REVIEW

Mistletoes in a changing world: a premonition of anon-analog future?1

Francisco E. Fontúrbel

Abstract: Mistletoes are a group of flowering plants that have developed a parasitic lifeform through complexeco-evolutionary processes. Despite being considered a pest, mistletoes represent a keystone forest resource andare involved in complex plant–plant and plant–animal interactions. Their parasitic lifeform and specializedecological interactions make mistletoes an ideal model with which to understand the effects of anthropogenicdisturbances in a changing world. The accelerated growth of the human population has altered all ecosystems onEarth, leading to biodiversity loss. Land-use changes (involving habitat loss, fragmentation, degradation, andtransformation processes) can alter the ecological scenario for mistletoe by altering hosts, mutualists, and nutri-ent cycling. Those changes may have large consequences at the community level, changing the spatial structure ofmistletoes, as well as interaction effectiveness, facilitation process, interaction disruption, and novel interactionswith invasive species, leading to non-analog communities in the long run. Furthermore, climate change effectsoperate on a global scale, enhancing the effects of land-use changes. As temperatures increase, many specieswould alter their distribution and phenology, potentially causing spatial and temporal mismatches. But morecritical is the fact that water stress is likely to disrupt key ecological interactions. Thus, mistletoes can providevaluable insights for what we can expect in the future, as a result of human disturbances.

Key words: climate change, eco-evolutionary dynamics, facilitation, land-use change, spatial mismatch, temporalmismatch.

Résumé : Le gui comprend un groupe de plantes à fleurs qui ont développé une forme de vie parasitaire grâce à desprocessus écoévolutifs complexes. Bien qu’il soit considéré comme un parasite, le gui constitue une ressourceforestière fondamentale et il est impliqué dans des interactions plantes-plantes et plantes-animaux complexes. Saforme de vie parasitaire et ses interactions écologiques spécialisées font du gui un modèle idéal pour comprendreles effets des perturbations anthropiques dans un monde en changement. La croissance accélérée de la populationhumaine a modifié tous les écosystèmes de la Terre, entrainant une perte de diversité. Les changementsd’utilisation des terres (impliquant la perte, la fragmentation, la dégradation et la transformation des habitats)peuvent modifier le scénario écologique du gui en affectant ses hôtes, ses mutualistes et le cycle de ses nutriments.Ces changements peuvent avoir des conséquences importantes à l’échelle de la communauté, en modifiant lastructure spatiale du gui, l’efficacité des interactions, le processus de facilitation, l’interruption des interactions etl’établissement de nouvelles interactions avec des espèces envahissantes, donnant lieu à long terme à des com-munautés non analogues. De plus, les effets des changements climatiques se répercutent à l’échelle mondiale,accroissant les effets des changements d’utilisation des terres. Avec l’augmentation des températures, de nom-breuses espèces pourraient modifier leur distribution et leur phénologie, ce qui pourrait provoquer des déséquili-bres spatiaux et temporels. Mais le fait que le stress hydrique puisse perturber des interactions écologiques clés estencore plus critique. Ainsi, le gui peut donner un aperçu précieux de ce que nous pouvons attendre de l’avenir, enconséquence des perturbations humaines. [Traduit par la Rédaction]

Mots-clés : changements climatiques, dynamique écoévolutive, facilitation, changement d’utilisation des terres,déséquilibre spatial, déséquilibre temporel.

IntroductionAmong the flowering plants, mistletoes are a particu-

larly fascinating group not only because of their parasiticlifeform, but also because of their importance in the

ecosystem (Watson 2001; Mellado and Zamora 2017).There are about 1400 mistletoe species worldwide, allbelonging to five families within the Order Santalales(Watson 2004). Mistletoes are often considered a pest

Received 26 November 2019. Accepted 12 February 2020.

F.E. Fontúrbel. Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Avenida Universidad 330, Valparaíso 2373223, Chile.Email for correspondence: fonturbel@gmail.com.1This Review is one of a selection of papers published in the special issue from the IUFRO World Congress, Curitiba, Brazil 2019 Symposium onMistletoes.

Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink.

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because they can compromise host plant growth, repro-duction, and survival (Arruda et al. 2012; Henríquez-Velásquez et al. 2012; Teixeira-Costa and Ceccantini 2015;Koenig et al. 2018). However, the ecological particulari-ties of parasitic plants make them more complex thanany other plant (Watson 2009). Mistletoes are entirelydependent on their host plants to survive. Despite thefact that many of them are hemiparasites and capableof photosynthesizing, mistletoes are rootless and takewater and minerals from the host. However, in thiscase, these plant–plant interactions have more com-plex co-evolutionary processes (Aukema 2003; Geniniet al. 2012; Guerra et al. 2018). Also, mistletoes are akeystone resource in forest ecosystems because theyprovide food resources during seasonal periods of scar-city (Watson 2001; Watson and Herring 2012) and areinvolved in many mutualistic interactions (Aizen2003; Rodríguez-Mendieta et al. 2018).

Mistletoe–host relationships are far more complexthan any other parasite–host system. The tight co-evolutionary processes between mistletoes and theirhosts determine: (i) host range, (ii) chemical interactions,and (iii) facilitation events. Host range is determined byhost competence and mistletoe transmission (Roxburghand Nicolson 2005; Okubamichael et al. 2016), which re-sults in a large variability of host range values amongmistletoe species (Mathiasen et al. 2008). Even within thesame genus we may find substantial host range differ-ences. For example, the hemiparasitic mistletoe Tristerixcorymbosus (Fig. 1a) parasitizes about 30 native host plantsand at least another 10 exotic trees. In contrast, the ho-loparasitic mistletoe Tristerix aphyllus (Fig. 1b) can onlyparasitize a few species of cactus. Both species are sym-patric and depend on the same pollination and seed dis-perser species (Medel 2000; Amico et al. 2007). Chemicalinteractions between host plants and mistletoes involvesecondary metabolite uptake along with water and nu-trients from the host’s xylem (Anselmo-Moreira et al.2019; Lázaro-González et al. 2019) and may be a determi-nant to attract mutualists (Troncoso et al. 2010; Lemaitreet al. 2012). Further, mistletoes can play a major role inthe ecosystem via indirect facilitation interactions. Para-sitized host plants are indirectly benefited by mistletoes,because they attract more diverse pollinators and seeddispersers, which results in large recruitment outputs(van Ommeren and Whitham 2002; Candia et al. 2014;Mellado and Zamora 2016). Also, mistletoes provide nest-ing sites for a wide range of animal species (Room 1972;Hedwall et al. 2006; Watson et al. 2011; Smith et al. 2013),and mistletoe litter is rich in nutrients, playing an im-portant role in facilitating the establishment and growthof understory plants (Soler et al. 2015; Mellado et al.2019).

Mistletoes depend on biotic pollination and seed dis-persal interactions (Watson 2004), as a result of complexco-evolutionary processes. Most mistletoes are mainly

pollinated by birds and insects (Mathiasen et al. 2008),but some species can be pollinated by bats or the wind(Restrepo et al. 2002; Robertson et al. 2005; Arruda et al.2012; Fadini et al. 2018, 2020). Among the Loranthaceaefamily, mistletoes have showy flowers with bright colors(yellow to red), and tubular corollas with sugar-rich nec-tar rewards, which are highly attractive to both hum-mingbirds and bumblebees (Arruda et al. 2012). However,many other mistletoes present small flowers that aretypically pollinated by insects alone. However, the seeddispersal process is more critical than pollination formistletoes, because seeds must arrive at suitable siteswithin the host plants (Reid 1991). While birds are theprimary mistletoe dispersers (Mathiasen et al. 2008),some mammals can play this role as well (Amico andAizen 2000; Arruda et al. 2012).

A changing world aheadThe hyper-exponential growth of the human popula-

tion during the last century has largely modified all eco-

Fig. 1. (a) The hemi-parasitic mistletoe Tristerix corymbosushas a wide host range, parasitizing at least 30 tree species.(b) The holo-parasitic mistletoe Tristerix aphyllus has anarrow host range, only parasitizing a few species ofcactus (photos: Francisco E. Fontúrbel). [Colour online.]

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systems on Earth (Armesto et al. 2010), resulting in adramatic biodiversity loss. There are four major biodiver-sity loss drivers: land-use change, resource overexploita-tion, invasive species, and climate change (Sala et al.2000). The interaction of those drivers is causing a rapiddecline in species diversity and their ecological interac-tions (Valiente-Banuet et al. 2015). Ecological interactionsusually cease before the species involved become ex-tinct, thereby altering ecosystem functioning and com-munity structure (Bascompte and Jordano 2007). Owingto their life-history traits and high dependence on mutu-alistic interactions, mistletoes are an excellent studymodel for understanding and forecasting the effects ofanthropogenic disturbances.

Human activities in natural areas may result in habitatloss, fragmentation, degradation, and transformation.Habitat loss and fragmentation are usually intertwinedand highly correlated (Fahrig 2003). When a continuoushabitat is fragmented, area and edge effects largely ex-plain biodiversity changes, as habitat remnants becomesmaller, and edges increase, exposing those remnantsto a heterogeneous matrix (Ewers and Didham 2006;Didham et al. 2012). Habitat degradation implies changesin habitat quality rather than area or spatial configura-tion. Therefore, habitat quality becomes reduced by theloss of key elements, such as nesting cavities or microcli-matic conditions (González et al. 2019). Last but not least,habitat transformation (i.e., the partial or total replace-ment of native species by one or a few exotic species)leads to significant changes in habitat structure andspecies composition, altering the ecological scenario(Fontúrbel et al. 2017a; Fontúrbel and Medel 2017). Sur-prisingly, mistletoes are capable of persisting in all thosedisturbance scenarios. However, the underlying ecologi-cal and evolutionary consequences remain largelyunknown, as well as the cascade effects that habitat dis-turbances may have at a community level.

Disturbance, mistletoes, and cascading effects on thecommunity

Humans have created a heterogeneous mosaic of nat-ural, semi-natural, and transformed habitats, in whichnative species may persist depending on their tolerance,adaptativeness, and the possibility of maintaining theirecological interactions or finding new partners to inter-act with (Kiers et al. 2010). Despite their ecological spe-cialization and their dependence on specific host plantsas well as pollinators and seed dispersers, mistletoes areoften found in disturbed habitats. Understanding howmistletoes thrive in different types of disturbed habitatsmay shed some light on the ecological processes behindtheir success. In hierarchical order, these processes in-volve: (i) host plants, (ii) pollinators and seed dispersers,(iii) nutrient cycling, and (iv) novel interactions (includ-ing exotic species).

Host plantsMistletoe–host relationships imply complex plant–

plant interactions that determine host competence(whether a plant species can be used as a host or not),host preference (mistletoes are present in one or moreplant species more frequently than we expect, owing totheir relative abundance), chemical interactions (second-ary compounds from the host infected by the mistletoe),and indirect interactions (facilitation as a result of over-lapping flowering or fruiting seasons between the mis-tletoe and the host). The host range gives us the firsthint of the mistletoe’s ability to persist in disturbed hab-itats. Highly-specialized mistletoes (e.g., Tristerix aphyllus,which only parasitizes a few species of cactus; Medelet al. 2004) have limited chances to persist in disturbedhabitats, but mistletoes with a wide range of hosts (e.g.,Viscum album, which can parasitize over 400 species;Barney et al. 1998) are usually common and abundant indisturbed areas (Bowen et al. 2009; Zuria et al. 2014). Also,many mistletoe species can find new hosts (includingexotic tree species) in novel habitats (Mellado andZamora 2020). Nevertheless, mistletoe performance ondifferent host species is expected to vary, either posi-tively or negatively (Roxburgh and Nicolson 2005), alongwith mistletoe metapopulation dynamics (Teodoro et al.2013).

Pollinators and seed dispersersA mistletoe may find a competent host in a dis-

turbed habitat, but this does not guarantee its long-term persistence, because most mistletoe speciesdepend on mutualist interactions for reproduction.While Misodendraceae mistletoes can be pollinated anddispersed by wind (Vidal-Russell and Nickrent 2007;Tercero-Bucardo and Rovere 2010), many other mistletoespecies have adapted to pollination by birds and insects(which favors cross-pollination; Tadey and Aizen 2001),and some neotropical mistletoes are pollinated by bats(Arruda et al. 2012; Fadini et al. 2020). Furthermore, per-haps more critical, is their dependence on seed dispers-ers to reach suitable sites (i.e., branches or stems) on thehost plants (Watson and Rawsthorne 2013). As with thehost range, mistletoe species around the world present avariable degree of specialization regarding their mutual-ist counterparts. While specialist frugivores are usuallymore effective seed dispersers, they tend to producedense aggregations (concentrating their food resources),resulting in short seed dispersal distances. By compari-son, generalist frugivores, despite being less effective,are usually involved in long-distance dispersal events(Watson and Rawsthorne 2013). Further, mistletoes inter-acting with specialist species are usually pollen- andseed-limited (Kelly et al. 2004, 2007), but those interact-ing with generalist species are not (Yule and Bronstein2018a, 2018b). Disturbed habitats are usually dominatedby a subset of generalist species (Barlow et al. 2007),

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which is likely to change the reproductive output of mis-tletoes.

Mistletoes are mainly pollinated by birds; however,insects also act as legitimate pollinators in some cases.Owing to their morphology, mistletoe flowers are usu-ally pollinated by hummingbirds and sunbirds (Aizen2003; Vidal-Russell and Nickrent 2008; Weston et al.2012). As for most plant species, no bird species areknown to be a specialists with regard to mistletoe polli-nation (Watson 2004). Thus, mistletoe–bird interactionsare highly asymmetric, because the plant depends moreon the bird than the bird on the plant (Guerra and Pizo2014). Consequently, most mistletoe pollinators are gen-eralists and thus persist in disturbed habitats (Maruyamaet al. 2019). In some mistletoe species, the fruit ripeningprocess depends on the amount of sunlight received,leading to changes in shape, color, and shape (Bach andKelly 2007; Amico et al. 2011; Fontúrbel and Candia 2018).Such changes in fruit phenotype due to habitat distur-bance are expected to influence seed dispersal andfrugivore-mediated selection (Fontúrbel and Medel2017), potentially altering the mistletoe genotype as aconsequence. On the other hand, an important fractionof mistletoe seed dispersers are specialists, showingmore symmetric interactions. Therefore, mistletoesare likely to lose their pollinators (Robertson et al.1999) or their seed dispersers in disturbed habitats(Rodriguez-Cabal et al. 2007, 2013), thereby collapsingrecruitment. Looking at the whole plant recruitmentprocess, mistletoes thriving in disturbed habitats maybe maintaining their pollination interactions, formingviable fruits after cross-pollination, but experiencing arecruitment collapse as a result of losing their seeddispersers, threatening their long-term persistence.

Nutrient cyclingMistletoes acquire water and nutrients from the host’s

xylem. To ensure their water supply, mistletoes havehigher hydric potentials than the hosts, which results inhigher nutrient concentrations in their tissues (Scalonand Wright 2015). For this reason, mistletoe litter is richin nutrients (Muvengwi et al. 2015; Ndagurwa et al. 2015;Fadini et al. 2020) and indirectly facilitates the establish-ment of many other plant species via soil enrichment(March and Watson 2007; Thomsen et al. 2018). There-fore, changes in mistletoe abundance and spatial distri-bution will also alter soil quality (March and Watson2010). Furthermore, if mistletoes shift hosts as a result ofhabitat disturbance, we can expect changes in the nutri-ent content of mistletoe litter, potentially altering facil-itation interactions with other plant species as well.

Novel interactionsAlong with land-use changes, invasive species thrive in

disturbed habitats, integrating themselves in the exist-ing ecological interactions networks (Memmott andWaser 2002). Impoverished communities (as in disturbed

habitats) are more prone to be invaded (Montero-Castañoand Vilà 2012), and invasive species can rapidly dominate(González-Varo et al. 2013). Mistletoes can interact withinvasive species at four levels: (i) hosts, for example, ex-otic Acacia spp. or Populus spp. trees are usually heavilyparasitized by mistletoes in disturbed habitats (Bowenet al. 2009); (ii) pollinators, for example, the Europeanbumblebee Bombus terrestris has invaded southern SouthAmerica, becoming the most common pollinator (Medelet al. 2018); (iii) plant neighborhood, where showy inva-sive species near mistletoes produce large flower/fruitdisplays, competing with mistletoes for pollinators andfrugivores (Fontúrbel et al. 2017b); and (iv) facilitation ofannual, weedy herbaceous species in the understory, lo-cated beneath infected trees (March and Watson 2010).We expect mistletoes to present idiosyncratic responsesto invasive species depending on their relative abun-dance and time elapsed since the invasion.

Community cascading effectsFrequently, there is a positive numeric response to

habitat disturbance (i.e., mistletoes are more abundantin disturbed habitats compared with non-disturbed hab-itats), but it also implies deep changes in their spatialarrangement (dense aggregations; Fontúrbel et al. 2015,2017b). Also, many shade-intolerant plants are benefitedby habitat disturbances and thrive, offering large flower/fruit displays, creating a strong community-wide effecton pollinators and frugivores, and reducing pollen/seeddispersal distance as a consequence (Maruyama et al.2012; Morales et al. 2012; Amico et al. 2017; Fontúrbelet al. 2017b). However, such apparent positive effect mayhave negative consequences in terms of genetic diversityloss and increased rates of inbreeding, as those densemistletoe clumps hamper gene flow and mating patternsat the landscape scale by altering pollination and seeddispersal processes (Fontúrbel et al. 2019). A summary ofthe possible outcomes of habitat disturbance on mistle-toes is presented in Fig. 2.

Climate change: expected and unexpected outcomesWhereas land-use change, resource overexploitation,

and invasive species operate at local and landscapescales, climate operates at a global scale. There is enoughscientific evidence demonstrating that temperatures onEarth are rapidly increasing, significantly exceeding nat-ural temperature changes (Walther et al. 2002; Parmesan2006). In this warming scenario, species are expected tomigrate towards cooler places (Memmott et al. 2007;Walck et al. 2011). However, this could be a challengingtask for mistletoes, as they depend on other species (i.e.,hosts, pollinators, and seed dispersers), which may dif-fer in their ability to disperse and shift their distribu-tion ranges (Rai et al. 2018; Sangüesa-Barreda et al.2018). Therefore, mistletoes may experience spatialmismatches that preclude their persistence (Ornelaset al. 2018; Fig. 3). On the other hand, phenology is an

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important aspect of plant–plant and plant–animal in-teractions for mistletoe (Teixeira-Costa et al. 2017).When mistletoes co-flower/co-fruit with their hostplants, they may be indirectly benefiting them by at-tracting pollinators/frugivores (Candia et al. 2014). Cli-mate change is likely to alter flowering/fruitingpatterns as well as the seasonal migratory/activity pat-terns of animals, potentially disrupting mistletoe fa-cilitation on host plants as flowering/fruiting overlapbecome reduced (Fig. 4). Also, these distribution rangeshifts may lead to new mistletoe–host combinations,which might have adverse effects on reproductive suc-cess, as recently reported by Mellado and Zamora(2020).

As temperatures increase, drought events are becom-ing more frequent and severe (Allen et al. 2010; Garreaudet al. 2017). Therefore, water shortages will worsen theeffects of temperature increase on plant communities(Bell et al. 2019). Mistletoes are particularly sensitive toprolonged drought events because they may drain out

the host (Mortenson et al. 2015; Bell et al. 2019), therebycommitting a “delayed suicide”, as host death inevitablyleads to mistletoe death a few months later. This phe-nomenon was reported in the Mojave Desert in Califor-nia, (Spurrier and Smith 2007) and in the Valdivianrainforest ecosystem in southern Chile (Fontúrbel et al.2017c, 2018). Unfortunately, drought effects are not onlya matter of mistletoe mortality, but they also can disruptpollination and seed dispersal interactions. During themost severe drought in 50 years in south-central Chile,the reduction in the amount of summer precipitationreduced soil water content, thereby causing a significantreduction in terms of flower and fruit production(Fontúrbel et al. 2018). Such reduction affected not onlymistletoe flower and fruit production, but also thosefrom other plants, further reducing food resource avail-ability for pollinators and seed dispersers. Thus, this maybe collapsing overall plant recruitment, resulting in cas-cade effects at the community level (Fontúrbel et al.2018). This phenomenon does not seem to be restricted

Fig. 2. Possible outcomes of land use changes on mistletoes and their cascading effects on the community via plant–plant andplant–animal interactions, and indirect facilitation interactions to other species.

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to the Valdivian rainforest, as a similar outcome wasreported for insect pollinators in the United Kingdom(Phillips et al. 2018). Moreover, mistletoe-infected treesmay experience negative consequences in terms ofgrowth and mortality under water stress conditions (Bellet al. 2019), worsening the scenario. Although more re-search is needed to fully understand this phenomenon,mistletoes can be used as “climate change monitors”,because of their dependence on plant–plant and plant–animal interactions and their sensitivity to water stress.

Conclusions and future perspectivesHumans have altered Earth’s ecosystems in every pos-

sible way, posing a major threat to all biodiversity andtheir ecosystem services, ultimately threatening theirvery own existence in the long run. In general terms, weacknowledge land-use changes, natural resource overex-ploitation, biological invasions, and climate change asthe major biodiversity loss drivers (Sala et al. 2000). How-ever, there is more to this than meets the eye, as thosedrivers are not independent of each other but can inter-act and boost their individual effects. The extent of an-thropogenic alterations to natural habitats in this area ofthe Anthropocene has produced massive changes in ashort time (Armesto et al. 2010), leading to dramatic in-

creases in the rates of species extinction (Humphreyset al. 2019). Those alterations act as strong selectiveforces changing the eco-evolutionary scenario (Kinnisonand Hairston 2007) and inducing rapid evolutionary re-sponses at unprecedented rates (Stockwell et al. 2003).The diversity of responses to anthropogenic distur-bances is complex and intertwined, and our understand-ing is limited by our current analytical abilities (andmaybe our understanding); however, mistletoes maygive us an idea as to what could we expect in the future.

This “changing world” merges novel ecosystems(Hobbs et al. 2006; new species combinations impossibleto occur naturally; Hobbs et al. 2009; Morse et al. 2014),and novel climates, giving place to a massive reshuffling

Fig. 3. Spatial mismatch scenarios among a mistletoe, itsmutualists (a pollinator and a seed disperser), and its hostplants under a climate change scenario. Owing to theirlife-history traits, mistletoes are expected to have lowerdispersal capabilities than their mutualists and their host,and consequently lower capacity to change theirdistribution ranges in response to mutualist and hostdistribution changes. [Colour online.]

Host range changes Host and mutualistranges change

Fig. 4. Temporal mismatch between a mistletoe and (a) itspollinator and (b) its seed disperser, owing to changes inphenology (changing the flowering and fruiting patternsof the plant, and the migratory or activity patterns ofanimals) as a consequence of increasing temperatures in aclimate change scenario. [Colour online.]

Time

Time

(a) Pollination

(b) Seed dispersal

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of nature that may produce non-analog ecosystems inthe near future (Fox 2007). Human beings are currentlynegatively affecting millions of years of evolutionary his-tory and causing a massive extinctions, but as some spe-cies go extinct others arrive, favored by new climates andfacilitated by the ability to become invasive species(Simberloff and Von Holle 1999; Simberloff 2006; Fox2007). Let us think like a mistletoe… thriving in a de-graded habitat remnant, parasitizing exotic trees in highabundances but experiencing water stress due to pro-longed droughts, lacking an effective seed disperser andlosing genetic diversity because of a hampered pollina-tion process, facilitating and competing with invasivespecies, and dealing with a new plant community and amajor turnover in animal visitor species. If a single spe-cies has to face that many changes, what can we expectin the actual ecological and evolutionary scenario of anentire ecosystem is beyond our comprehension. Earthhas undergone many big changes during the past4.5 billion years, and there is no reason to believe thatlife will cease to exist in the Anthropocene. Biodiver-sity will find its own way, and the recombination ofnovel ecosystems and climates will lead to a non-analog future, from which humans will probably beabsent.

“There is grandeur in this view of life, with its several powers,having been originally breathed into a few forms or into one; andthat, whilst this planet has gone cycling on according to the fixedlaw of gravity, from so simple a beginning endless forms mostbeautiful and most wonderful have been, and are being, evolved”

Charles Darwin, The Origin of Species by Means of NaturalSelection (1859)

AcknowledgementsEnriching discussions with Antonio Lara and Guillermo

Amico helped me to develop some of the ideas discussedhere. I am grateful to Dave Shaw for inviting me to join themistletoe workshop at the IUFRO 2019 meeting and for hiscomments on an earlier version of this review. The writingof this paper was supported by Fondo Nacional de Desar-rollo Científico y Tecnológico (FONDECYT project 11160152)and Natural Environment Research Council project NE/S011870/1 (SURPASS2).

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488 Botany Vol. 98, 2020

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