored populations of L. multiflora, despite the disturbed mining landscape. ...
... In the current study, proximity to a large and relatively pristine nature reserve has apparently provided a source of pollinators for restored populations of L. multiflora, despite the disturbed mining landscape. Ritchie et al. (2019) identified strong connectivity facilitated by pollen dispersal via multiple species of highly mobile nectar feeding birds among new and old Banksia populations within a highly fragmented urban landscape. From an analysis of paternity using genetic markers, Krauss et al. (2009) found that 16% of all seeds within an isolated stand of the bird-pollinated B. hookeriana were sired by plants >250 m from the study population, and there was only a weak association between siring and distance between mates for the population of 112 plants. ...
The restoration of diverse self‐sustaining ecosystems requires re‐establishment of functional interactions among species. For plant communities, pollinators are usually essential for pollination, seed set and seed quality. A common assumption in ecological restoration for plants pollinated by animals is one of ‘build it and they will come’, which is rarely tested. Beyond seed set, there may be negative genetic consequences for seed quality if pollinators and their behaviour do not reflect those in reference populations.
Here, we conduct an ecological genetic assessment of seed quality via mating system parameters in Lambertia multiflora (Proteaceae), a species dependent on nectar‐feeding birds for pollination. Four populations of L. multiflora in disturbed sites that were rehabilitated following mineral sands mining were compared with four native reference populations, near Eneabba, Western Australia. In each population, approximately 10 offspring from each of 10 maternal plants were genotyped with 11 highly polymorphic microsatellite markers.
From these data, genetic diversity and mating system parameters were assessed, and found to be equivalent across all populations. Mean allelic diversity and heterozygosity across loci were very high. All populations were completely outcrossing with no bi‐parental inbreeding. Mean correlated paternity, sibship and effective population size estimates for restored and natural populations were not significantly different and reflected uniformly high paternal diversity and wide outcrossing. Equivalent genetic results for restored and natural reference populations indicate successful restitution of bird‐pollinator services for L. multiflora in these post‐mining rehabilitation sites.
Synthesis and applications . Reviewing our results with other published studies to date suggests a resilience of bird‐pollinator services in restored plant communities. These findings provide some reassurance to restoration practitioners working in these global south systems where bird pollination is a feature, at least for similar landscape scenarios. Our study also highlights the global contribution of ecological genetics to the objective assessment of functional species interactions in ecological restoration, an increasingly important goal of land managers and regulators seeking to improve restoration standards.
... However, the evaluation of extinction risk relating to the species' extent of occurrence is strongly context dependent. Different species with similar ranges may be vulnerable to different threats depending on their life history traits such as lifespan (Thrall et al. 2014), breeding (Willi et al. 2005) and mating systems Nora et al. 2016;Ritchie et al. 2019), reproductive rates (Rymer et al. 2005) and seedbank dynamics (Kenny 2000;Pickup et al. 2003), as well as genetic diversity (Frankham 2015) and population size (Leimu et al. 2006;Caballero et al. 2017). Moreover, to add to the complexity of the task, all of the above should be considered in the context of the species' landscape, disturbance history and interspecific interactions, particularly, pollination ecology (Cranmer et al. 2012;Llorens et al. 2013). ...
Narrowly endemic species are particularly vulnerable to catastrophic events. Compared to widespread species, they may also be less capable of adapting to shifts in environmental pressures as a result of specialisation on a narrow range of local condition and limited ability to disperse. However, life-history traits, such as preferential outcrossing and high fecundity can maintain genetic diversity and evolutionary potential, and boost species resilience. The endangered Grevillea bedggoodiana (Enfield Grevillea) is an understorey shrub restricted to an area of ca. 150 km 2 in southeastern Australia with a legacy of large-scale anthropogenic disturbance. Prior to this study little was known about its biology and population structure. Here, its breeding system was assessed through a controlled pollination experiment at one of its central populations, and eight populations were sampled for genetic analysis with microsatellite markers. The species was found to be preferentially out-crossing, with no evidence of pollination limitation. In most populations, allelic richness, observed heterozygosity and gene diversity were high (Ar: 3.8-6.3; H o : 0.45-0.65, H e : 0.60 − 0.75). However, the inbreeding coefficients were significant in at least four populations, ranging from F i-0.061 to 0.259 despite high outcrossing rates. Estimated reproductive rates varied among sampled populations but were independent of gene diversity and inbreeding. Despite its small geographic range, the species' populations showed moderate differentiation (AMOVA: F ST = 0.123), which was largely attributable to isolation by distance. We interpret these results as suggesting that G. bedggoodiana is reproductively healthy and has maintained high levels of genetic diversity despite recent disturbance.
... These included direct observations of species movement between two patches using playback experiments of mobbing calls [44] and echo-location calls [38] and field-based observations of organisms used to define least-cost surfaces [33]. One of these papers [45] defined the edges in their population graphs using conditional genetic covariance. ...
Purpose of Review
This review uses a combination of narrative and systematic review techniques, including automated content analysis (ACA), to summarize the last 5 years of research on urban connectivity. It addresses the evolution of the field relative to prior reviews, identifies common themes and research gaps in the studies, and assesses the use of novel methods and data.
Recent Findings
We found a broadening of geographic and taxonomic scope in recent studies, including more research from Chinese cities and on multiple species. We also found more studies that covered multiple time periods than have been documented in prior reviews. However, we observed a continuing reliance on best professional judgment rather than empirical field data to parameterize models and on analytic methods that are 10–20 years old. Our review framework identified several distinct conceptual themes in the literature including foci on land cover, including roads, water, and vegetation; green spaces and infrastructure; ecological conservation, planning, and management; habitat structure and function; and species movement.
Summary
Urban areas offer the opportunity to leverage unique data sets and novel analytical methods that incorporate both human and other biological needs for connectivity, acknowledging that these two needs may not always align. In terms of data, few of the connectivity results were supported by or tested with empirical data. While nearly two-thirds of the papers reviewed included some measure of functional connectivity, which is an increase from previous reviews, future research would benefit from new modeling approaches that explicitly incorporate the challenges of measuring landscape connectivity within the urban context and from a clear set of shared objectives and goals.
... These included direct observations of species movement between two patches using playback experiments of mobbing calls [44] and echo-location calls [38] and field-based observations of organisms used to define least-cost surfaces [33]. One of these papers [45] defined the edges in their population graphs using conditional genetic covariance. ...
This review uses a combination of narrative and systematic review techniques, including automated content analysis (ACA), to summarize the last 5 years of research on urban connectivity. It addresses the evolution of the field relative to prior reviews, identifies common themes and research gaps in the studies, and assesses the use of novel methods and data.
We found a broadening of geographic and taxonomic scope in recent studies, including more research from Chinese cities and on multiple species. We also found more studies that covered multiple time periods than have been documented in prior reviews. However, we observed a continuing reliance on best professional judgment rather than empirical field data to parameterize models and on analytic methods that are 10–20 years old. Our review framework identified several distinct conceptual themes in the literature including foci on land cover, including roads, water, and vegetation; green spaces and infrastructure; ecological conservation, planning, and management; habitat structure and function; and species movement.
Urban areas offer the opportunity to leverage unique data sets and novel analytical methods that incorporate both human and other biological needs for connectivity, acknowledging that these two needs may not always align. In terms of data, few of the connectivity results were supported by or tested with empirical data. While nearly two-thirds of the papers reviewed included some measure of functional connectivity, which is an increase from previous reviews, future research would benefit from new modeling approaches that explicitly incorporate the challenges of measuring landscape connectivity within the urban context and from a clear set of shared objectives and goals.
... At present, tests of the predictions of the genetic consequences for pollination by birds are predominately based on studies of woody shrubs and trees. These studies have provided support for the prediction that bird pollinators tend to facilitate extensive pollen carryover (Krauss et al. 2009), which promotes both paternal diversity (Campbell 1998;Krauss et al. 2017;Bezemer et al. 2019) and genetic connectivity between geographically isolated individuals and populations (Byrne et al. 2007;Bezemer et al. 2016;Ritchie et al. 2019;Nakanishi et al. 2020). However, few studies have examined non-woody species (Krauss et al. 2017), which in many cases will occur in the understory, are less floriferous than their woody counterparts, and experience lower pollinator visitation rates (e.g. ...
The behaviour of pollinators has important consequences for plant mating. Nectar-feeding birds often display behaviour that results in more pollen carryover than insect pollinators, which is predicted to result in frequent outcrossing and high paternal diversity for bird-pollinated plants. We tested this prediction by quantifying mating system parameters and bird visitation in three populations of an understory bird-pollinated herb, Anigozanthos humilis (Haemodoraceae). Microsatellite markers were used to genotype 131 adult plants, and 211 seeds from 23 maternal plants, from three populations. While outcrossing rates were high, estimates of paternal diversity were surprisingly low compared with other bird-pollinated plants. Despite nectar-feeding birds being common at the study sites, visits to A. humilis flowers were infrequent (62 visits over 21,552 recording hours from motion-triggered cameras, or equivalent to one visit per flower every 10 days), and the majority (76%) were by a single species, the western spinebill Acanthorhynchus superciliosus (Meliphagidae). Pollen counts from 30 captured honeyeaters revealed that A. humilis comprised just 0.3% of the total pollen load. For 10 western spinebills, A. humilis pollen comprised only 4.1% of the pollen load, which equated to an average of 3.9 A. humilis pollen grains per bird. Taken together, our findings suggest that low visitation rates and low pollen loads of floral visitors have led to the low paternal diversity observed in this understory bird-pollinated herb. As such, we shed new light on the conditions that can lead to departures from high paternal diversity for plants competing for the pollination services of generalist nectar-feeding birds.
... Differences in bird foraging movements can influence the pollination service they provide to plants, which can impact the comparative seed production between sites (Ritchie et al., 2019). We found bird-pollinator movements to be largely (35%-47%) within trees or between near neighbors in all sites, consistent with previous studies (Ramsay, 1989;Vaughton, 1990). ...
... Bird movements between more distant plants became more common as remnant size increased, a trend also observed in other fragmented landscapes with birdpollinated plants (Llorens et al., 2012;Yates et al., 2007). There are thus likely different genetic consequences for natural and restored populations of Banksia because of known differences in spatial population genetic structure, and inbreeding avoidance mechanisms (see Krauss et al., 2009;Ritchie et al., 2017Ritchie et al., , 2019Ritchie & Krauss, 2012), which ultimately determine reproductive success (Wooller & Wooller, 2001). The observed differences in visitation and movement patterns among sites reflect the natural variability of interactions and resource availability in natural and disturbed parts of this urban-dominated landscape. ...
... Knowledge of which pollinators are negatively impacted by habitat fragmentation and urbanization is required to develop an understanding of the impacts (e.g., for pollinator services) and solutions for their reinstatement. Consideration needs to be given to the landscape positioning and connectivity of restored sites to ensure the movement of pollinators' communities and maintenance of pollinator services between these remnants (see Ritchie et al., 2017Ritchie et al., , 2019. ...
Pollinators and the pollination services they provide are critical for seed set and self-sustainability of most flowering plants. Despite this, pollinators are rarely assessed in restored plant communities, where their services are largely assumed to re-establish. Bird–pollinator richness, foraging, and interaction behavior were compared between natural and restored Banksia woodland sites in Western Australia to assess their re-establishment in restored sites. These parameters were measured for natural communities of varying size and degree of fragmentation, and restored plant communities of high and low complexity for three years, in the summer and winter flowering of Banksia attenuata and B. menziesii, respectively. Bird visitor communities varied in composition, richness, foraging movement distances, and aggression among sites. Bird richness and abundance were lowest in fragmented remnants. Differences in the composition were associated with the size and degree of fragmentation in natural sites, but this did not differ between seasons. Restored sites and their adjacent natural sites had similar species composition, suggesting proximity supports pollinator re-establishment. Pollinator foraging movements were influenced by the territorial behavior of different species. Using a network analysis approach, we found foraging behavior varied, with more frequent aggressive chases observed in restored sites, resulting in more movements out of the survey areas, than observed in natural sites. Aggressors were larger-bodied Western Wattlebirds (Anthochaera chrysoptera) and New Holland Honeyeaters (Phylidonyris novaehollandiae) that dominated nectar resources, particularly in winter. Restored sites had re-established pollination services, albeit with clear differences, as the degree of variability in the composition and behavior of bird pollinators for Banksias in the natural sites created a broad completion target against which restored sites were assessed. The abundance, diversity, and behavior of pollinator services to remnant and restored Banksia woodland sites were impacted by the size and degree of fragmentation, which in turn influenced bird–pollinator composition, and were further influenced by seasonal changes between summer and winter. Consideration of the spatial and temporal landscape context of restored sites, along with plant community diversity, is needed to ensure the maintenance of the effective movement of pollinators between natural remnant woodlands and restored sites.
... Despite being bird pollinated, we found significant levels of selfing in the wild populations. While comparable to some bird-pollinated proteaceous species (Bezemer et al. 2016), these levels of inbreeding are notably higher than many others (Whitehead et al. 2018;Ritchie et al. 2019), leading to speculation that species such as L. orbifolia may be able to tolerate significant levels of inbreeding (Coates & Hamley 1999). Clearly high numbers of selfed individuals have survived to give the estimates in this study. ...
There is an increasing need to establish populations of threatened plants in threat‐free habitat to prevent species extinction. The amount of genetic diversity in founding plants will influence whether the new population has the capacity to persist and evolve over time, and factors that influence the maintenance of genetic diversity, such as the mating systems will also play a role in population persistence. We developed 13 nuclear microsatellite markers and used these to evaluate genetic diversity and mating system parameters of three translocated populations of two subspecies of Lambertia orbifolia, and compared these parameters to seven wild populations. Genetic diversity was maintained in the translocated population of L. orbifolia subsp. Scott River Plains, established using a single source population (Nar = 3.270 and He = 0.534 in translocated population; Nar = 3.280 and He = 0.478 in wild populations), and maintained or increased in the two admixed translocated populations of L. orbifolia subsp. orbifolia (Nar = 3.115, 3.830 and He = 0.511, 0.635 in translocated populations; Nar = 2.780 and He = 0.438 in wild populations) compared to wild populations of each subspecies. Mating system parameters were comparable between translocated and wild populations of L. orbifolia subsp. Scott River Plains indicating the likelihood of genetic diversity being maintained in future generations. However, there was increased selfing in translocated populations of L. orbifolia subsp. orbifolia, suggesting suboptimal pollination and high values for the inbreeding coefficient in these admixed populations (Fis = 0.474, 0.275), which may be an artifact of the Wahlund effect or from less fit (inbred) seedlings surviving ex situ propagation and translocation.
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... As B. marginata was once a widely distributed, but likely scattered, species in savannahlike ecosystems [32,73], it is unclear whether the genetic diversity patterns presented here are indicative of the species' history, of recent fragmentation, or both. However, the SSR indices reported here are comparable with rare species such as B. mimica, B. vestita and B. arborea [74,75] as well as the widespread but fragmented B. menziesii [76], suggesting that recent fragmentation is likely the driver of low diversity. While few SNP-based comparisons are available for Banksia our diversity indices were generally higher than those observed in the disjunct B. biterax [77] but similar to the more widely distributed B. seminuda [78]. ...
... Pollen-mediated gene flow in banksias is primarily via insects, birds and mammals [39,94,95]. Birds can potentially transport pollen over large distances with B. menziesii pollen known to travel from 400 m to <2 km [76,96], although [97] highlight that most B. sphaerocarpa var. caesia pollen travels very short distances (<20 m). ...
Landscape degradation is a major threat to global biodiversity that is being further exacerbated by climate change. Halting or reversing biodiversity decline using seed-based restoration requires tons of seed, most of which is sourced from wild populations. However, in regions where restoration is most urgent, wild seed sources are often fragmented, declining and producing seed with low genetic diversity. Seed production areas (SPAs) can help to reduce the burden of collecting native seed from remnant vegetation, improve genetic diversity in managed seed crops and contribute to species conservation. Banksia marginata (Proteaceae) is a key restoration species in south-eastern Australia but is highly fragmented and declining across much of its range. We evaluated genetic diversity, population genetic structure and relatedness in two B. marginata SPAs and the wild populations from which the SPA germplasm was sourced. We found high levels of relatedness within most remnants and that the population genetic structure was best described by three groups of trees. We suggest that SPAs are likely to be important to meet future native seed demand but that best practice protocols are required to assist land managers design and manage these resources including genetic analyses to guide the selection of germplasm.
... Similarly, Ritchie, Dyer, Nevill, Sinclair, and Krauss (2019) in average allele numbers and 31% reduction in heterozygosity in the next 15 generations in the absence of intervention. This is a concern as the majority of B. marginata remnant populations spanning the VVP, and across much of its distribution, persist as small stands consisting of <20 individuals in total (Heyes et al. in review). ...
Habitat fragmentation imperils the persistence of many functionally important species, with climate change a new threat to local persistence due to climate‐niche mismatching. Predicting the evolutionary trajectory of species essential to ecosystem function under future climates is challenging but necessary for prioritizing conservation investments. We use a combination of population genetics and niche suitability models to assess the trajectory of a functionally important, but highly fragmented, plant species from south‐eastern Australia (Banksia marginata, Proteaceae). We demonstrate significant genetic structuring among, and high level of relatedness within, fragmented remnant populations, highlighting imminent risks of inbreeding. Population simulations, controlling for effective population size (Ne), suggest that many remnant populations will suffer rapid declines in genetic diversity due to drift in the absence of intervention. Simulations were used to demonstrate how inbreeding and drift processes might be suppressed by assisted migration and population mixing approaches that enhance the size and connectivity of remnant populations. These analyses were complemented by niche suitability models that predicted substantial reductions of suitable habitat by 2080; ~ 30% of the current distribution of the species climate niche overlaps with the projected distribution of the species climate niche in the geographic region by the 2080s. Our study highlights the importance of conserving remnant populations and establishing new populations in areas likely to support B. marginata in the future, and adopting seed sourcing strategies that can help populations overcome the risks of inbreeding and maladaptation. We also argue that ecological replacement of B. marginata using climatically‐suited plant species might be needed in the future to maintain ecosystem processes where B. marginata cannot persist. We recommend the need for progressive revegetation policies and practices to prevent further deterioration of species such as B. marginata and the ecosystems they support.
... Greater pollen immigration was observed with greater proximity to potentially large pollen sources and pollinator habitat provided by mature remnant populations. The high rate of pollen immigration at the Monjebup North A study area is comparable with a large number of studies of pollen dispersal among fragmented remnant populations (Byrne et al., 2007;Byrne et al., 2008;Sampson et al., 2014;Sampson et al., 2016;Thavornkanlapachai et al., 2018), among remnant and agroforestry populations (Millar et al., 2010), and among remnant and restoration populations (Ritchie & Krauss, 2012;Frick et al., 2014;Ritchie et al., 2019) of animalpollinated species in the SWAFR landscape. Our results support the importance of mature remnant vegetation as a source of pollen and as pollinator habitat, and providing genetic exchange and rapidly establishing connectivity at the greater landscape scale, which has been previously highlighted for animal-pollinated species (Dixon, 2009). ...
... For example, pollen dispersal was highly variable in bird-pollinated Calothamnus quadrifidus but pollen immigration into small isolated populations was found to come predominantly from large nearby remnant reserve populations and not from very small but closer remnant populations (Byrne et al., 2007). Similarly, a nearby large remnant population of mature (300-year-old) B. attenuata was found to be the predominant pollen source for a nearby restoration population (Ritchie & Krauss, 2012), and strong interpopulation pollinator service have been found in restoration populations of B. menziesii adjacent remnants (Ritchie et al., 2019). ...
... Our findings suggest that general pollinator services have been restored in restoration populations of B. media as early as four years after establishment. The result is consistent with other studies that have shown the rapid establishment of generalist pollinator services in restoration populations of other vertebrate-pollinated Banksia species (Ritchie & Krauss, 2012;Frick et al., 2014;Ritchie et al., 2019). ...
Evaluation of patterns of pollen dispersal, mating systems, population fitness, genetic diversity and differentiation in restoration and remnant plant populations can be useful in determining how well restoration activities have achieved their objectives. We used molecular tools to assess how well restoration objectives have been met for populations of Banksia media in the biodiversity hotspot of south-west Western Australia. We characterized patterns of pollen dispersal within, and pollen immigration into, two restoration populations. We compared mating system parameters, population fitness via seed weight, genetic diversity and genetic differentiation for restoration and associated reference remnant populations. Different patterns of pollen dispersal were revealed for two restoration sites that differed in floral display, spatial aggregation of founders and co-planted species. Proximity to remnant native vegetation was associated with enhanced immigration and more short-range pollen dispersal when other population variables were constant. Greater seed weights at remnant compared to restoration populations were not related to outcrossing rate. Equivalent mating system and genetic diversity parameters and low to moderate levels of genetic differentiation between restoration and remnant populations suggest pollinator services have been restored in genetically diverse restoration populations of local provenance B. media as early as four years from planting.
