Challenges Inherent in Controlling Prickly Pear Species; a Global Review of the Properties of Opuntia stricta, Opuntia ficus-indica and Opuntia monacantha

Opuntia species (prickly pear) were deliberately introduced to many countries around the world for fruit, cochineal dye production, living fencing or as ornamentals. They are now some of the world’s most significant weeds, particularly in regions with warm and or dry climates, as they pose threats to economic and environmental assets. In addition, they can cause considerable health issues for humans and animals. Opuntia spp. have prolific reproduction abilities, being able to reproduce both vegetatively and by seed. They have generalist pollination and dispersal requirements, which promotes their establishment and spread. Opuntia stricta, O. monacantha and O. ficus-indica are the most globally widespread of the Opuntia spp. In many countries, biological control agents, particularly the cactus moth (Cactoblastis cactorum) and various cochineal insects from the Dactylopius genus, have successfully reduced land-scape scale populations. On a smaller scale, controlling these weeds by either injecting or spraying the cladodes with herbicides can provide effective control. Care must be taken during herbicide treatments as any untreated areas will regenerate. While biological control is the most cost and time effective control method for landscape-scale infestations, further research into the combined efficacy of herbicides, fire, grubbing and pre-burial techniques would be beneficial for land managers to control small-scale and establishing populations. It would also be useful to have greater knowledge of the potential seedbank longevity and seed ecology of these species so that integrated management strategies can be developed to not only deal with initial populations but also the subsequent seedling regrowth.


Introduction
Opuntia species are the largest clade within the Cactacaeae family, and are native to both American continents. They have evolved many adaptive strategies that allow them to thrive under extreme climatic and environmental conditions, including extreme heat, low water availability and salinity [1]. This is mainly due to their exceptional water-conserving strategies, including the ability to photosynthesise with minimal transpiration by utilizing the Crassulacean Acid Metabolism (CAM) photosynthetic pathway [2]. In this process, the enzyme phosphoenolpyruvate (PEP) bonds a CO 2 molecule to a 3-carbon sugar to produce the storable compounds; malate or oxaloacetate. These pH-reducing compounds are readily stored within vacuoles until the presence of sunlight. When the malate or oxaloacetate leave the vacuole to be used for photosynthesis, the compounds are decarboxylated and the carboxyl (CO 2 ) is released at the rubisco activity site. The benefits of being able to store CO 2 in this manner allows for the cells to open their stomata when conditions are cooler, cases, Opuntia spp. were introduced into their invasive range by humans for cochineal dye production, living fencing, or fruit cultivation [10][11][12][13][14][15][16]. In the invaded range, the Opuntia spp. were released from their often specialist, host-specific predators [3,15]. Furthermore, the spread of the Opuntia spp. was facilitated by a wide-variety of animals, including pollinators and frugivores [3,[6][7][8].

Europe
It has been speculated that O. ficus-indica was first introduced to Europe by the Spanish at the end of the 15th Century or in the early 16th Century [12]. It was considered a highly prized plant due to the magnitude of benefits it offered, but particular interest was taken in establishing the cochineal dye industry [12]. It was cultivated for this purpose throughout Spain and the Canary Islands, with the latter being very successful, and is still currently in operation [12]. The fruit was also highly regarded, and in the 1950s, O. ficus-indica was the third most cultivated produce in Sicily, second only to grapes and olives [12]. In Greece, it was first cultivated by Venetians in Crete and the Aegean Islands in the late 1600s, where it grew well in dry, rocky soils [11]. It is considered an important crop in Greece [11], Turkey [23] and Italy, where annual fruit exports exceed 12,000 tons [12,24].
Despite this impressive level of economic importance, Opuntia spp. are regarded as significant weeds throughout Europe [25], particularly in the Mediterranean countries including Spain, Portugal, France, Italy Greece, Croatia and Turkey [26]. Opuntia spp. do not appear to have established in Northern European countries, most likely due to the cooler climate and higher rates of precipitation in these areas [27].
In Spain and Portugal [18,28], O. stricta is most often found in abandoned fields and natural landscapes, particularly those in close proximity to urbanised areas, which suggests that humans are facilitating its dispersal [26]. The cochineal insect, D. opuntiae, was unintentionally introduced to Spain where O. ficus-indica was considered invasive [29]. The favourable Mediterranean climate promoted establishment and the cochineal insect has provided significant control of this species [29]. Despite O. monacantha being recorded as an invasive weed in Spain, France [26], Italy and the Czech Republic [7], there is very limited information regarding the impact of O. monacantha on agricultural and environmental assets, or how it is currently managed.
The higher annual rainfall in the Mediterranean, compared to its native range, has been linked to improved rates of germination and seedling establishment, which has contributed to them becoming significant weeds in this environment [30]. Opuntia spp. have been observed to outcompete native plants in Portugal's coastal regions, and their dense thicket growth form makes them difficult and expensive to manage [18]. Successful biological control agents have not yet been found for Portugal, and control relies predominantly on manual removal during the wet season, and by glyphosate injections prior to fruiting [18]. In Greece, O. ficus-indica has high genetic diversity, further complicating any management efforts [31]. Research into using spineless cultivars of O. ficus-indica for climate mitigation in the Czech Republic found that these cultivars reverted back to their spiny, invasive wild form in only a few generations of escaping cultivation, suggesting their release would have devastating implications on the ecosystem [32].

Africa
South Africa's Biodiversity Act 10 of 2004 categorises all Opuntia spp., with the exception of the spineless cultivars, as Category 1 weeds. The spineless variety of O. ficus-indica was deliberately introduced to at least five African countries (South Africa, Eritrea, Ethiopia, Madagascar and Somalia) for crops, ornamental use, emergency fodder, cochineal production and bee forage [13,14]. It was purposefully introduced to the Karoo region of South Africa in 1656 and spread beyond the cultivated area. These escaped cultivars were observed to quickly revert back to their glochid forming wild type [33], and by 1942, O. ficus-indica covered over 900,000 ha of the Karoo region, making it one of the most widespread weeds in the  [16,34]. The purposeful introduction of the 'ficus' biotype of D. opuntiae reduced the spread of the O. ficus-indica population to less than 100,000 ha [35,36].
Opuntia stricta is considered one of the most aggressive Opuntia spp. in South Africa [37]. It was introduced as an ornamental plant to the Kruger National Park, South Africa, in 1953 [32], but by the late 1990s it had invaded over 30,000 ha. It was introduced to east Africa in the 1950s and populations have recently increased throughout Kenya. It is currently considered invasive in 14 African countries [6], and is particularly problematic in Kenya [34] and Namibia [36]; suitable biological control agents for controlling this species are under investigation. Dactylopius opuntiae was first released in Lakipia County, Kenya, in 2014. Significant improvements were observed after three years, although the population remained localised to the initial introduction site [32]. This same cochineal was deliberately introduced to South Africa in 1997, 10 years after C. cactorum was first introduced. Over a 22-year monitoring program, no reductions in the population density of O. stricta were observed during the time only C. cactorum was present, but the addition of D. opuntiae provided significant, cost-effective control within three years [36].
Opuntia monacantha has spread throughout 19 countries in Africa [7], and is particularly problematic in east Africa. It was first identified in South Africa in 1772, and it was widespread by the 1890s [38]. In some cases, this species occupied 100% of the standing vegetation canopy, creating hazardous thickets and facilitating the establishment of other invasive species, including rats [4].
Opuntia monacantha was the first cactus to be successfully controlled in Africa with the implementation of a biological control program in 1913 [38]. Various Dactylopius spp. were first introduced in South Africa [38], and then to Madagascar [4]. Attempts to introduce C. cactorum as a biological control agent were hindered by heightened predation of the egg sticks and larvae, as well as the limited resources to implement the program compared to those available in Australia [39,40]. In Madagascar, the spineless variety, O. ficus-indica, was cultivated in place of O. monacantha to overcome objections to the latter's removal from the local communities and to create competition to reduce the re-emergence of the less favourable species [4].

Asia
In 1924, Sri Lanka introduced the biological control agent D. opuntiae to control O. stricta and other invasive Opuntia spp. [41]. While this insect has successfully become established, O. stricta is a serious concern in Sri Lanka's arid [42] and coastal areas [43], and has rapidly spread throughout Bundala National Park [43]. Several Opuntia spp. have become invasive throughout India, with O. stricta being of particular concern [6]. Two insects, D. coccus and D. ceylonicus, were released in 1795 for controlling O. monacantha, which was at the time widespread [44,45]. These insects had a significant impact on reducing this species' population density, but were ineffective against O. stricta [46,47]. After the success of the cochineal insect in Sri Lanka, D. opuntiae was introduced to India in 1925 and provided significant control of O. stricta, clearing over 40,000 ha of invaded land [48].
While O. ficus-indica was purposefully introduced to India in the seventh century by the British for cochineal dye production and as a fruit crop species, it failed to establish, and therefore, it is not listed as an invasive species. The failure of these plantations to establish is associated with pest insects and multiple flooding events [47]. This finding suggests that in addition to purposeful, human-aided introduction, release from herbivory and pests plays an important role in the invasive spread of these Opuntia spp.
To date, three Opuntia spp. have been deliberately introduced to China [49][50][51]. Opuntia stricta was introduced in 1702, O. monacantha in 1625 and O. ficus-indica in 1645. They are all now classed as Group III weeds, defined as being invasive species that only occupy a small area and have low harmful impacts on humans and the environment [52]. Opuntia ficus-indica and O. stricta are now invasive across five provinces in China, while O. monacantha is invasive in six [42,49]. These three Opuntia spp. occupy different envi- ronments throughout China. Opuntia monacantha is often found growing on slopes near coastal areas, O. stricta is also mostly found at sea level growing in rocky or sandy soils, while O. ficus-indica is more suited to hot and dry valleys [52]. In addition, O. ficus-indica is widely grown for its fruit throughout China, but it is currently unknown the extent to which these cultivations have reached [38]. As these Opuntia spp. have escaped cultivation, it appears the populations are contained and are not spreading. Opuntia stricta is currently widespread in Yemen, where it is having a significant impact on both environmental and human health, and there is no access to controlling the populations using biological control agents [53].

Oceania
At least 20 Opuntia spp. are naturalized in Australia, all of which, with the exception of O. ficus-indica and O. dejecta, are on Australia's 'Weeds of National Significance' list [54]. Opuntia stricta is the most widely distributed Opuntia spp. in Australia, and this species has been observed in all states and territories [55]. Opuntia ficus-indica has also been recorded in all states and territories, with the exception of Tasmania [56], while O. monacantha has only been recorded in Queensland, New South Wales, South Australia, Western Australia and Victoria [57].
Opuntia monacantha was the first species introduced to Sydney in 1787 from Rio de Janeiro, in the hope of developing a cochineal dye industry [15]. It was also introduced as an affordable fodder for livestock, living fencing, fruit production and ornamental purposes [15]. Opuntia monacantha increased at a prolific rate throughout Queensland, increasing from 10,000,000 acres (approximately four million hectares) in 1900 to 60,000,000 acres (over 24 million hectares) by 1925 [58]. In climatically favourable years, O. monacantha could increase its population size by over 10 million hectares [57]. Opuntia stricta was introduced to Scone, NSW, for cultivation in 1939, from which it escaped and consequently prolifically spread across the border into Queensland [59]. By 1843, it was a significant weed throughout Queensland, covering an area of 240,000 km 2 [58,59].
Opuntia ficus-indica was also deliberately introduced to Australia in the 1840s for cultivation of its high-quality fruits [15]. It escaped cultivation and has adapted to a wide variety of environments including coastal sites, woodlands, grasslands and scrublands, being most climatically suited to the southern half of the continent [54].
In 1912, investigations into finding a suitable biological control agent was commissioned by the Queensland Government, which resulted in the successful introduction of the cochineal insect, D. ceylonicus. This insect provided significant control of O. monacantha, and almost resulted in its complete eradication from Queensland [60]. Soon after, D. opuntiae was introduced to target both O. stricta and O. ficus-indica, and displayed similar levels of success [55,56]. Cactoblastis cactorum was introduced in 1926, and the high density released in Australia resulted in almost complete eradication [54]. The combination of these biological control agents, in addition to cultural and chemical methods, have provided ongoing control of all Opuntia spp. in Australia.
Three Opuntia spp. are naturalized in New Zealand, including O. monacantha and O. ficus-indica [61,62]. Opuntia monacantha was introduced from southern Brazil and Argentina as an ornamental, where it escaped and was naturalized by 1855 [58]. Opuntia ficus-indica, on the other hand, was not considered naturalized until 2000 [62,63]. Opuntia monacantha is listed as a significant weed in New Zealand, but information detailing its environmental and economic impact is limited [62,64]. These Opuntia spp. have become problematic to New Zealand's coastal areas and beaches, as they grow well in sandy soils and are tolerant to moderate levels of salinity [62,64], although cladode growth is significantly reduced by moderate salinity [63].
Many of the Pacific Islands have introduced various Opuntia spp. for cultivation, with O. monacantha being the most widely established species. Fiji and Samoa have declared O. monacantha to be a noxious weed [65,66]. This species has also been recorded as invasive in the Fijian Islands, New Caledonia and the Philippines [7]. In these areas, information regarding the extent of the species' invasiveness is not stated [65,66]. Opuntia stricta is also considered invasive in New Caledonia and the Solomon Islands [65,66].

Climate Suitability
Opuntia spp. are well suited to areas with low precipitation and high temperatures, and they can tolerate moderate salinity. The ability of these plant species to be competitive in these harsher environments has assisted in their spread throughout arid, semi-arid, Mediterranean and coastal climates, particularly in degraded and over-grazed landscapes [2]. They prefer shallow, well-drained soils, and have been found growing well in rocky and sandy areas [2,6,8]. Their distribution has been observed to be restricted by latitude and altitude [27], as frost usually kills the growing apical meristems, although some frost tolerance has been observed in O. stricta and O. monacantha [6,8], which has assisted in these species invading temperate climate zones where winter frosts are common.

Physical Description
Opuntia spp. have several ecological and biological attributes that promote their establishment and spread when introduced to a novel environment, with these features providing a particular advantage in arid areas. An important growth trait that is unique to Opuntia spp. is the growth form of the cladodes, which are flattened succulent stems that grow in a direction that minimises their surface area exposed to the sun at the hottest part of the day, allowing the plants to avoid excessive heat stress [2]. Between Opuntia spp., cladodes differ in shape, size and colour, which influences their growth form and cladode-detachment, which is a vital mechanism for asexual reproduction [2]. Their fastgrowing, shallow root system is one of these key adaptive strategies [2,67]. Within two years, their roots can spread 2.5 m from the plant's stem, which allows Opuntia spp. to efficiently absorb water from light rainfall events [1,67]. Furthermore, during significant rainfall events, fine, temporary 'rain-roots' are rapidly produced to assist in additional water uptake [67]. Glochids are fine, hair-like spines that are present in wild Opuntia spp. and can provide some protection against herbivory. Due to the risk that glochids pose to the health of humans and animals, they are often absent or reduced in cultivated varieties . The glochids play an additional role in harvesting water by collecting and channelling it towards the plant [69]. Opuntia spp. have also developed strategies that significantly reduce water loss from transpiration. These include (i) producing spines in place of leaves to reduce surface area, (ii) exuding a waxy coating to protect the cuticles, (iii) inducing a metabolic shutdown process called aestivation during summer to conserve energy, and (iv) using a CAM photosynthetic pathway, which allows for photosynthesis to occur with minimal transpiration [2].

Physical Description of Opuntia stricta
The dull, grey-green cladodes of O. stricta are 10-25 cm long and have an elliptical to obovate shape, and rather than growing tall (the plant only reaches 2 m), it has a sprawling shrub-like growth form, allowing it to rapidly spread across the landscape ( Figure 1) [6,54]. This lateral growth form contributes to the hostile invasiveness of this weed, as once it is established, it smothers light and space for competing plants more rapidly than those with vertical growth. This species is considered the most aggressive Opuntia spp. worldwide and is listed among "100 of the World's Worst Invasive Alien Species" [70]. Opuntia stricta has approximately 80 glochids surrounding each areole, which are 5 mm in length [69]. Opuntia spp. produce one sessile flower at the areole, and these are often yellow to orange for O. stricta [54]. Opuntia stricta has approximately 80 glochids surrounding each areole, which are 5 mm in length [69]. Opuntia spp. produce one sessile flower at the areole, and these are often yellow to orange for O. stricta [54].

Physical Description of Opuntia monacantha
Opuntia monacantha has larger cladodes than O. stricta, ranging between 20-30 cm in length. This species is colloquially known as drooping prickly pear, and as the name suggests, it has a drooping appearance [15]. Despite this, the bright green cladodes are  [8,54]. Opuntia monacantha produces mostly spineless, green to red fruit from yellow flowers [8,54]. Opuntia monacantha has larger cladodes than O. stricta, ranging between 20-30 cm in length. This species is colloquially known as drooping prickly pear, and as the name suggests, it has a drooping appearance [15]. Despite this, the bright green cladodes are strongly attached, allowing it to grow up to 3.5 m in height ( Figure 2) [8,54]. Opuntia monacantha produces mostly spineless, green to red fruit from yellow flowers [8,54].

Physical Description of Opuntia Ficus-Indica
Opuntia ficus-indica has similar shaped cladodes to O. stricta. They are a pale bluegreen colour and are considerably larger (20-60 cm long) and more firmly attached, giving it a tree-like structure and allowing it to reach up to 5 m in height ( Figure 3) [7,54]. The large cladodes of O. ficus-indica have high concentrations of mucilage, which is a waterabsorbing carbohydrate that allows the cladode to hold higher volumes of water [71]. This contributes to its success in ecosystems prone to drought [71]. While this species is globally cultivated and these domestic varieties are often free of glochids, wild O. ficus-indica

Physical Description of Opuntia ficus-indica
Opuntia ficus-indica has similar shaped cladodes to O. stricta. They are a pale blue-green colour and are considerably larger (20-60 cm long) and more firmly attached, giving it a tree-like structure and allowing it to reach up to 5 m in height ( Figure 3) [7,54]. The large cladodes of O. ficus-indica have high concentrations of mucilage, which is a waterabsorbing carbohydrate that allows the cladode to hold higher volumes of water [71]. This contributes to its success in ecosystems prone to drought [71]. While this species is globally cultivated and these domestic varieties are often free of glochids, wild O. ficus-indica have small (10 mm long) glochids which return within several generations of escaping domestication [32]. The flowers of O. ficus-indica are bright yellow, red or orange and can reach 9 cm in diameter [54,72,73]. The colour of their fruit can also vary, showing similar colours to the flowers, and are mostly spineless or have spines that are very fine and easy to remove. Fruit maturation occurs in late summer for O. ficus-indica, approximately 30-70 days after anthesis, and each fruit contains upwards of 200 viable seeds [74]. have small (10 mm long) glochids which return within several generations of escaping domestication [32]. The flowers of O. ficus-indica are bright yellow, red or orange and can reach 9 cm in diameter [54,72,73]. The colour of their fruit can also vary, showing similar colours to the flowers, and are mostly spineless or have spines that are very fine and easy to remove. Fruit maturation occurs in late summer for O. ficus-indica, approximately 30-70 days after anthesis, and each fruit contains upwards of 200 viable seeds [74].

Pollination
Floral buds begin to emerge from areolas during the spring months for O. ficus-indica, which are triggered as a result of increased average daily temperature (at least 14 °C) and extended day lengths (of at least 12 h) [34]. Anthesis occurs mid-spring to summer for all three species, and multiple pollination methods are viable, with allogamy being the most common [12,29,33]. Opuntia spp. are able to attract a diversity of pollinators to enhance allogamy, and O. ficus-indica flowers are visited by more than 50 insect species, with Hymenoptera, particularly bees, providing the highest pollination success [29,[33][34][35][36].

Pollination
Floral buds begin to emerge from areolas during the spring months for O. ficus-indica, which are triggered as a result of increased average daily temperature (at least 14 • C) and extended day lengths (of at least 12 h) [34]. Anthesis occurs mid-spring to summer for all three species, and multiple pollination methods are viable, with allogamy being the most common [12,29,33]. Opuntia spp. are able to attract a diversity of pollinators to enhance allogamy, and O. ficus-indica flowers are visited by more than 50 insect species, with Hymenoptera, particularly bees, providing the highest pollination success [29,[33][34][35][36].
The flowers are considered botanically perfect, meaning they contain both male (stamen) and female (carpel) reproductive organs [2]. It has been observed that the preferred sexual reproductive strategy is xenogamy [72]; however, some flowers are self-compatible, allowing for self-fertilization [2]. The ability to self-fertilize gives these Opuntia spp. an adaptive advantage when introduced to a new area, or areas where suitable pollinators are rare or absent. The benefits of producing viable fruit and seeds in a novel environment enhance their ability to attract animals to facilitate their spread [75].

Seed Dispersal
Opuntia spp. produce brightly coloured fruits that attract a diversity of birds, reptiles and mammals for wide-scale seed dispersal [33,34,37,40,76]. Throughout Africa, a wide variety of animals have contributed to the rapid expansion of Opuntia spp. It was observed that elephants can transport seeds up to 15 km ahead of their current invasive range [34], and many frugivorous birds dispersed seeds over great distances, allowing these species to reach islands [76]. The presence of arils on Opuntia seeds also attracts dispersal and burial by ants (myrmecochory), which may act to protect the seeds from opportunistic predation [77].

Seed Dormancy
The thick seed coats in Opuntia spp. provide a mechanical barrier that prevents the protrusion of the radical, resulting in physical dormancy [78]. Over 90% of O. stricta seeds demonstrate long-term persistence, with the seeds remaining viable through dormancy for up to 20 years [16,74], and O. monacantha seeds have been observed to remain viable for up to 15 years [72].

Seed Germination
Opuntia spp. have been observed to have low rates of seed germination under both laboratory [77][78][79] and natural field conditions [80]. Additionally, rates of seed germination for O. ficus-indica [78] and O. stricta [18] were enhanced by light, but Podda et al. [30] found no significant difference between alternating photoperiods and complete darkness for O. ficus-indica. Increasing concentrations of salinity has been shown to reduce seed germination of O. ficus-indica but, nevertheless, the seeds were able to tolerate moderate salt concentrations and did not lose viability under high saline concentrations, indicating they could germinate and flourish in coastal regions [30]. While O. ficus-indica has observed low germination rates in the wild, domesticated varieties with high viability and vigour have been selected, demonstrating accelerated imbibition rates [81].
Alternating temperature regimes of 30/20 • C, scarification and sufficient water availability have provided the highest germination rate (approximately 80%) in O. stricta, which would coincide with spring and early summer conditions [16]. Often, scarification of the seeds can be achieved through the process of the seeds passing through the digestive tract of animals [76]. This was, however, not the case for O. stricta, which had significantly reduced viability after consumption by animals [76], suggesting other environmental disturbances, such as fire, may provide important germination cues for this species. It has been found that scarification of O. ficus-indica [30,78], O. stricta [16] and O. monacantha [72] seeds under laboratory conditions improved germination rates.

Vegetative Reproduction
To increase reproductive odds in an arid environment, Opuntia spp. are able to vegetatively reproduce, whereby any part of the parent plant with areoles that break away will develop roots and grow into a new plant [74,82]. Whilst this most often involves a cladode, vegetative reproduction from underdeveloped fruits has also been observed [2,16]. When areolas of the detached cladode come into contact with the soil surface, they will form roots and subsequently grow into a new plant [29].
Most often, cladodes will fall near the parent plant, attributing to dense populations, but it is possible for cladodes to be effectively dispersed via geochory and hydrochory. Spines can enhance dispersal by attaching to animals, boots and vehicles. Cladodes can survive for a considerably long period without sending out roots, and have remained viable for up to three years in a sealed container [72]. It is particularly relevant that vegetative reproduction has very high success rates in Opuntia spp., often with a 100% survival rate [74].

Management
The most appropriate control methods are often dependent on the invasion stage of the cactus infestation. Due to the prolific vegetative reproduction ability of these Opuntia spp., coupled with animal-assisted seed dispersal, the integration of multiple control methods is often needed to achieve sufficient control. This can include various combinations of cultural, chemical, manual and biological methods to kill standing plants, reduce the seedbank and prevent regeneration. Control efforts often take several years of consistent application before a significant reduction in the population can be observed, and thus, preventative measures should be ongoing.

Management Intervention for Early Invasive Stages: Introduction and Colonisation
The most ideal solution for targeting Opuntia spp. is to prevent invasion by maintaining a highly functional and competitive system. This was observed by Strum et al. [34], whereby O. stricta was not a problem weed for over 50 years in the Kruger National Park, South Africa, until the ecosystem underwent a state change caused by overgrazing and increased urbanisation, allowing the weed to establish and become widely spread. In addition to restoration and maintaining healthy land, invasive species hygiene practices are essential to prevent unintentional introductions. Hygiene practices, in this sense, refer to the measures taken to prevent the spread of invasive plant propagules by removing seeds and contaminated soil, water and organic materials from clothing, footwear, vehicles and equipment [83]. This includes inspecting vehicles and machinery after being used in an invaded site, using hay which is free of Opuntia seeds, and regularly inspecting the property and removing and immediately destroying any emerging Opuntia spp. [72,84].

Grazing
Livestock and wildlife can be used to reduce small populations of Opuntia spp. by grazing the cladodes [37,84]. In times of drought, consumption of cladodes can provide hydration as well as sustenance when other forage materials may be limited [84,85]. However, the spines and glochids can result in ulcerations and sores around the eyes and mouths of livestock, and providing supplementary feed will be required to prevent a build-up of glochids in grazing animals' stomachs. In some cases, to encourage livestock to graze the Opuntia spp., land managers have used blow torches to singe away glochids, allowing livestock to graze with reduced physical harm [84]. It is unlikely that grazing alone would provide complete control of a moderate invasion, and it would be critical for any dropped cladodes to be sprayed to prevent vegetative reproduction, as well as monitoring the site for any seed germination that may have passed through the grazing livestock.

Chemical Control
Arsenic pentoxide was first trialed for the control of O. stricta and O. monacantha in 1916 [5,6,27]. This herbicide has been replaced with more widely available herbicides, including glyphosate [19], MSMA [51], picloram and triclopyr, with the latter two often used in combination [54]. Herbicides can be sprayed directly on the foliage, but they must be applied with care as any areas missed will regenerate [3,54]. Furthermore, the uptake of herbicides is restricted by their thick epidermal cells, which prevent absorption of the herbicide, and this is further enhanced by the stomata remaining closed during the day, which is often the time of the herbicide application, reducing the rate of herbicide absorption [86]. To overcome these barriers, herbicides can be directly injected into either the topmost cladodes [19] or to the plant's stem [87]. As Opuntia spp. often grow in unproductive locations that are unsuitable for cultivation, the cost:benefit ratio for control is often financially unviable, which results in many populations being left untreated [58].

Grubbing
Manually removing Opuntia spp. is highly effective; however, doing so can pose a hazard to human health and safety. It is also important to consider the reproductive methods of Opuntia spp., as in most cases, they can either directly recolonise from the seedbank or vegetatively regenerate unless every part of the plant is removed [19]. As a consequence, the removed fragments must be treated and sufficiently buried to prevent regeneration [88]. Pre-burial treatments include soaking the plant fragments in water for 20 days to accelerate the rotting process, or burning the plant fragments [86].

Fire
While cacti are not fire tolerant, their high-water content acts to resist fire and makes them difficult to ignite [89]. Therefore, in order for fire treatments to be most successful, they should be implemented when the plants are dry. Implementing fires when the plant is drier after the summer resulted in 96% mortality of Opuntia spp., compared to only about 50% mortality during a winter burn [20]. In the USA, aerial spraying of large infestations with Picloram (2-4 pints per acre) has been observed to dry the plants, and thus, promote more effective burning during summer [84].

Management Intervention for Late Invasive Stages: Landscape-Scale Spread
Within their native range, Opuntia spp. do not often become invasive due to natural enemies, such as grazing mammals, insects and diseases, that maintain population levels. The establishment of biological control agents to tackle landscape-scale infestations is the most economical solution for long-term control [90]. When infestations of Opuntia spp. are widely spread, grazing mammals are not suitable for control as they can assist in dispersal of seeds and vegetative segments, whilst dense populations can restrict movement and cause the animals injury. Several insects, fungi and diseases have been trialed for controlling various Opuntia spp. on a landscape scale. Amongst these, the cochineal insect (Dactylopius spp.) and the cactus moth (Cactoblastis cactorum) have provided the most significant control and have been the most globally adopted.

Cochineal Insect
In many cases, the cochineal insect, Dactylopius coccus (from order Hemiptera and the Dactylopiidae family), was globally introduced alongside O. ficus indica and other domesticated varieties for coccidoculture (cochineal breeding) to produce carminic acid, an important and diversely useful red pigment obtained by crushing the sessile females [91]. There are 11 known Dactylopius spp. in this monophyletic genus, all of which are parasitic of cactus plants [92]. These insects are native to North or South America and, like the Opuntia spp., have evolved to tolerate arid and water-limited environments [91]. Cochineal insects are attractive biological control agents as they display host specificity and feed on only one or a few closely-related Opuntia spp. [3,54,93].
Cochineal insects display sexual dimorphism and drastic differences are observed in the appearance and behaviour of adults [18,94]. The female cochineal insects have three life stages after hatching: the nymph stage, an intermediate nymph stage and the adult stage [18,95]. During the nymph stage, emphasis on finding a suitable feeding position is priority, and their bodies are covered in fine bristle to assist in wind dispersal, moving from a crowded cactus to a less populated plant [96]. During the intermediate stage, the insect inserts its mouth piece into the cactus and remains sessile in the spot for its entire life [18,60]. In this position, it then undergoes two malting events, where it develops a waxy coat for protection from harsh environmental conditions and predation [94,97], as shown in Figure 4. It enters the adult life stage after the second malting phase, where it reaches sexual maturity [94,95]. Male cochineal insects also undergo a similar nymph and from a crowded cactus to a less populated plant [96]. During the intermediate stage, the insect inserts its mouth piece into the cactus and remains sessile in the spot for its entire life [18,60]. In this position, it then undergoes two malting events, where it develops a waxy coat for protection from harsh environmental conditions and predation [94,97], as shown in Figure 4. It enters the adult life stage after the second malting phase, where it reaches sexual maturity [94,95]. Male cochineal insects also undergo a similar nymph and intermediate nymph life stage; they develop wings in their adult life stage and are rarely observed feeding on the cacti [95]. Dactylopius coccus, as well as D. austrinus, D. ceylonicus, D. confuses and D. opuntiae, have all been trialled for the control of O. stricta, with only the latter providing extensive, widescale control, which has been subsequently exploited in Australia, Africa and the Middle East [36,98]. The 'ficus-indica' biotype of this species has also been identified to effectively target and control O. ficus-indca and provide reasonable, but not complete, control for O. monacantha [99]. Higher control levels were observed with D. ceylonicus for controlling O. monacantha throughout Africa and Australia [45,100].
The widely commercialised D. coccus has one of the broadest host ranges, and has been reported to feed on at least 14 Opuntia spp. [18,101]. This is the only cochineal insect that produces a high enough concentration of carminic acid to be considered economically Dactylopius coccus, as well as D. austrinus, D. ceylonicus, D. confuses and D. opuntiae, have all been trialled for the control of O. stricta, with only the latter providing extensive, widescale control, which has been subsequently exploited in Australia, Africa and the Middle East [36,98]. The 'ficus-indica' biotype of this species has also been identified to effectively target and control O. ficus-indca and provide reasonable, but not complete, control for O. monacantha [99]. Higher control levels were observed with D. ceylonicus for controlling O. monacantha throughout Africa and Australia [45,100].
The widely commercialised D. coccus has one of the broadest host ranges, and has been reported to feed on at least 14 Opuntia spp. [18,101]. This is the only cochineal insect that produces a high enough concentration of carminic acid to be considered economically viable for coccidoculture [18]. While this species feeds on a variety of invasive Opuntia spp., it is not a suitable biological control as it does not cause significant harm to adult plants [18].
Not all environments are suitable for establishing the cochineal insect as a biological control agent, and establishment has failed in some regions and countries [20,47]. Rainfall has a significant effect on colony survival of D. opuntiae, with 15 min of rain being enough to kill an establishing colony, and small colonies can be washed away after 120 min. In larger populations, at least 40% of the initial population was removed from the cladodes after 30 min of rain. Therefore, biological control is not suitable in areas that receive regular rainfall [102].

Cactoblastis Moth
The phycitid moth, Cactoblastis cactorum (from the Lepidoptera order and Pyralidae family), is known for its successful control of O. stricta in Australia [100]. The Cactoblastis genus is native to southern South American countries, and C. cactorum is specifically native to Argentina, Uruguay and Paraguay. Unlike cochineal insects, the moth has a broader host range among Opuntia spp. [103,104]. Despite being native to South America, it has provided partial or complete control of invasive North American Opuntia spp., including O. stricta and O. ficus-indica [38].
The moths lay their eggs in a stick-like cluster on a cladode that is camouflaged to look like a cactus spine [105][106][107]. The emergence of the orange larvae occurs in unison, and this allows the insects to work together to break through the thick outer layer of the cactus and feed inside the cladodes and stems [38]. While feeding, C. cactorum work as a colony to tunnel and consume an entire cladode, leaving only the fibrous vascular layers untouched [18]. Mature Opuntia plants with woody cladodes are often less affected by the moths than younger plants with fresh cladodes, as the larvae struggle to break through the hardened outer layers [38].
In addition to the damage caused by larval feeding, the openings allow for diseases to enter the cactus and assist in killing the plant [108]. The cladodes detach from the plant, and these rotting cladodes provide the moth with shelter after they drop to the ground to pupate [18]. The emerging adult moths are inconspicuous, with brown to white wings and bodies [105,106]. The moths only live for nine days as adults due to their underdeveloped mouthparts, preventing them from feeding [38]. Therefore, dispersal is limited by this short life span of the adult females, and in Australia, C. cactorum populations have only travelled about 24 km from their site of establishment within 2.5 years, whilst in South Africa, they have only travelled 6 km within the same time frame [38,60].
In addition to suitable climatic conditions for the establishment of C. cactorum, population density is the biggest influence on the success of this moth as a biological control agent [109]. In Australia, C. cactorum provided excellent control of O. stricta due to the extensive resources available in terms of rearing facilities and volunteers, and approximately two billion egg sticks were released within three years [58,60,109]. It has been found that Opuntia spp. will survive low densities of the moths, where, for example, in South Africa's Kruger National Park, the cladodes of O. stricta were only partially consumed, and when they detached from the parent plant, they were able to vegetatively regenerate, resulting in the population increasing [39].
The O. stricta plants in South Africa were also identified as being larger than the Australian population, which usually have less than 14 cladodes, and it is known that the moths are less affective against larger plants where the older cladodes are usually hardened, preventing the larvae from burrowing inside [110][111][112]. In South Africa, the cactus moth was also introduced to target O. ficus-indica, but it did not successfully kill the plants due to low density numbers [110]. It was found that the moths' eggs and larvae were suffering higher predation rates from wildlife compared to those recorded in Australia, which prevented the population from reaching the required density [39,111]. However, the moth did cause enough damage to reduce the reproductive output of O. ficus-indica, and slowed the rate of the weeds' spread [113]. Additionally, a small release of 60 egg sticks on O. stricta in the Kruger National Park had a noticeable impact on the population density, but did not provide complete control [109].

Key Findings
The global invasive spread of O. stricta, O. monacantha and O. ficus-indica has been facilitated by their purposeful introduction for crop cultivation and other human uses, as well as several key ecological traits that promote their dominance [114]. These key ecological traits and the associated management challenges are outlined in Table 1. Table 1. Summary of key ecological traits of the three Opuntia spp. explored in this review, and how these traits facilitate their establishment, invasive spread and dominance in a landscape. The management challenges associated with these ecological traits are described.

Ecological Trait Facilitates Invasion Management Challenges
Generalist growth conditions Tolerant to a broad range of climates and environments and can tolerate extreme heat as well as light frost.
Opuntia spp. populations can establish in different landscapes and environments, all which may require different management strategies. Bright flowers and fruit attract a variety of pollinators and dispersal agents.

Glochids and spines
Protects cladodes from animals grazing, and can result in overgrazing of desirable plant species. Glochids and spine cause hazards to human health and can limit access to control dense populations of Opuntia spp. Further, the spines can assist in cladode attachment to shoes, clothing, vehicles and equipment for dispersal, therefore hygiene practices are essential to prevent spread.
Assists to harvest moisture in times of water scarcity.
Assists in dispersal of cladodes for vegetative reproduction.

Reproduction
Utilizes both sexual and vegetative reproduction.
The ability for these weeds to vegetate poses a challenge to control actions, as all cladodes must be either removed, buried, or treated to prevent the plant re-establishing. The long flowering and fruiting season can make it and ongoing challenge to reduce seed production and dispersal.
Cladodes can survive for an extended period on the ground before establishing roots.
High cross-pollination to improve genetic diversity.
Flowering and fruit production can continue for several months.
Some flowers are self-pollinating to ensure seed and fruit production in areas with small populations and/or limited pollinators.

Low fire tolerance
The high-water content of Opuntia sp. makes them difficult to ignite. In areas with high population densities, fire regimes are reduced in frequency or intensity, and this reduces biodiversity and native regeneration from the seedbank.
Fire is often an effective restoration tool for fire-prone ecosystems. Fire is often an economical control action to implemented at a land-scape scale, however Opuntia spp. do not effectively carry fire and this treatment is only beneficial when the plants are dry, usually after summer.

CAM photosynthetic pathway
The stomata are often closed during the day, particularly on hot days to conserve water. The stomata being closed throughout the day can limit the ability for herbicide to enter the plant. Reduced transpiration and photorespiration.
Thick, waxy coating The thick, waxy coating on the cladodes act to protect the cuticle and conserve water.
The thick, waxy coat of the cladode act to block herbicide application, which significantly reduces the effect of spraying herbicide. The alternative for land managers is to inject the plants with herbicide, however this is extremely time consuming and poses a significant health risk.
Fast growing and responsive root system Opuntia spp. quickly establish fibrous root systems that can outcompete other plants for water. Temporary rain-roots allow for rapid uptake of water in areas of unpredictable rainfall.
Fibrous root systems make it challenging to remove plants through manual removal control actions such as grubbing.

Seed dormancy
The hard-coated seeds are able to persist in the seedbank for an estimated 20 years. Long-lived persistent seedbanks pose significant ongoing challenges to treated landscapes. Seedbank recruitment needs to be monitored and any emerging seedling should be controlled for at least 20 years post control actions.
The seed coat can be scarified by the digestive tract of animals. This promotes germination after dispersal.
Scarification can be also achieved by disturbance events, allowing seeds to germinate under low competition.
Limited enemies outside native range There are no natural predators to Opuntia spp. outside of its native range, which allows populations to grow larger and faster than in their native range.
Establishing biological control agents is a time consuming and expensive process. Extremely high numbers of C. cactorum egg sticks are required in order for this species to have a significant impact on population densities. Using Dactylopius spp. for control is dependent on climate, thus biological control agents are not suitable for cool climates, or areas with regular rainfall.
The key to the successful establishment of these Opuntia spp. is directly linked to the purposeful, human-aided introduction to almost every country where they are considered invasive. It is known that colonization pressure is increased for species that are purposefully introduced as they often have increased genetic diversity, with high numbers of individual plants or seeds being introduced to promote their establishment [115,116]. These Opuntia species were able to escape their cultivated range and establish wild populations via the effective dispersal techniques observed for these species, including: zoochory, hydrochory and attachment to vehicles, clothing and equipment. As a result of this, multiple populations were able to establish across landscapes free from natural predators and, as a result of the sharp spines and glochids, grazing animals avoided these species.
The glochids and spines also present significant health risks to humans and the dense thickets can prevent access to implement control actions, such as herbicide application, by foot. Aerial spraying Opuntia spp. populations with herbicide is often thwarted as a result of the thick waxy coat that reduces the herbicide uptake, and this is further restricted by the CAM photosynthesis that allows the stomata to remain closed during hot and dry weather conditions. It has been observed that invasive species that greatly differ from native species can have a competitive advantage [117], and CAM photosynthesis is unique to the Cactacaeae family and has significant advantages over the C 3 and C 4 photosynthetic pathways in water-limited and hot climates.
As a result of the release from natural enemies in their invasive range [118], coupled with the low grazing pressure from native mammals and livestock due to the hazardous glochid [119], these Opuntia spp. were likely able to increase their competitive ability through designating more resources to higher fecundity and growth [120,121].
Therefore, the introduction of biological control agents is the best solution for landscapescale control of Opuntia spp. However, there are several challenges associated with establishing the two currently used genus of species. Cactoblastis cactorum has been successful only when high volumes of egg sticks are simultaneously released to target a population, while moderate volumes can only reduce the further spread. The challenges associated with the highly successful Dactylopius spp. include the sensitivity of these insects to cool climates and rainfall.
The final challenge associated with managing Opuntia spp. is associated with the long-lived, persistent seedbank, with seeds being observed to remain viable for up to 20 years. Due to the wide dispersal potential of the seeds, new populations could emerge in seemingly unaffected areas, or in areas that have previously successfully controlled the Opuntia spp. invasion. Any populations left unchecked to re-emerge from the seedbank would likely successfully establish as a result of the diversity of reproductive strategies these species can adopt, including sexual reproduction by xenogamy or self-fertilized flowerers, as well as vegetative reproduction. It has been noted that these Opuntia spp. seedlings are not competitive and they often invade after continuous ecosystem disturbance. However, re-emerging Opuntia spp. have been observed in areas of high, competitive, native grass cover [122], which adds further complexity to post-treatment restoration efforts.

Recommendations for Future Research
Much of the literature for controlling Opuntia spp. has focused on the discovery of suitable biological control agents, which has been seen to be successful in many parts of the world, and these efforts are enhanced when multiple species are introduced and cultural and chemical controls are combined [53]. In regards to the seed ecology for O. ficus-indica, O. stricta or O. monacantha, more research is required. Whilst light and temperature requirements have been studied, as well as factors affecting dormancy, investigation into other factors such as salinity, water availability, intermitted water availability, heat exposure, burial depth and seed longevity could assist in planning follow up management or understanding how to uniformly break dormancy or devitalise the seeds. Further research into fast and effective treatments to use on manually removed plants prior to burial would significantly enhance physical removal treatments, and the provision of more information on landscape-scale restoration projects that target sites invaded by Opuntia spp. would be beneficial for modelling similar future restoration projects.

Conclusions and Management Implications
The combined factors of prolific fruiting, strong vegetative reproduction and hazardous physical traits, with dense growth forms, spines and glochids, make O. stricta, O. ficus-indica and O. monacantha globally significant weeds. The findings of this review demonstrate that biological control agents provide the most effective landscape-scale control of invasive Opuntia spp., especially in degraded, nonarable areas, with dense populations quickly decimated when effectively applied. As Dactylopius spp. are species specific, they pose little threat to cultivated varieties or native vegetation. Due to the prolific vegetative reproduction of these species, after the implementation of biological control agents, it would be advised that any surviving cladodes be removed or treated with herbicide to prevent reestablishment. Further seedling emergence should be monitored for up to 20 years due to the persistent seedbank as a result of the seeds having mechanical dormancy due to the thick seed coats. In areas where biological control agents are not suitable, due to either cooler climates, high rainfall zones or limited funding, fire has been observed to successfully remove dense populations when implemented after summer, when these weeds are at their driest. It would be recommended to also treat cladodes that were not completely killed by the fire. Monitoring seedbank emergence would be critical as fire treatment may increase germination rate and uniformity, as fire is known to scarify hard-coated seeds. Once these Opuntia spp. are treated and removed, it would be beneficial to establish competitive and diverse native plant cover to outcompete seedlings for long-term control.
It is recommended that further research investigates the longevity of the seedbank of these three Opuntia spp. and ways to promote uniform germination to flush out the seedbank and target the emerging plants while they are in the juvenile form, as small plants are easier to kill than adults. Biological control should be further investigated for non-American countries that have not yet implemented successful introduction programs. Community awareness initiatives have been effective in reducing infestations of Opuntia spp. (as seen in Portugal and South Africa), and a focus to develop similar programs in other countries could also be highly beneficial.
Author Contributions: T.H.; conducted research, paper design and writing, editing, S.F.; paper conception, editing, S.C.; sourced photographs, editing. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.

Conflicts of Interest:
The authors declare there are no conflict of interest, and that this research did not receive any funding.