A review of potential biological controls for Ailanthus altissima

Abstract

Ailanthus altissima (Mill.) Swingle (Sapindales: Simaroubaceae) (tree-of-heaven) is an invasive tree species first introduced to the United States in 1784. With high rates of sexual reproduction, rapid growth, and prolific vegetative sprouting, A. altissima is an aggressive competitor that reduces native plant diversity and is difficult to manage beyond small-scale infestations. In the United States, the issues associated with Ailanthus management were compounded by the 2014 arrival of Lycorma delicatula (spotted lanternfly). Lycorma delicatula coevolved with A. altissima, its primary host, in eastern Asia. Suppression of A. altissima is recommended as an important strategy to slow the spread of L. delicatula. Due to the inadequacy of traditional control methods to manage A. altissima, biological controls are desired. Several potential biological control agents have been proposed for A. altissima. This review discusses current research on several promising candidates, specifically a native fungus, Verticillium nonalfalfae Inderb. et al. (Hypocreales: Plectosphaerellaceae); a trunk-boring beetle, Eucryptorrhynchus brandti (Harold) (Coleoptera: Curculionidae: Cryptorrhynchinae); and an eriophyid mite, Aculops ailanthi (Lin-Fuping, Jin-Changle & Kuang-Haiya) (Arachnida: Eriphyidae). A list of other possible biological control agents is also provided. We discuss unanswered questions for each species, the limits of biological controls in this system, and call for further research on integrated pest management practices for managing A. altissima.

Introduction

Ailanthus altissima (Mill.) Swingle (Sapindales: Simaroubaceae) (hereafter Ailanthus) is a fast-growing deciduous tree often considered one of the most invasive plants in North America due to its deleterious effects on native biodiversity (Kasson et al. 2013, Sladonja et al. 2015, Brooks et al. 2021). Known commonly as the tree-of-heaven, Ailanthus is native to the temperate forests of eastern Asia but is now found on every continent except Antarctica (Sladonja et al. 2015). Humans are responsible for Ailanthus’ establishment outside its natural range, as it was intentionally introduced to many countries due to its aesthetic value and tolerance for disturbed habitats (Feret et al. 1974). Ailanthus was first brought from China to France in the 1740s (Hu 1979). Coinciding with “Chinoiserie,” an increased interest in Chinese culture, Ailanthus was subsequently traded throughout Europe and brought to the United States in 1784 (Kasson et al. 2013, Schley et al. 2023). Ailanthus is currently naturalized in over 40 US states (Kasson et al. 2013). Despite its modern invasive status, Ailanthus seedlings can still be purchased in the United States for as little as $26 (Wholesale Nursery Co. 2024c).

Adaptations for growth and reproduction are a large part of the invasion success of Ailanthus. Ailanthus is one of the fastest-growing trees in North America; seedlings can reach up to 2 m in height in their first year (Knapp and Canham 2000). Mature female trees may produce over 300,000 samaras annually, with germination rates up to 98% (Kowarik and Säumel 2007). Ailanthus can also reproduce asexually. Vegetative sprouts can emerge at the base of an existing tree from the stem or root crown (Kowarik and Säumel 2007), and shoots may arise from lateral roots as far as 27 m from the parent tree (Fryer 2010). The emergence of vegetative shoots may be a stress response by the species, making eradication with conventional methods difficult or impossible on the landscape scale.

Allelopathy is a common trait of invasive plants (Kalisz et al. 2021). Allelopathic plants secrete secondary metabolites into their environments, which interact with other organisms directly or by disrupting their allelochemicals (Rice 2012). The secondary metabolites in Ailanthus include a few alkaloids and many quassinoids, which are active against microorganisms, insects, and plant competitors (Heisey 1990). In Ailanthus, the primary herbicidal quassinoid, ailanthone, has been studied for its medicinal properties (Chang and Woo 2003, Okunade et al. 2003, Kundu and Laskar 2010, Wang et al. 2018) and potential as a commercial bioherbicide (Heisey 1996, De Feo et al. 2003, Heisey and Kish Heisey 2003, Kozuharova et al. 2022). Ailanthone possesses inhibitory properties that suppress competition and are thought to contribute to the invasion success of Ailanthus (Gómez‐Aparicio and Canham 2008). The effect of allelopathy in Ailanthus may differentially affect native and nonnative plants. Nonnative plants reportedly have a higher tolerance to its allelopathy, potentially contributing to the establishment of other invasive species (Small et al. 2010).

In the United States, increased urgency in managing Ailanthus followed the 2014 arrival of the spotted lanternfly, Lycorma delicatula (White) (Hemiptera: Fulgoridae). Ailanthus is the preferred host species of L. delicatula (Dara et al. 2015). Ailanthus has been spreading in the United States for over 200 years, particularly in urban centers and along industrial corridors, which provide L. delicatula with ample hosts, often along highways and railroads, that aid in its rapid dispersal (Urban et al. 2021, Elsensohn et al. 2024). Early instars are highly polyphagous, but their diet narrows with age, eventually feeding almost entirely on Ailanthus (Song et al. 2018, Dechaine et al. 2021, Elsensohn et al. 2023). While L. delicatula does not require Ailanthus to complete development, its survival and fecundity are reduced without access to its preferred host (Uyi et al. 2020). In addition to the trophic relationship, L. delicatula deploys defensive adaptations related to Ailanthus. The planthopper sequesters the allelochemical ailanthone, which makes it distasteful to avian predators (Song et al. 2018, Johnson et al. 2023). Sequestering ailanthone is also associated with aposematic coloring (Song et al. 2018).

In its native range, L. delicatula is considered a minor pest of trees, except for its primary host, Ailanthus (Zhang et al. 2023). In the United States, L. delicatula is primarily an indirect pest of grape (Vitus spp.) (Leach and Leach 2020). Experimental evidence suggests L. delicatula has a high affinity for grape and experiences higher fitness when feeding on grape than other non-Ailanthus hosts (Elsensohn et al. 2023). Feeding stress and black sooty mold associated with copious honeydew contribute to grapevine death (Dara et al. 2015, Leach and Leach 2020). Fortunately, L. delicatula does not appear to be causing significant harm to native tree species in the United States (Lavely et al. 2022) aside from feeding injury as a potential secondary infection route in red maple (Acer rubrum) (Hoover et al. 2023). Ailanthus populations in forests adjacent to vineyards may pose an economic threat as a refuge for L. delicatula populations (Keller et al. 2020, Leach et al. 2023). Early intervention methods to manage L. delicatula include reducing Ailanthus stands near infested sites and using Ailanthus as trap trees (Parra et al. 2017, Urban et al. 2021). Suppressing Ailanthus populations is an established strategy to slow the spread of L. delicatula (Parra et al. 2017).

The best management strategy for invasive species is to prevent their initial establishment with robust regulatory and monitoring practices (Roy et al. 2023). However, when eradication is no longer feasible, integrated pest management (IPM) calls for a combination of cultural, chemical, and biological controls for the suppression of pest species (Ehler 2006, Venette and Koch 2008). In the United States, Ailanthus has few closely related genera, which suggests the threat of nontarget effects of biocontrol agents is low (McAvoy et al. 2023). Given the inadequacy of conventional control methods and the high germination rate, rapid growth, asexual reproduction, and widespread distribution of Ailanthus, biological controls are highly desired (Ding et al. 2006, Wickert et al. 2017, Soler and Izquierdo 2024).

The last significant review of biocontrol options for Ailanthus by Ding et al. (2006) produced a substantial list of Ailanthus natural enemies in its introduced and native ranges. Of the over 130 species listed, only 12 were observed to be monophagous on Ailanthus (Table 1). Releasing a polyphagous arthropod or pathogen into the environment may suppress the intended pest, but the risk of nontarget effects would prohibit their release. Host specificity is a stringent requirement for potential biological controls (Grevstad et al. 2021). The purpose of this review is to provide an updated discussion on potential biological control agents for Ailanthus, with an emphasis on current research associated with 3 organisms: a fungus native to North America, Verticillium nonalfalfae Inderb. et al. (Hypocreales: Plectosphaerellaceae); the Ailanthus feeding weevil, Eucryptorrynchus brandti (Harold) (Coleoptera: Curculionidae: Cryptorrhynchinae); and the Ailanthus leaf curl mite, Aculops ailanthi (Lin-Fuping, Jin-Changle, and Kuang-Haiyua) (Arachnida: Eriphyidae).

Table 1.

Natural enemies and potential biocontrol agents of Ailanthus altissima

Species	Part(s) of Ailanthus attacked	Known distribution	Current biocontrol potential, status	References
Animalia  Arthropoda   Arachnida    Trombidiformes     Eriophyidae      Aculops ailanthi	Leaves	USA, Italy, Hungary	Yes, research ongoing	Ripka and Érsek (2014), De Lillo et al. (2017), Skvarla et al. (2021), Bielski et al. (2024)
Insecta     Coleoptera      Buprestidae       Agrilus smaragdifrons	Bark	USA	Unknown	Hoebeke et al. (2017)
Curculionidae       Ecryptorrhynchus brandti	Bark, phloem, leaves	China	Yes, research ongoing	Kok et al. (2008), Herrick et al. (2011), McAvoy et al. (2023)
Eucryptorrhynchus scrobiculatus	Roots	China	Unlikely	McAvoy et al. (2014), Ji et al. (2017), Ma et al. (2022)
Hemiptera        Dictyopharidae         Orthopagus lunulifer	Unknown	China	Unknown	Ding et al. (2006)
Fulgoridae         Lycorma delicatula	Phloem	China, S. Korea, Japan, USA	No potential	Urban and Leach (2023)
Lepidoptera        Attevidae         Atteva aurea	Leaves, flowers, seeds	USA, Canada	Unknown	Kok et al. (2008), Becker (2009), Van Zandt et al. (2020)
Fungi  Ascomycota   Dothideomycetes    Botryosphaeriales     Botryosphaeriaceae      Phyllosticta ailanthi	Leaves	China	Unknown	Ding et al. (2006)
Capnodiales     Mycosphaerellaceae      Cercospora glandulosa	Leaves	USA, China	Unknown	Ding et al. (2006)
Pleosporales     Pleosporaceae      Alternaria ailanthi	Leaves	China	Unknown	Ding et al. (2006)
Leotiomycetes    Erysiphales     Erysiphaceae      Phyllactinia ailnathi	Leaves	China	Unknown	Ding et al. (2006)
Uncinula delavayi	Leaves	China	Unknown	Ding et al. (2006)
Sordariomycetes    Diaporthales     Valsaceae      Cytospora ailanthi	Leaves	China	Unknown	Ding et al. (2006)
Hypocreales     Plectosphaerellaceae      Verticillium nonalfalfae	Xylem	USA, Europe	Yes, research ongoing	Schall and Davis (2009a, 2009b) Inderbitzin et al. (2011), Brooks, Wickert, et al. (2020a), Hrabovský and Hladík (2024)
Basidiomycota   Pucciniomycetes    Pucciniales     Coleosporiaceae      Coleosporium sp.	Unknown	China	Unknown	Ding et al. (2006)
Incertae sedis      Aecidium ailanthi	Leaves	China	Unknown	Ding et al. (2006)

Pathogens of Ailanthus

Verticillium nonalfalfae

Verticillium nonalfalfaeInderb et al. (2011), formerly synonymous with Verticillium albo-atrumReinke and Berthold (1879), is a cosmopolitan ascomycete fungus of the family Plectosphaerellaceae (Inderbitzin et al. 2011) (Table 1). Currently, 10 known species comprise the genus Verticillium, and all are plant pathogens that cause Verticillium wilt (Pegg and Brady 2002, Inderbitzin et al. 2011). Verticillium wilt has been observed on Ailanthus several times internationally in the last century (Gravatt and Clapper 1932, Kasson et al. 2013, Maschek and Halmschlager 2017, Pisuttu et al. 2020, Hrabovský and Hladík 2024). Between 2002 and 2008, researchers in Pennsylvania found over 8,000 dead canopy Ailanthus trees due to Verticillium wilt caused by Verticillium dahliae Kleb. and V. nonalfalfae (Schall and Davis 2009a). In 2009 and 2012, Verticillium wilt of Ailanthus was also found in Virginia and Ohio, respectively (Rebbeck et al. 2013, Snyder et al. 2013, Pile Knapp et al. 2022). Subsequent greenhouse and field trials concluded V. dahliae caused disease only in seedlings, while V. nonalfalfae was determined to be the primary pathogen associated with Verticillium wilt in Ailanthus (Schall and Davis 2009a, Brooks et al. 2020a). Further studies concluded that coinfection of V. dahliae with V. nonalfalfae did not result in fungal hybridization or have a synergistic effect on virulence (Brooks et al. 2020a). Symptoms of Verticillium wilt in Ailanthus progress from foliar chlorosis to necrosis, wilt, defoliation, and eventual death (Schall and Davis 2009a). Staining of xylem vessels can also be observed following bark removal (Kasson et al. 2015, Brooks et al. 2020b).

Recent research shows that V. nonalfalfae can be cultured and used as a biocontrol product for Ailanthus by filtering conidia from hyphae and producing an aqueous inoculum in solutions of 1 × 10⁷ spores ml⁻¹ (Schall and Davis 2009b, Kasson et al. 2015, Brooks et al. 2020a). The solution may be administered to Ailanthus via stem injection or “hack and squirt” (Maschek and Halmschlager 2016, Brooks et al. 2020a). A trial of over 30 strains of V. nonalfalfae resulted in 1 strain with high virulence, VnAa140, that was chosen for development as a commercial biocontrol agent (Kasson et al. 2014). VnAa140 has shown high host specificity for Ailanthus (Kasson et al. 2015) despite initial concern over deaths of striped maple (Acer pensylvanicum) and black locust (Robinia pseudoacacia) in experimental plots. None of these dead trees showed wilt symptoms (Kasson et al. 2015), and deaths were instead attributed to the canker fungus Botryosphaeria dothidea (Cesati and De Notaris) (Botryoshpaeriaceae: Botryosphaeriales) and the locust borer Megacyllene robiniae Forster (Coleoptera: Cerambycidae), respectively (Kasson et al. 2015).

Compared to conventional methods, interest in the use of V. nonalfalfae as a biocontrol is attributed to its ability to survive in the soil and spread to uninfected Ailanthus trees. Ailanthus grows extensive lateral roots from which shoots emerge (Kowarik and Säumel 2007). These roots and those from nearby Ailanthus trees can merge, forming networks of connected trees (Kowarik and Säumel 2007, O’Neal and Davis 2015). O’Neal and Davis (2015) demonstrated the ability of V. nonalfalfae to spread through root grafts using dye translocation and by inoculating a single stem with V. nonalfalfae, which resulted in the infection of 187 root sprouts after 1 year. The high host specificity of V. nonalfalfae, its ability to infect new Ailanthus through the soil or connected roots, and its long-term survivability in soil, make it a strong candidate for biological control (Harris et al. 2013, Kasson et al. 2015, O’Neal and Davis 2015). The development of the VnAa140 strain as a commercial bioherbicide in the United States is ongoing.

Additional Fungal Species

Ding et al. (2006) also named 8 monophagous fungal species known to infect Ailanthus (Table 1). Of these species, only 1, Cercospora glandulosa Ellis and Kellerm, was known to occur in the United States. Other polyphagous fungi or species with unknown host specificity have also been proposed, but all require further investigation to confirm their specificity to Ailanthus (Ding et al. 2006, Kasson et al. 2014). While V. nonalfalfae is the only fungal species seriously discussed as a candidate for biological control, it is important that managers continue to monitor Ailanthus populations for signs of other microbial pathogens.

Arthropod Antagonists of Ailanthus

Eucryptorrhynchus brandti

Eucryptorrhynchus brandti is a tree-feeding weevil native to eastern Asia, where it is considered a significant pest of Ailanthus (Zhang et al. 2017, Yang et al. 2019) (Table 1). Eucryptorrhynchus brandti adults become reproductively mature by eating Ailanthus buds and leaves (Guo et al. 2019). Larvae of E. brandti develop under the bark in high densities leading to tree death (Guo et al. 2019). In 2005, several hundred E. brandti were imported from China to the United States to study its potential for use as a biocontrol of Ailanthus (Kok et al. 2008, Herrick et al. 2011). Host specificity testing has demonstrated the weevil is highly selective for Ailanthus as feeding was observed on only 3 other Simaroubaceae species found in the United States, Simarouba glauca, Leitneria floridana, and L. Pilosa, with reduced fecundity and survival compared to feeding only on Ailanthus (Herrick et al. 2011, McAvoy et al. 2023). The potential effect of E. brandti on these related native North American tree species is not considered problematic (Herrick et al. 2011, McAvoy et al. 2023). Eucryptorrhynchus brandti may be able to vector V. nonalfalfae, adding to its potential as a biocontrol agent (Snyder et al. 2012). The Technical Advisory Group with USDA APHIS in 2022 recommended field release of E. brandti based on the petition submitted by the E. brandti biological control group at Virginia Tech, Blacksburg, VA, United States (McAvoy et al. 2023). At the time of this writing, the status of this agent is still under review with the US Fish and Wildlife Service.

A closely related species, Eucryptorrhynchus scrobicaulatus (Motschulsky), formerly E. chinensis, feeds on the roots of Ailanthus as larvae (McAvoy et al. 2014, Ji et al. 2017, Ma et al. 2022). Due to the difficulty of rearing this species, it is not being considered as a biocontrol agent.

Aculops ailanthi

Eriophyid mites of the genus Aculops have been suggested as potential biocontrol agents for Ailanthus around the globe (Ding et al. 2006, Ripka and Érsek 2014, De Lillo et al. 2017). Eriophyid mites feed directly on leaf tissues, which interferes with host development (Marini et al. 2021). One species, Aculops ailanthi (Lin-Fuping, Jin-Changle, and Kuang-Haiyua) (Trombidiformes: Eriophyidae), has been described on Ailanthus in Europe and several US states, including Pennsylvania, West Virginia, Maryland, Virginia, and Michigan (Skvarla et al. 2021, Bielski et al. 2024). Feeding by Ac. ailanthi on Ailanthus leaves causes chlorosis, curling, stippling, premature drop, necrosis, and host death (Skvarla et al. 2021, Bielski et al. 2024). Death of Ailanthus attributed to Ac. ailanthi has only been observed in potted seedlings in greenhouses (Skvarla et al. 2021, Bielski et al. 2024). Preliminary observation of the mites outside greenhouses suggests they may prefer and only cause significant damage to young plants and leaves (Skvarla et al. 2021, Bielski et al. 2024). Field trials are warranted to determine the effect of the mite on mature trees and whether effective populations can establish in natural environments.

While Ac. ailanthi is well documented on Ailanthus, further study is needed to demonstrate the host specificity and impact on nontarget species before it is considered for release as a biocontrol agent. The species’ phylogeny must also be resolved. For example, Ac. ailanthi may be synonymous with several other Aculops and Aculus species due to their small size and difficulty of identification without electron microscopy or molecular analysis (De Lillo et al. 2017, Marini et al. 2021, Skvarla et al. 2021). The geographic range and phenology of Ac. ailanthi are also understudied. Eriophyid mites are thought to disperse primarily through the air; therefore, wind exposure may provide opportunities for Ac. ailanthi to reach new Ailanthus stands (Kiedrowicz et al. 2017). However, basic aspects of their biology, such as the overwintering stage, remain unknown (Bielski et al. 2024).

Others

Agrilus smaragdifrons

The East Asian metallic wood-boring beetle, Agrilus smaragdifrons Ganglbauer (Coleoptera: Buprestidae), is an Ailanthus specialist first described in North America in 2017 (Hoebeke et al. 2017). Initial reports of Ag. smaragdifrons were from a bycatch in monitoring traps for the closely related emerald ash borer (Agrilus planipennis Fairmaire (Coleoptera: Buprestidae)) (Hoebeke et al. 2017). While Ag. planipennis is widely known for devastating ash populations (Herms and McCullough 2014), there has been little study of the impact or specificity of Ag. smaragdifrons to Ailanthus.

Atteva aurea

The Ailanthus webworm moth, Atteva aurea Fitch (Lepidoptera: Attevinae), formerly Atteva punctella (Cramer) (Lepidoptera: Yponomeutidae), is a specialist herbivore native to Central and North America (Becker 2009). The flowers, seeds, and leaves of Ailanthus are fed upon by Atteva aurea (Kok et al. 2008). Caterpillars of this species build communal nests by folding back terminal leaflets, often breaking the rachis, and stitching together leaves with a dense, irregular web. While this species does not appear to cause severe damage to mature Ailanthus, it may completely defoliate seedlings or immature trees (Kok et al. 2008). Atteva aurea produces as many as 4 overlapping generations per year. The larval stage is the most damaging and is present throughout the Ailanthus growing season. Large populations of At. aurea are commonly found in Ailanthus stands in the United States (Kok et al. 2008). While often proposed as a potential biological control of Ailanthus, At. aurea has not been formally studied as such. Additional research must be conducted to determine if At. aurea moths are pollinators of Ailanthus, which may counteract its potential as a biological control (Van Zandt et al. 2020).

Lycorma delicatula

The spotted lanternfly is not considered a potential biological control due to its pest status and known impact on Vitis spp. (Urban and Leach 2023). However, it is important to note that feeding stress caused directly by L. delicatula and the black sooty mold associated with its honeydew can kill Ailanthus (Hoover et al. 2023). The release of biological controls within L. delicatula infestations may have a synergistic effect on Ailanthus, but this concept requires experimental confirmation. Whether L. delicatula is capable of vectoring pathogens, like V. nonalfalfae, between Ailanthus populations is also understudied (Brooks et al. 2020c). Studies are ongoing by researchers at USDA, Virginia Tech, and other universities to test the effect of Verticillium wilt in Ailanthus on L. delicatula fitness and whether L. delicatula can vector V. nonalfalfae.

Towards Ailanthus Biological Control

Ailanthus altissima is a resilient organism. Unburdened by humans from the limitations imposed by its evolved setting, Ailanthus will continue to proliferate around the globe (Brown and Barney 2021). Given the inadequacy of conventional control methods to keep up with this tree’s rapid growth and vegetative reproduction, biological controls are of high interest. However, it is important for stakeholders to understand that no single biological control species will be a panacea. For instance, none of the proposed organisms have geographic ranges, currently or potentially, that encompass the entirety of Ailanthus’ distribution globally or within the United States (Wang et al. 2022). Some organisms, like At. aurea and Ac. ailanthi, only appear to damage seedlings or fresh leaves. Verticillium nonalfalfae may be able to spread through the soil and connected roots to other Ailanthus individuals, but the fungus does not have an obvious means of dispersal between distant populations. These limitations may be addressed by the simultaneous release of multiple biological controls. While combining multiple biological controls is not a novel concept (Denoth et al. 2002), there is currently no research on the interactions between any of the proposed Ailanthus biocontrols. The use of natural enemies in this system in conjunction with chemical controls is also understudied (Hrabovský and Hladík 2024).

Social perceptions may also limit the effectiveness or application of these biological controls (van Lenteren 2012, Deguine et al. 2021). Many of the candidate organisms induce a steady progression of symptoms prior to death rather than immediate mortality. This might be aesthetically unpleasing or poorly understood, so many may still opt for the immediate, albeit short-lived, gratification of mechanical removal that only exacerbates an infestation. This issue is also related to Ailanthus’ brittle nature (Kowarik and Säumel 2007, Terzopoulou et al. 2023). Lycorma delicatula, besides being a pest of grapes, is also an issue in urban and suburban settings (Urban and Leach 2023) where mature Ailanthus, further weakened by biological controls, may cause property damage as branches and trunks fall. Protocols that call for the manual removal of large, potentially damaging trees followed by the introduction of biological controls to manage subsequent Ailanthus growth are a likely solution in these settings.

Protocols developed by APHIS are designed to protect against potentially negative impacts that could result due to intentionally releasing biocontrol agents. This process takes multiple years to complete but is justified (Heimpel and Cock 2018). It has been nearly 20 years, for example, since E. brandti was brought to the United States as a potential biocontrol agent, and it has still not been approved for field trials. These regulations are in place to limit the possibility of today’s solution becoming tomorrow’s problem. However, the current pace of Ailanthus biocontrol research cannot keep up with the rapid expansion of L. delicatula, which is dependent on Ailanthus for optimal reproduction. Each of these biological control agents, E. brandti, V. nonalfalfae, and Ac. ailanthi, are years away from commercial release, so they are unlikely to be a factor in preventing the establishment and spread of L. delicatula in the United States. However, this conclusion does not preempt the continued study of Ailanthus biological controls. Continued strategic suppression of both Ailanthus and L. delicatula using IPM practices is the best approach to dealing with these challenging and damaging invasive species.

Author contributions

Harrison Miles (Conceptualization [lead], Writing—original draft [lead], Writing—review & editing [lead]), Scott Salom (Writing—review & editing [equal]), Timothy Shively (Writing—review & editing [equal]), Jason Bielski (Writing—review & editing [equal]), Tom McAvoy (Writing—review & editing [equal]), and Carrie Fearer (Conceptualization [equal], Supervision [lead], Writing—original draft [supporting], Writing—review & editing [equal])