Biology, Ecology, Impacts and Management of the Invasive Weed, Blue Heliotrope (Heliotropium amplexicaule Vahl)—A Review

Abstract

Blue heliotrope (Heliotropium amplexicaule Vahl) is an extremely drought-hardy perennial weed that is often problematic within agricultural production systems and natural environments in some parts of the world. It has the capacity to outcompete and displace desirable plant species and it contains various biochemical compounds that are toxic to grazing livestock and humans. Heliotropium amplexicaule plants can grow within a range of climatic and environmental conditions and produce seeds that remain dormant for several years within the soil which exhibit staggered emergence long after the original parent plants have expired. While control options, including biological, chemical, cultural, and physical methods, are available, many are not suitable as a single-use approach for the long-term management of this species. Therefore, an integrated weed management (IWM) program is necessary for the confident and long-term management of H. amplexicaule, particularly within dryland ecosystems. This review explores the biology, ecology, distribution, and suitable management options currently available for H. amplexicaule, while identifying research gaps that can be addressed to assist in its future management. While particular emphasis is placed on the Australian experience, information from a global perspective is included, providing valuable insights for the long-term management of H. amplexicaule worldwide.

1. Introduction

Invasive plant species pose a serious threat to agricultural and natural landscapes, as they have the capacity to alter a range of ecosystem functions in the invaded landscape [1,2,3]. If these species are not appropriately managed, they will continue to expand beyond their current distribution and can reduce the economic and environmental value of the land [2,3]. One particular problematic species that has shown increasing signs of expanded invasion in Australia and around the world and continues to be a destructive and difficult-to-control weed is blue heliotrope (Heliotropium amplexicaule Vahl) [4,5]. Native to the temperate regions of South America, H. amplexicaule is a herbaceous, perennial plant that has the capacity to form dense monocultures that compete against and displace desirable plant species [6,7,8,9]. Of additional concern is its role as a source of pyrrolizidine alkaloid poisoning in livestock, which can have severe animal health and economic consequences if it is not appropriately controlled [10].

The successful invasion and colonisation of H. amplexicaule into new areas is commonly attributed to its (i) diverse reproductive biology, (ii) ability to grow across a wide range of environments, (iii) high drought tolerance, (iv) rapid development and ability to grow across a range of photoperiods, and (v) ability to tolerate some conventional herbicides and management approaches [6,7,11,12]. Although a range of management options have been deployed to control H. amplexicaule, such as the use of biological, chemical, cultural, and physical methods, many of these options do not provide adequate long-term control when used as stand-alone approaches [7,11,12,13]. To identify the most suitable options for controlling any weed species, it is important to understand their biology and ecology, which, in essence, can be used to manipulate weaknesses in the species for improved confidence in long-term control [14,15]. Accordingly, this review provides an insight into the biology and ecology of H. amplexicaule in order to identify suitable management strategies, whilst also highlighting key areas which future research should focus on to improve the long-term management of the species around the world.

2. Nomenclature and Taxonomy

• Domain: Eukaryote
• Kingdom: Plantae
• Phylum: Spermatophyta
• Subphylum: Angiospermae
• Class: Dicotyledonae
• Order: Boraginales
• Family: Boraginaceae
• Genus: Heliotropium
• Species: Heliotropium amplexicaule Vahl.

Heliotropium amplexicaule is commonly known as blue heliotrope but is also known as clasping heliotrope, purple-top, summer heliotrope, wild heliotrope, and wild verbena [12]. It is a member of the Boraginaceae family which also includes several globally invasive weeds such as comfrey (Symphytum officinale L.), green Alkanet [Pentaglottis sempervirens (L.) Tausch ex L.H. Bailey], Paterson’s curse (Echium plantagineum L.), and Wood Forget-me-not (Myosotis sylvatica Hoffm.) [12]. Heliotropium is a large genus with over 350 species, originating from the Old-World tropics and sub-tropics [16,17]. In Australia, the genus is represented by 78 species, of which at least 73 are considered to be endemic (indigenous) [12,18]. Four of these species are ambiguously considered to have been introduced during European settlement and include dwarf heliotrope (H. supinum L.), H. amplexicaule, Indian heliotrope (H. indicum L.), and salt heliotrope (H. curassavicum L.) [18]. Most native Heliotropium species belong to the Orthostachys section; however, the introduced H. amplexicaule belongs to the Heliophytum section of the genus Heliotropium and no other Australian species are found in this section [4,17,19]. Further, relatively few Heliotropium species have geographic ranges that overlap with H. amplexicaule [11,20,21].

3. Distribution and History

3.1. Native Range

Heliotropium amplexicaule is native to the temperate regions of South America, particularly Argentina, Brazil, Bolivia, Chile, and Uruguay [17]. Within these regions, H. amplexicaule is commonly found growing within grasslands, open woodlands, recently disturbed areas, roadsides, and unused or abandoned farmland [12]. Although H. amplexicaule has the capacity to colonise these areas, it is generally only found in low densities within its native range and does not persist within the environment for long periods of time [7]. The lack of persistence within its native range is largely due to natural predation from several species, some of which include cell-sucking bugs (Dictyla spp.), flea beetles (Longitarsus spp.), leaf-blotch fungus (Pseudocercosporella sp.), leaf-eating beetles (Deuterocampta quadrijuga), and shoot-feeding thirps (Haplothrips heliotropica) [7]. Outside of its native range, these species are often limited in abundance or not present; therefore, H. amplexicaule populations are often larger and more persistent outside of its native range [7].

3.2. Introduced Range

Beyond its native range, H. amplexicaule can now be found distributed across several countries within Asia, Africa, Europe, North America, and Oceania (Figure 1). Although the exact timeline of introduction to these countries is unknown, reports suggest that its distribution and spread was more prevalent in the mid-1900s and was probably a result of an increase in the ornamental plant trade between interconnected locations [4,6,7,22,23]. Further spread of H. amplexicaule into new areas has also been linked to plants escaping intended cultivation, or to their unintentional spread as seed contaminants [6,7]. In Asia, the distribution of H. amplexicaule is not currently widespread, and has only recently been detected within Malaysia and India in the last few decades [5,22]. In Africa, H. amplexicaule is mostly reported as a troublesome weed within the south of the continent but has also been identified growing within grasslands or disturbed areas across Algeria, Egypt, South Africa (Gqeberha, KwaZulu-Natal, and the Pretoria region), Mauritius, and Zimbabwe [4,5]. In Europe, H. amplexicaule is recognised as an invasive weed and has been reported within several countries including Belgium, France, Portugal, Spain, and Italy [4,23]. In North America, H. amplexicaule is also recognised as a weed with the potential to pose a serious threat to agricultural and natural environments within the United States of America, particularly across the states of Alabama, California, Florida, Georgia, Louisiana, Mississippi, North Carolina, Oregon, South Carolina, Tennessee, Texas, and Virginia [23].

Of particular concern, H. amplexicaule has shown recent signs of expansion across Oceania, particularly within the southeast region of Australia [6,7]. The literature suggests that the species was first reported in Australia between 1907 and 1908 in the Moreton district of Queensland and Whittingham, New South Wales (NSW) [6], although earlier reports suggest it may have been present since 1893 in Athelstone, South Australia, 1902 in South Brisbane, and 1908 in the Hunter Valley in NSW [9,18]. Of particular interest, research has identified that H. amplexicaule populations within Australia appear slightly different in terms of their morphology (i.e., leaf shape, size, and colour) compared to those from the native range, suggesting that the invasion in this area may have originated from a garden cultivar of the species [7]. It also suggests that different environmental factors or selection pressures within Australia may have altered the morphology of the species over time [6,7,12]. By the early 1990s, H. amplexicaule had spread across most of eastern and southeastern Australia, from south of Cairns (in the tropics) right through to temperate regions of South Australia, and was estimated to have infested an area of over 110,000 hectares and continues to expand across much of southeast Australia today [6,12].

3.3. Habitat Suitability

Heliotropium amplexicaule has the capacity to grow across a wide range of environments, where it can invade and colonise an area [12]. It is generally most common within temperate and sub-tropical climatic regions and in areas that receive at least 500 mm of annual rainfall, although it can often persist in areas with lower rainfall [6,12]. In these areas it can withstand a wide range of soil types, including alluvial, black cracking, red clay, duplex, calcareous or volcanic red, and heavy brown clay loam soils; however, it is generally more problematic in sandy loam or red loam soil types [6,18,24,25,26]. Heliotropium amplexicaule can also withstand highly acidic soils and is more abundant in areas of recent disturbance [6,27].

3.4. Future Projections

Based on the recent expansion history of H. amplexicaule within southeast Australia, it is likely that the species will follow this trend within other regions around the world and continue to spread beyond its current distribution [10,12,28]. According to future climate change scenarios with hotter temperatures, elevated atmospheric carbon dioxide (CO₂) levels, prolonged droughts, and frequent extreme weather events, it is suggested that H. amplexicaule may readily adapt to these conditions and expand into higher elevations and other regions where it may currently not exist [12,29]. Currently, the spread of H. amplexicaule is restricted due to its frost sensitivity, although the influence of climate change will probably increase the area of suitable habitat for the species leading into the future [6,12,29].

In Australia, it is projected that H. amplexicaule will probably expand further southward into the states of South Australia, Victoria, and Western Australia by 2050 [29]. Conversely, by 2065, its potential habitat suitability within Australia will either remain the same or decrease [30]. To obtain a better understanding of the potential distribution of H. amplexicaule, future research should focus on developing suitable bioclimatic modelling for the species. This information will be useful in identifying areas where H. amplexicaule poses a future risk of invasion, not just in Australia but also in other regions where the species is currently invasive, with particular focus of countries within Asia, Africa, Europe, and North America. Such information will help inform land managers and researchers in those susceptible areas and allow them to participate in early detection and eradication programs to proactively limit the future impact and spread of this species.

4. Biology and Ecology

4.1. Botanical Description

Heliotropium amplexicaule has dull-green, prostrate, branched stems that radiate from the central woody rootstock, which grows between 15 cm to 30 cm in height and 30 cm to 200 cm in diameter [12,31] (Figure 2). They are cylindrical in shape, swiftly branched, and often bear either long and bristly or short hairs [6,18,31,32]. Leaves are alternately arranged, sessile or sub-sessile (no distinct stalk), elongated in shape (oblanceolate to lanceolate), and can reach up to 2 cm to 9 cm in length and 0.4 cm to 2.5 cm in width [4]. Leaves also have wavy margins, a hairy lamina, pointed or rounded tips, and prominent veins [4,31,33]. Compared to the leaves at the base, the terminal leaves are often linear, smaller, and thinner [4]. The upper surface of the leaf is dull-green, while the lower surface is paler, with arcuate veins printed on the upper face and protruding from the lower surface [4]. The terminal inflorescence is bractless, dense, formed from three to four scorpioid, unilateral, multiflorous cymes, and grows to a length of 15 cm [6]. Each inflorescence holds multiple small, vivid, light blue to lilac flowers (4 mm to 6 mm long and 3 mm to 6 mm wide) with rounded lobes and tubular yellow throats and are alternately arranged in dense clusters along one side of a coiled flower spike [4,6,33].

The flowers contain five petals that are merged into a corolla tube for the majority of their length and are encircled by five sepals [4,6]. Fruits are globular, 3 mm to 4 mm long, narrowed at the top, and glabrous, with a succulent coating that becomes wrinkled and warty at maturity [4,6]. Fruits are separated into two small segments, referred to as nutlets or mericarps, with tuberculate backs and each containing one seed that is dark brown to black in colour, sub-globule in shape, and has a wrinkled or warty surface [4,6,31]. The root system is slender, woody, and can extend over 100 cm to 200 cm within the soil profile, with several complex horizontal lateral roots reaching up to 300 cm in length [9,25,34].

In some cases, H. amplexicaule may appear morphologically similar to H. europaeum, H. curassavicum, and H. indicum [12]. Key differences that help to distinguish these species include (i) H. europaeum is often more upright or semi-upright, has multi-branched stems, few basal, oval-shaped leaves, and small whitish flowers with a yellow centre; (ii) H. curassavicum is hairless and has basal, oblong-to-elongated leaves, and very small white flowers with yellow or red centres; and (iii) H. indicum has mostly unbranched stems, larger leaves, a longer inflorescence, and purple flowers that fade to dull-white flowers with yellowish centres [4,6,12,31].

4.2. Life Cycle and Phenology

Heliotropium amplexicaule is a short-lived perennial herb with a deep and extensive root system and, once mature, the plant can undergo several annual cycles of growth and die-back of above-ground vegetation [12]. Vegetative growth often begins in late winter to early spring and continues into the warmer months of summer (

Table 1. Average seasonal growth patterns of H. amplexicaule *.

Plant Life Cycle Event	Spring			Summer			Autumn			Winter
Seed germination
Active growth period
Flowering
Growth from rootstocks
Dormant/less active growth

* Shading represents seasonal growth patterns of H. amplexicaule as reported in the literature [6,8,9,12,27].

). It develops a large root system which stores important nutrient reserves that can assist with its survival during the cooler months in late autumn to winter, when the foliage of the plant partially dies back or is killed by frost [27]. The timing of vegetative growth, flowering, seed production, and germination of H. amplexicaule is often strongly influenced by the local environment, predominately the rainfall and temperature [12,27].

4.3. Seed Biology, Dispersal, and Population Dynamics

Heliotropium amplexicaule has the capacity to reproduce from its seeds and cultivated root material [6,32]. Seed germination generally occurs from late spring to summer, and sometimes in autumn if soil moisture and temperatures are adequate [6,8]. The majority of seedlings originate from buried seeds, with cultivation and fire often triggering significant germination events [11,27]. Seedlings recruited in summer and autumn contribute significantly to plant establishment and vigorous vegetation regeneration the following spring, developing deeper and more extensive root systems compared to those recruited in cooler months, where frost damage is more likely [6]. Flowers begin to emerge most noticeably from late spring to summer and continue sporadically through the summer until the end of autumn, and rarely in mid-winter [6,8,9,28]. In warmer climates though, certain plants may blossom and set seeds in winter [8].

The seed production potential of H. amplexicaule is large, with some populations estimated to produce up to 18,600 ± 4800 seeds/m² [7]. Variation in the number of seeds produced in each nutlet occurs between populations and may be related to variable annual precipitation, which can influence seed development [6]. Although the seed germination of H. amplexicaule has not been extensively studied, research indicates that most seeds germinate at 25 °C/15 °C (day/night), with optimal germination observed at 25 °C [6]. In the cooler months of the year, seeds will tend to enter a period of dormancy, which can last from one month to one year and is a mechanism used to prevent the potential damage caused by winter frost, which can kill the plant [6,12,27]. Although the seed dormancy of H. amplexicaule has not been widely studied, it has been reported that it is often relieved by cultivation or soil disturbance, fire, or an increase in daily temperatures and light availability, often a result of the transition from winter to spring [6,12,27].

This species has a fairly persistent soil seedbank. In a long-term study, an analysis summarising five different sites with differing infestation and seed rain histories indicated that up to 18,000 seeds m⁻² could be expected after three years of infestation and nearly 50,000 seeds m⁻² after eight years [7]. Seedbank decline occurred rapidly, with more than 20,000 seeds m⁻² removed after two years with no inputs and 50,000 seeds m⁻² after 12 years [7]. Despite this, a considerable number of seeds (1500 seeds m⁻²) remained after 12 years with no seed input, highlighting the longevity of the species within the soil seedbank [7]. On the other hand, the seed germination of H. amplexicaule could also be influenced by burial depth, light availability, and soil moisture, although further investigation is required to better understand and quantify the effect of these environmental factors and how they influence its germination across different climatic regions [6,8,11,12,27].

Heliotropium amplexicaule proliferates vigorously due to its abundant seed output and cultivated root material. Dispersal is often assisted by soil disturbance, slashing regimes, water, and the movement of various animals [12]. The wrinkled and tuberculate nutlets easily adhere to wool and animal fur or hooves, while seeds pass through the digestive tracts of most animals unharmed [8,9]. It is also commonly reported that H. amplexicaule seeds are discovered as a contaminant of several agricultural products, such as grain or hay, which often act as vectors for its transportation between different areas [8]. Cultivated root material has the capacity to grow from a depth of 15 cm within the soil, and, in some cases, may regenerate from deeper within the soil profile, although this is less common and requires greater energy reserves [6]. It is also noted that root fragments are not viable after being left on the soil surface or planted after three days, while fragments left to harden for a day may have more viability than those replanted immediately [6]. These fragments are commonly spread by machinery, particularly cultivation machinery or graders, as well as being moved by water across a landscape or within a waterway [7].

4.4. Stress Tolerance

Heliotropium amplexicaule is a highly drought tolerant species that has the capacity to withstand periods of low rainfall and high temperatures, contributing to its successful invasion and persistence within an area [12,35]. Seedlings are also known to be frost-sensitive, but opportunistically escape under surrounding vegetation [6]. In contrast, adult plants are evergreen and tolerant to 0 °C, with roots being tolerant to −6.5 °C [6]. It is also noted that during intense hot and dry periods, H. amplexicaule may become stressed, and its growth and development can become severely slowed or even halt, although plants can quickly rejuvenate and flourish when conditions start to become favourable [12].

5. Impacts and Interference

5.1. Agricultural Impacts

Heliotropium amplexicaule is expanding in crop production systems and rangelands, possibly due to its high reproductive capacity, hardiness, vigorous growth, and drought tolerance [10]. In rangelands, this plant can develop dense monocultures (Figure 3) and choke out other vegetation and create ongoing problems due to its perennial nature [7,8,9,10]. Production losses due to H. amplexicaule in agricultural systems are rising due to its increased spread and direct competition with more desirable crop and pasture species for resources such as light, nutrients, and soil moisture [7,8,9,10]. It has also been reported that H. amplexicaule is problematic in cropping systems, competing against desirable species, with examples including cotton (Gossypium spp.), lentils (Lens culinaris L.), pearl millet [Pennisetum glaucum (L.) R.Br.], pineapples (Ananas comosus L. Merr.), sugarcane (Saccharum officinarum L.), and a range of other cropping systems [9,28]. Although there are limited quantitative data in the global literature to identify these losses, the species has the capacity to severely impact crop production by displacing and outcompeting desirable species, all of which can result in the reduction of profitable and desirable species [12]. It is also noted that H. amplexicaule can become a problem within domestic situations such as on lawns or gardens, which can have further economic implications regarding its management [12].

Although H. amplexicaule is not widely or commonly grazed on, it may sometimes be grazed by young or inexperienced stock or when other food sources are scarce [8,9,36]. Of important consideration here is that all the above-ground parts of H. amplexicaule, including its seeds, contain pyrrolizidine alkaloids that cause toxic physiological impacts on most grazing animals [6,10,36,37]. Cattle (Bos taurus L.), pigs (Sus scrofa L.), horses (Equus caballus L.), and a range of poultry are among the livestock that might be impacted, in order of vulnerability [9]. While goats (Capra hircus L.) and sheep (Ovis aries L.) are relatively resistant to poisoning, they may be affected if intake is large enough or prolonged [37].

Plants with high levels of pyrrolizidine alkaloids cause a range of impacts to livestock and are commonly associated with damage to the liver or within the digestive system [36]. Over time, damaged livers in some ruminants may accumulate an excessive amount of copper, which can be released and potentially lead to the death of the animal [12,36]. In southern Queensland, Australia, cases of cattle poisoning from H. amplexicaule resulted in a range of symptoms including asthenia, chronic wasting, compulsive walking, evident blindness, incoordination, jaundice, photosensitization, ruminal atony, scouring, and tenesmus [38]. Post-mortem examination of their livers would often show hyperplasia (enlargement) of the bile ducts, variable levels of fibrosis (scar tissue), and megalocytosis (impaired cell division) of the liver cells [36]. Although the impact of alkaloid poisoning appears to be cumulative in adult animals, it can be more immediate in young cattle after a short period of exposure (within 1.5 months) [36,37]. In this regard, it is critical to ensure that livestock be excluded from areas infested with H. amplexicaule to prevent any severe animal health issues. In addition to being a pest itself, H. amplexicaule also has the potential to be a host for other insect pests and diseases, posing a biosecurity risk to surrounding desirable species [12]. Further investigation into potential pests and diseases should be carried out to identify any current or future risks.

5.2. Environmental Impacts

Heliotropium amplexicaule is commonly recognised as an environmental weed with a reputation for infesting disturbed areas, roadsides, and a range of ecosystems such as grassland and woodland communities [12,24]. It has also been known as a key threat towards endangered flora, such as obcordate-leafed Zieria (Zieria obcordata A. Cunn.) in Australia, and to a range of vegetation communities worldwide [24,34]. Heliotropium amplexicaule is highly adapted to periods of drought, facilitating its invasion across diverse landscapes and enabling it to quickly outcompete native species when water becomes available [9,12]. Another environmental impact of H. amplexicaule is its potential as a fire hazard due to the large accumulation of dry biomass it produces [12]. On the other hand, H. amplexicaule can also provide suitable habitat or shelter for a range of animals, including foxes (Vulpes vulpes L.), rabbits (Oryctolagus cuniculus L.), and rodents (Rodentia spp.), all of which contribute to its dispersal across the landscape [12,24].

5.3. Human Health

The genus Heliotropium is well known for its toxicity, and H. amplexicaule poses a threat to human health [10,39]. Of particular concern are the various human health issues associated with the digestive system and liver if consumed [10,12,39]. H. amplexicaule has been implicated in several cases of human poisoning, either directly through herbal medicine or indirectly through contaminated grain consumption [10,39,40]. Another major human health concern linked to pyrrolizidine alkaloids involve their contamination of food commodities such as eggs, honey, milk, and meat, which do not naturally contain alkaloids [40]. When contaminated material is consumed by humans, these traces are often too low to cause any severe toxic effects, although further investigation into this area should be considered to ensure safe levels of food can be consumed [10,39,40]. This type of contamination primarily occurs when these pyrrolizidine alkaloids contaminate honey produced by bees that forage on H. amplexicaule [10]. An analysis of regional market honey samples highlighted pyrrolizidine alkaloid contents of up to 2.0 µg g⁻¹ of honey, indicating the need for honey producers to be aware of this issue, particularly when honey is sourced from locations around H. amplexicaule [10]. This may particularly be the case where single-source (unblended) honey is consumed.

5.4. Socioeconomic Impacts

It is clear that H. amplexicaule causes several agricultural, environmental, and human health impacts. Collectively, these negative impacts also exert substantial socioeconomic impacts, especially in rural communities (

Table 2. Summary of key socioeconomic impacts caused by H. amplexicaule.

Type of Socioeconomic Impact	Reason	References
Animal health consequences	Juvenile or inexperienced livestock may feed on H. amplexicaule which can cause poisoning or reduce livestock fertility rates, resulting in loss of livestock or increased cost of care.	[12,33,36,37]
Increased cost of land management	Control works required for large infestations of H. amplexicaule can be costly and time consuming.	[10,12,36,37]
Land devaluation	Large infestations of H. amplexicaule require ongoing work to control which can be costly and may reduce or restrict land activity (e.g., number of livestock).	[12,36,37]
Neighbour disputes	Disputes may arise if neighbours do not work together to control H. amplexicaule infestations. Alternatively, control works can be undone if surrounding properties do not work together.	[12,36]
Reduced recreational access	Infested landscapes may have reduced recreational access and limited access to waterways or important structures such as feeding areas or water points for livestock.	[12]
Reduced stocking rates	Invasion by H. amplexicaule can result in reduced pasture production by outcompeting and displacing desirable species. This results in the carrying capacity of the land being reduced. Additional food sources may be required on the infested landscape which can increase the cost of farm production.	[12,26,37]
Seed contamination	Livestock or visitors to the infested area may unintentionally spread H. amplexicaule seeds into new areas.	[12]

).

Although reports of the economic impacts are limited within the global literature, a study in Australia evaluated the responses of 138 land managers within NSW regarding the impacts of H. amplexicaule. The results from this study highlighted that 42% of the land managers were concerned with or experienced decreased stocking rates, 35% were concerned about land devaluation due to the heavy infestations, and 11% experienced decreased reproduction rates in livestock [12]. It was also noted in the study that 48% of the land managers surveyed experienced financial distress from the cost associated with the control and loss of production caused by H. amplexicaule, while 39% experienced psychological distress, and 18% had recent disputes with neighbouring property managers due to the lack of action to control the species [12]. Therefore, controlling H. amplexicaule is important not only for its environmental and economic impacts but also for its social impacts. Further investigation into the economic impacts of H. amplexicaule would be valuable to land managers and researchers to identify and manage the species on a landscape scale. Such information would also assist in resource allocation and improve seasonal planning for the management of this species.

6. Management

6.1. Biosecurity Measures and Prevention

To minimise the impact and spread of any weed species, such as H. amplexicaule, it is essential that newly emerging populations are quickly identified and appropriately controlled. To assist in this area, recent developments in the use of weed detection systems, such as the use of drones, specialised camera imagery, and machine learning algorithms, might be useful for detecting weed populations across various life stages [41,42]. Although it is unclear if H. amplexicaule has been the centre of such research, this emerging field of weed detection could substantially improve detection times and could be a useful, cost-effective strategy to identify weed populations before they become widespread [41,42,43]. Heliotropium amplexicaule may also be a suitable species for this type of technology due to its distinctive leaf formation and attractive, colourful flowers, which help distinguish the plant from surrounding species, although this area of research requires further investigation. Other biosecurity and preventative measures that should be adopted to reduce the impact and growth of H. amplexicaule include (i) early detection and surveillance protocols throughout the year; (ii) ensuring on-farm biosecurity measures are followed to prevent seed and weed movement and ensure appropriate on-farm hygiene occurs to prevent any translocation of infested material; (iii) maintaining competitive pastures and paddocks with minimal soil disturbance; and (iv) planning and preparing for early-season weed control programs to identify plants before they become problematic [4,12].

6.2. Chemical Control

Herbicides are often used to control H. amplexicaule around the world, although in some cases they can have varying results [12,44]. For optimal results, herbicides need to be applied to actively growing plants before flowering to prevent subsequent seed development [9]. To control H. amplexicaule, herbicides can be applied using the broadcast method where an even distribution of herbicides is sprayed across an area, or with the spot spray method where individual plants are treated separately [12]. Using the broadcast method to control H. amplexicaule can be beneficial as it can be used across large areas such as pastures when using selective herbicides, whilst it can also be used to treat dense infestations uniformly [12]. On the other hand, broadcast applications of H. amplexicaule may not completely control all plants, as some may be missed due to being hidden under other vegetation, or may not receive adequate amounts of herbicide for complete plant death [12]. This method may also cause off-target damage to species that grow adjacent to H. amplexicaule infestations. In this regard, spot spray applications would be beneficial in controlling targeted plants or isolated populations when the species is growing adjacent to desirable plants.

Although there are currently no reports of herbicide resistance in H. amplexicaule, it is important to regularly alternate between the different modes of action to reduce the chance of developing resistance [7,12,35,44,45]. Ensuring that a range of modes of action are used (

Table 3. Common herbicides and their modes of action used to control H. amplexicaule.

Herbicide Active Ingredient	Herbicide Group Classification and Mode of Action	References
2,4-D	Group 4: Disruptors of plant cell growth (Auxin mimics)	[12,45]
Aminopyralid	Group 4: Disruptors of plant cell growth (Auxin mimics)	[12]
Amitrole	Group 32: Inhibition of solanesyl diphosphate synthase	[12,45]
Ammonium thiocyanate	Group 34: Inhibition of lycopene cyclase	[12]
Dicamba	Group 4: Disruptors of plant cell growth (Auxin mimics)	[12,45]
Fluroxypyr	Group 4: Disruptors of plant cell growth (Auxin mimics)	[12,45]
Glyphosate	Group 9: Inhibition of 5-enolpyruvyl shikimate-3 phosphate synthase (EPSP inhibition)	[12,35,44]
Metsulfuron-methyl	Group 9: Acetolactate synthase (ALS) or acetohydroxyacid synthase (AHAS) inhibitors	[12,35,45]
Picloram	Group 4: Disruptors of plant cell growth (Auxin mimics)	[12,45]
Sulfonylurea	Group 9: ALS or AHAS inhibitors	[12]
Tebuthiuron	Group 5: Inhibition of photosynthesis at photosystem II	[12,45]
Triazine	Group 5: Inhibition of photosynthesis at photosystem II	[12,35]
Triclopyr	Group 4: Disruptors of plant cell growth (Auxin mimics)	[12,45]

) to control H. amplexicaule will also help to target different aspects of the plants biology and reduce the likelihood of it developing resistance in the future, whilst also increasing the success rates [7,12,35,44,45]. To further increase the efficiency of herbicide use, a combination of active constituents has proven to be beneficial, with some examples used for H. amplexicaule including aminopyralid (8 g/L) + picloram (100 g/L) + triclopyr (300 g/L) (registered as Grazon^® Extra, Australia), picloram 75 g/L + 2,4-D 300 g/L (registered as Tordon^® 75-D, Australia), and picloram 75 g/L + triclopyr (300 g/L) (registered as Adama Fightback^®, Australia) [12,45]. Although the use of herbicides can provide direct control, their success is often varied and some non-selective herbicides such as glyphosate may cause damage to surrounding desirable plant species [12].

It is also noted that the long-term use of herbicides can have several unwanted consequences on the surrounding environment, such as the potential development of herbicide resistance, impact on soil biota, damage to surrounding waterways from runoff, and the potential unwanted damage to desirable species [46,47]. To address these issues, future research in the field of alternative options such as the use of bioherbicides [48], or automatic chemical control options [42], could prove beneficial in the control of H. amplexicaule, although this field requires further investigation specific to H. amplexicaule. Further investigation on a range of herbicides and herbicide rates within different climatic regions would also be useful in identifying the most suitable combination to control H. amplexicaule around the world. In addition, the combination of herbicides with other control options, such as physical, cultural, and biological elements, may also provide enhanced control, although these combinations would require further investigation for more confident control.

6.3. Physical and Cultural Control

Physical removal of entire H. amplexicaule plants, including their roots, can be used to help control small or isolated populations of the species [12]. Although this method can be useful for smaller or isolated plants, careful consideration needs to be made to ensure entire plants are removed, as the species can regenerate from its rootstocks within the soil [9,25,34]. In this regard, methods such as cultivation or harrowing may not be suitable as a single method of control, as this may result in the further spread of the species, or in some cases these methods can stimulate seed germination [7,11]. Although fire can remove aboveground biomass of H. amplexicaule, it can also contribute towards mass seed germination events [11,27]. To assist in this area, it would be suitable for physical or cultural control methods to be integrated with other methods of control, such as chemical control, for more confident control and to help exhaust the soil seedbank. These integrated approaches can enhance seed germination in the soil, which can then subsequently be controlled using other methods. However, this area requires more focused research to identify the most suitable combinations.

Another important area of H. amplexicaule control is the strategic use of grazing and pasture management. Strategic grazing may include the methods of livestock rotation, exclusion zones, or decreasing livestock numbers to an area to help reduce the likelihood of overgrazing or soil disturbance from occurring [12]. If strategic grazing is not managed appropriately then it may provide suitable conditions for H. amplexicaule to emerge and quickly take over an area. In addition, maintaining competitive pastures can also be used to help suppress and prevent the growth of H. amplexicaule [12]. This method can restrict the growth and development of H. amplexicaule by increasing its competition from other pasture species and reduce its access to available resources such as light, water, nutrients, and space. Of particular interest, several pasture species have shown promising signs of being suitable for suppressing and preventing the growth of H. amplexicaule, and may include cocksfoot (Dactylis glomerata L.), digit grass (Digitaria eriantha Stent. Kok.), lucerne (Medicago sativa L.), panic grass (Panicum spp.), and phalaris (Phalaris spp.) [12]. Although these pasture species may be suitable in some cases, it is important to note that pasture management may vary across geographical locations and some species might not be suitable for all areas, thus highlighting the need to identify alternative and appropriate pasture species to manage H. amplexicaule specific to the area it is found growing.

Appropriate pasture management, including soil health management, can also be an important factor to consider when trying to prevent or reduce the establishment of H. amplexicaule [12]. For example, it is reported that H. amplexicaule grows well in a range of soil types but will particularly invade acidic and low nutrient soils; therefore, improved soil health may act as an additional barrier in preventing the establishment of the species [12]. In this regard, a combination of strategic grazing, pasture management, and improved soil health can help to minimise and prevent the establishment and spread of H. amplexicaule [4,5,12].

6.4. Biological Control

The use of natural enemies of H. amplexicaule in its native range as biological control agents has been investigated in Australia [20,27]. Of particular interest, D. quadrijuga has shown promising signs of localised impact on H. amplexicaule populations and causes repeated defoliation of the plants, ultimately followed by depletion of underground reserves over time, leading to plant death [4,7,12]. Although D. quadrijuga is widespread in NSW in Australia, since its multiple introductions between 2001 and 2010, its success is often limited by high summer temperatures or to plants that are exposed to moisture stress [4]. Other agents that have been identified from Argentina, such as Dictyla spp., H. heliotropica, Longitarsus spp., and Pseudocercosporella spp., have shown the potential to control H. amplexicaule but have either not been widely released, have been found to attack other closely related plants, or have not shown sustained success [7,16,27]. Initial trials of these biological control agents indicated that Dictyla spp., D. quadrijuga, Longitarsus spp., and H. heliotropica specifically target H. amplexicaule, H. arborescens, and H. nicotianaefolium, which are closely related species [49]. While these trails show promise, further testing of a range of biological agents would be suitable, particularly in other regions where the species is becoming problematic. There is also the potential for future research to focus on the co-release of agents such as D. quadrijuga and Longitarsus sp. to target multiple aspects of the plant’s biology for improved control. However, additional host-specific testing is necessary to identify the risks and opportunities of different biological agents across different geographical locations [4,11,21,27,49].

7. Integrated Weed Management—A Case Study

To effectively control H. amplexicaule over the long term, the application of an Integrated Weed Management (IWM) program is imperative [9]. One pragmatic option is integrating of chemicals with competitive pasture for improved control. Herbicides play a crucial role in controlling the plant directly, while establishing a competitive, summer-growing perennial pasture can provide effective and sustainable control by creating conditions which would make it difficult for H. amplexicaule to become established. Here, we present the findings of a comprehensive case study of long-term IWM for H. amplexicaule. In a study conducted in central-west NSW, pellets of the herbicide tebuthiuron were applied (at three different rates) to a field site with an H. amplexicaule density of 14 mature plants m⁻² in a naturalised grass and clover pasture [13]. Two years after the herbicide treatments, a consol lovegrass [Eragrostis curvula var. conferta (Schrad.) Nees] and premier digit grass (Digitaria eriantha Steud.) pasture was established in the same plots. The trial area was then fenced off to allow the grasses to establish properly, and once established, the area was opened to grazing similar to the surrounding field. Three years later, there was no presence of H. amplexicaule in the plots that were treated with tebuthiuron pellets followed by pasture establishment and strategic/sustainable grazing. It was also noted that there was no adverse effect on grasses, and clovers had re-established in all plots. Further assessment of the plots occurred approximately 14 years after the initial treatments were applied, showing minimal infestation in plots treated with tebuthiuron (only 0 to 2 plants m⁻²), while untreated control plots had 18 plants m⁻² [13]. These results highlight the efficacy of combining effective herbicides with a competitive perennial pasture for the sustainable, long-term control of H. amplexicaule. However, no other such study on the integrated management of this species is available, which justifies further research on this topic.

8. Conclusions and Future Research Directions

It is clear from this review that H. amplexicaule will continue to economically and environmentally impact the land it invades unless appropriate management is applied. Although there are several control options available, such as the use of biological, chemical, cultural, and physical controls, a single-use approach will not adequately manage the species and an IWM strategy will be required. Appropriate management programs should always be assisted by effective biosecurity and preventative measures to limit the spread and introduction of H. amplexicaule into new areas. Based on the findings of this review, the following IWM options must be researched and adopted in a site-specific manner:

(i)

The use of cultivation or ecological burning to increase seed germination, followed by the application of a registered herbicide to help exhaust the soil seedbank.

(ii)

A combination of physical (chipping/removal and destruction of whole plants) and chemical controls (spot applications) of small or isolated populations.

(iii)

A combination of biological control agents that target different aspects of the plant’s biology.

(iv)

The strategic use of suppressive pasture and crop species and/or cultivars as well as the grazing management of grasslands to maintain healthy vegetation that can compete with H. amplexicaule.

(v)

A combination of each of the above methods, depending on the size and location of the population.

Although these combinations may appear promising for the control of H. amplexicaule based on the plant’s biological aspects, further investigation is needed to conduct cost–benefit analyses, evaluate effectiveness, and ensure long-term success across a range of climatic regions. Future research focusing on bioclimatic modelling would also be beneficial for identifying new areas where H. amplexicaule may pose future invasion risk. This information will help guide land managers and researchers in identifying key areas where management should be prioritized leading into the future.