Early detection of Youngia japonica (L.) DC. (Asteraceae) in São Miguel Island, Azores, Portugal

Abstract

Youngia japonica (L.) DC. was recently discovered on the Azorean island of São Miguel. This species is a cosmopolitan herb that has been reported to be invasive in several regions of the world. It is unclear when and how this plant arrived in São Miguel, Azores. Nevertheless, we hypothesize that this is an unintentional and recent introduction. The populations are expanding in São Miguel, and action is needed to mitigate potential damage to native ecosystems.

Introduction

The genus Youngia Cass. (Asteraceae) comprises circa 40 species (POWO 2023; Shi and Kilian 2011) that are native to warm temperate and tropical eastern Asia (Shi and Kilian 2011). This genus is closely related to Lapsana L. and Crepis L. phylogenetically and morphologically (Slanis and Perea 2011). Morphologically, Youngia differs from Crepis by possessing compressed, unequally ribbed achenes, and from Lapsana by the presence of a pappus (Figure 1). Youngia japonica (L.) DC. is the most widely distributed species of the genus. In fact, its native range includes China, India, Japan, Korea, the Malay Peninsula, the Philippines, and Taiwan (Ling and Shih 1997). It has been introduced to five continents: Africa, South and North America, Australia, and Europe (Acevedo-Rodríguez and Strong 2007; Pagad et al. 2018; Pyke 2016). Youngia japonica is becoming an invasive weed worldwide, having established itself in parts of Europe, southern Africa, Australia, the Pacific Islands, and the eastern United States (Barker et al. 2005; Botha 2001; Botond and Zoltán 2004; Nakamura et al. 2012).

Figure 1. Youngia japonica and details of its (A) leaves and (B) flower heads (capitula). (C) A population near Lagoa das Furnas, São Miguel Island, Azores.

To date, no occurrence existed for this species in the Azores archipelago; the species appears to be expanding its range across São Miguel island, appearing mainly in roadsides, lawns, and highly disturbed natural areas (Figure 2).

Figure 2. Distribution map with the red dots showing the sightings of Youngia japonica across São Miguel Island in the Azores archipelago.

This invasion alert reports the presence of Y. japonica in the Azores archipelago and aims to summarize the current knowledge of the natural history and invasion biology of this species.

Natural History, Taxonomy, and Distribution

Taxonomy

Youngia has a complex and puzzling taxonomy (Yahara 1995). However, studies from Nakamura et al. (2012, 2013) clarified its taxonomy and proposed the following. First, Youngia japonica subsp. longiflora should be considered a distinct lineage from Y. japonica and thus treated as a separate species (i.e., Youngia longiflora). Moreover, three subspecies of Youngia japonica should be recognized (i.e., Youngia japonica subsp. japonica, Youngia japonica subsp. formosana, and Youngia japonica subsp. monticola). Youngia japonica subsp. japonica differs from the other two subspecies by having brown achenes that are less than 2-mm long. The inflorescence axes differentiate the other two subspecies. Youngia japonica subsp. formosana has densely pubescent inflorescence axes, at least at the base, while Y. japonica subsp. monticola inflorescence axes are glabrous or slightly puberulous at the base. The use of proper names for these ecologically and morphologically distinct subspecies is critical for genus nomenclature and biogeography, as well as invasiveness control activities (Nakamura et al. 2013). As a result, we conducted a detailed examination of Azorean plants that possessed achenes less than 2-mm long belonging to Y. japonica subsp. japonica.

Plant Traits

Youngia japonica is an annual or biennial species. According to the Flora of China Editorial Committee (2018), Y. japonica basal leaves are disposed as a rosette and are obovate to oblanceolate, pinnatipartite, or pinnatisect. The leaves and lower parts of the plant are variably pubescent, with weak, simple hairs scattered across the surface. The inflorescence forms a panicle or a corymbose cyme, with slender branches. The capitula are small and are composed of 10 to 20 florets, with phyllaries abaxially glabrous and adaxially appressed pubescent. The achene is light brown to dark reddish or purplish brown, ribbed, and fusiform with an attenuate apex. The pappus is white and has a single whorl of barbed hair.

Distribution Worldwide and in the Azores Archipelago

Youngia japonica is native to China, India, Japan, Korea, the Malay Peninsula, the Philippines, and Taiwan (Ling and Shih 1997). However, its nonnative range includes Africa, North and South America, Australia, Spain (Acevedo-Rodríguez and Strong 2007; Pagad et al. 2018; Pyke 2016); several Pacific islands (PIER 2016); and in the Macaronesia biogeographic region, Madeira (Jardim and Menezes de Sequeira 2021), Tenerife, and Gran Canaria (Verloove 2017). For the first time, we register the occurrence of Y. japonica in the Azores archipelago. This species has only been observed so far on the island of São Miguel (Figure 2), but it is already widely distributed on the island (Table 1).

Table 1. Observed Youngia japonica populations and their locations, altitudes, habitats, dates of observation, collectors’ names, and herbarium voucher numbers when collected.

Phenology

In its native range, Y. japonica flowering and fruiting periods vary depending on the region. In China, this taxon blooms and bears fruit from February to December (Flora of China Editorial Committee 2018), and in India, from October to April (India Biodiversity Portal 2018). In its nonnative area, this taxon has been seen to flower year-round (Davidse et al. 2018), a trait that has also been observed in the specimens from the island of São Miguel in the Azores archipelago.

Uses

Youngia japonica young leaves are consumed as a vegetable and used in traditional medicine. In terms of edibility, in its native range (i.e., China, India, Japan, Korea, the Malay Peninsula, the Philippines, and Taiwan), Y. japonica was consumed during times of famine, and nowadays is used in salads in North America (Ooi et al. 2004). It is used in folk medicine to treat colds and sore throats, as a diuretic to promote blood cleansing, and as an herbal treatment for diarrhea (Munira et al. 2018). It is used in external applications to treat boils, mastitis, shingles, and bruises (Ooi et al. 2004). Additionally, studies have shown that this species has anti-tumor activity and inhibitory potential against respiratory syncytial virus (Ooi et al. 2004), and it is a source of antioxidants (Kaur et al. 2019). Youngia japonica has also been shown to be a hyperaccumulator of cadmium (Yu et al. 2021), which may be useful for phytoremediation. Finally, it is used as an ornamental in various locations (Loewenstein and Loewenstein 2005).

Habitat

Youngia japonica is commonly found over a broad range of environmental conditions from coastal areas to mountain ranges and from forest margins to disturbed sites such as wastelands (Peng et al. 1998); in moist and semi-shaded habitats, but it is also found in intact or minimally disturbed natural areas (Rojas-Sandoval 2020).

Dispersal

Youngia japonica is an autogamic species, exhibiting high seed set, even when pollination rates are low (Hauber et al. 1989). The seeds are readily dispersed by wind (Peng et al. 2018) and water (Kalaman and Marble 2023) and by contamination of soil, crop, and grass seeds (Drake 1998; Kalaman and Marble 2023). Moreover, Y. japonica seeds have been observed as a contaminant in seed lots of cultivated species (Hauber et al. 1989; USDA-NRCS 2018)

Invasive Significance

Plant invasions can result in adverse impacts on agriculture, the environment, and the economy. Weed-related crop yield losses are determined by a variety of factors, including weed emergence time, weed density, weed type, and crop, among others, and if not controlled, can result in a 100% yield loss (Chauhan 2020). Annually, in the United States, weeds cost US$33 billion in lost crop production (Pimentel et al. 2005). Youngia japonica is a weed of coffee (Coffea arabica L.), sugarcane (Saccharum officinarum L.), and wheat (Triticum aestivum L.) (Dangol 2013; Davidse et al. 2018; McIntyre 1991; Vibrans 2018). It may also inhibit the growth of coffee and alfalfa (Medicago sativa L.) through allelopathy (Chérigo et al. 2017; Yin et al. 2008), leading to yield and economic losses.

Environmentally, nonnative species are recognized as one of the major drivers of global biodiversity loss (Shabani et al. 2020). In fact, invasive species can have a detrimental impact on the ecosystems they invade, degrading ecosystem services and causing severe damage to economies and social livelihoods (Sudmeier-Rieux and Ash 2009). Youngia japonica invades both disturbed and undisturbed natural areas. Across the United States, this species has been described as “very common” and is spreading rapidly, invading intact or minimally disturbed forests, prairies, and coastal plains (Swearingen and Bargeron 2016). It grows well in response to human disturbance and is very common in areas such as roadsides, cultivated fields, lawns, pastures, and forest margins (Loewenstein and Loewenstein 2005; PIER 2016; Swearingen and Bargeron 2016; USDA-NRCS 2018; Weakley 2015). More importantly, it has been reported growing in Haleakala National Park in Hawaii, in nearly intact wet forests (Wagner et al. 1999). Youngia japonica was assessed by the Hawaii-Pacific Weed Risk Assessment (HPWRA) system as a high-risk species (score 14); thus, it is highly invasive in Hawaii and other tropical Pacific islands (HPWRA 2019). Moreover, it is mentioned on several lists of invasive species that support policy makers in the management of invasive species around the world (i.e., Invasive Species Compendium Datasheet and Database of Plants Invading Natural Areas in the United States, https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.117921).

Several activities, such as clearing native vegetation for cereal crops and the introduction of numerous crops and forage, forest, ornamental, and hedgerow plant species, have had a significant impact on native vegetation since human settlement in the Azores (Silva and Smith 2004). In addition to this, the recent intensification of pasture production and cattle grazing in the Azores has lead to eutrophication of soils (Pinheiro et al. 2007). In fact, a study conducted by Kurz et al. (2006) shed light on the shift in nutrient concentration caused by cattle and discovered an increase in particulate N, organic P, and K concentrations. Studies on plant invasions have provided evidence that invasive species abundance is positively correlated with proximity to disturbed areas (González-Moreno et al. 2015) and the amount of N in the soil (Nackley et al. 2017; Stohlgren et al. 1999). Based on the abovementioned research, the Azores provide an ideal habitat for invasive species such as Y. japonica.

It is unknown how and when this plant arrived in São Miguel, Azores. Species checklists attempt to reflect locations’ species diversity. The most recent Azorean checklist was published in 2010 (Silva et al. 2010), and the online databases that are constantly updated, such as Portal da Biodiversidade dos Açores (2022) and eAZFlora (https://eazflora.org), do not have Y. japonica listed. Regarding its introduction pathway, according to the literature, a possible pathway is that it came as a contaminant in the seed lots of cultivated species (USDA-NRCS 2018). Based on its dominance on urban lawns and its presence in horticultural and agricultural fields, we hypothesize that Y. japonica was introduced recently as a contaminant in seed lots and that its occurrence in highly disturbed natural areas represents the start of an ongoing expansion that could reach intact forests, as the plant did in Hawaii.

No specific impacts of Y. japonica have been identified. However, given its propagation capacity, environmental versatility, allelopathic behavior, and recognized ecological risk by the HPWRA system, Y. japonica is a high-risk species for the Azores region, and monitoring must be undertaken in the vicinity of sites where it is known to occur (Figure 2). Youngia japonica control is even more crucial than ever. Recently, the Delta Cafés, the Azores Government, and the Association of Azorean Coffee Producers partnered in motivating growers to plant and produce coffee in the Azores. They provided financial support and encouragement to extant coffee producers for the expansion of their plantations and extended this support to new producers, promoting the cultivation of coffee in the Azores. This resulted in an unique and limited batch with 100% Azorean coffee that was commercialized by Delta Cafés (https://www.deltacafes.pt) and was referred to as “the impossible coffee,” because Europe’s climate did not provide the ideal conditions for the production of coffee.

Hence, the early detection of newly introduced species (particularly those with invasive behavior) is critical not only for minimizing potential damage to native populations and the ecosystem, but also, if Y. japonica colonizes coffee plantations, protecting the yield of the newest Azorean coffee, which is produced in small quantities. Therefore, because eradication is still feasible, we recommend the monitoring of and quick interventions for the rapidly spreading populations of Y. japonica in the Azores.

Control

When the plants are young, they can easily be pulled out. However, both above- and belowground plant parts must be removed. Mowing is ineffective, because this herbaceous plant will regrow quickly if root structures remain (USDA-NRCS 2018). It is critical for mechanical management of the plant to remove it before it matures and becomes deeply rooted. Moreover, the removal of plants should be performed before seed set, and care must be taken not to spread seeds to adjacent areas.

Mulching can help prevent any seeds in the soil from germinating or from falling into the soil. Natural mulches should be applied at least 5-cm (2-inches) deep to non-turf areas such as planting beds and foot paths for the best results (Unruh et al. 2020).

Chemical control is only recommended for highly invaded locations where mechanical control is no longer possible. According to Neal and Derr (2005), preemergence herbicides such as flumioxazin and tank mixes of oxyfluorfen and pendimethalin may control Y. japonica. Preemergence herbicides must be applied before weed emergence and incorporated after application to be effective. Most preemergence herbicides are generally effective for 6 to 12 wk and should be reapplied 6 to 9 wk later for optimum control (Unruh et al. 2020). Regarding postemergence treatment, pelargonic acid and broad-spectrum or nonselective herbicides such as glyphosate, glufosinate, and diquat are recommended (Kalaman and Marble 2023). However, caution should be exercised, because this species has shown resistance to herbicides such as diquat and paraquat (Hanoika 1987; Watanabe 1990).