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Home , Bergerocactus, Cactus, Cylindropuntia, Cylindropuntia bigelovii, Ferocactus, Ferocactus cylindraceus

Torrey Pines Docent Society 2019 Adaptation and Conservation Cacti are in the Lodge garden, the Whitaker Garden, and almost all the trails in TPSNR, but there is a lot more to simply look for the silver Argiope and the . Cacti exhibit many specialized adaptive features to an arid climate. For children, the discussion can revolve around adaptation. For adults, one can highlight conservation issues that confront slow-growing cacti.

Key points: • Green stem with spines? This is the first visual clue that cacti are specialized for something. What we observe are adaptations to survive in a dry climate. To reduce evaporative water loss ( loss), cacti have several adaptations: ◦ Cacti make spines, which are modified , to reduce surface area and to protect themselves from thirsty animals. (Nonetheless, there may be tiny foliage leaves on a very young stem.) ◦ The stem takes over the task of . Not only that, the stomata (microscopic openings for gas exchange) on the stem are closed during the day, and are only opened at night. ◦ Without sunlight, the cannot make use of immediately, and so it stores the gas as malic , which is the taste of sour apples. During the day, the plant converts back to carbon dioxide for photosynthesis. ◦ To reduce surface area, the entire plant is made of stems or stem segments. At the extreme, Barrel cactus takes on a globe-like shape. ◦ Cacti may have ribs or tubercles which allow the stem to expand or contract depending on their water content. ◦ The stem has a heavy waxy surface (cuticle). • Some specialized spines on the barrel cactus make a sugar solution to attract . The ants in turn drive away insect in a food-for-protection mutualism. • For protection, prickly-pear-related cacti also make glochids, essentially tiny, hair-like spines. They appear at the base of spines and on the , which become the prickly-pears. • The adaptations to survive in a dry climate come at a cost and that is cacti grow very slowly. As a result, many cacti and some succulent are threatened because of loss of habitat and illegal poaching for gardening and home décor. What is interesting about cacti? Most people know what a cactus is. They are the ones with succulent green stems and fierce spines. We may consider cacti as iconic of the American Southwest , but the cactus , Cactaceae, is quite diverse throughout the . There are about 127 genera and close to 2,000 species in the family. The also have a large variation in shape and size. Members of the family can be found in hot deserts, cold deserts, dry grasslands, coastal sage scrub, chaparral, and even alpine zones above the treeline. Regardless, these are all semi-arid or arid habitats. Where are the leaves? What are the roles of the spines? Why doesn’t the Indian fig have spines? Why are the stems green? Is this how I can survive in the ? In short, cacti are extremely well adapted to dry environments—they are . As aforementioned, cacti live in arid or semi-arid habitats, and as such they are highly specialized to survive in such environments. They carry out photosynthesis in their stems, and the spines can be considered as modified leaves to protect them from thirsty animals. The long answer follows. We shall look into their unique adaptations or specializations. The descriptions will focus on the key species in TPSNR. They are the Coast prickly- pear ( littoralis), Coastal cholla ( prolifera), the rare Coast barrel cactus ( viridescens), and the introduced Indian fig (Opuntia -indica). A few illustrations also make use of species from Anza-Borrego.

Figure 1. Left: Coast barrel cactus () with prominent ribs; Right: A close up on the two different types of spines. (The smaller, finer white ones might have secretory glands at the base, but no confirmation of this yet.)

2 Figure 2. Coastal cholla (). Left: A young stem made of tubercles; Right: A grown, expanded stem with tubercle-like undulations.

Cactus morphological features The cactus stem has many specialized features. For one, the stem has taken over the task of photosynthesis and this will be revisited below. Here, we look into the structural characteristics, and see how the stem is specialized for water conservation.

Stem structure and shape: Without leaves, cacti are easily recognizable by their stems. The stems generally can be cylindrical or flattened. Formally, a modified stem that replaces the functional role of leaves is a cladode.1 Columnar cacti are the ones with a main cylindrical cladode that we commonly call chollas. One example is the Coastal cholla (Cylindropuntia prolifera). We refer flattened cladodes as pads. Two examples are the Coast prickly-pear (), and Indian fig (Opuntia ficus-indica). All cacti take on some compact shape that may reduce the surface area. Here, the Coast barrel cactus (Ferocactus viridescens) is probably the most specialized. Its globular (globe-like) shape has a very small surface area to volume ratio, and is ideal for water storage.2

Many cacti have ribs and tubercles, which are small Figure 3. The woody nodule-like projections. Ribs are most distinct with a barrel skeleton inside Buckhorn cholla (Cylindropuntia cactus (Fig. 1). These structures allow the cactus stem to acanthocarpa) in Anza- expand or contract depending on water content. The ribs in Borrego. 1 Another term that one may come across is phylloclade, a modified . For cactus, cladode is the proper term. There is another similar spelling term, phyllode, which is a modified petiole that resembles and functions as a . This is what we find in acacia ( Acacia in Fabaceae) plants.

3 particular make a folded surface that impart strength to the structure. The groves on a ribbed surface also help to channel rainfall to the . When the sun is at an angle, the ribs provide a partial shade. Some cacti, notably the barrel cacti (genus Ferocactus) are known to tilt slightly toward the sun, especially on a slope, such that only the smaller top faces direct sun. Cacti with flattened stems have neither distinctive ribs nor tubercles. A columnar cactus such as the Coastal cholla can have tubercle-like undulations (Fig. 2). The Coastal cholla is unusual; its young cladode is made of tubercles. As the stem grows, the tubercles swell and the bases stretch out to become tepee-like. This is also the growth pattern with pincushion cacti (genus ). Unlike coconuts, we will not find liquid water. Cacti use water storage tissues, specialized thin-walled cells with a large water . The stem of a well hydrated Indian fig is close to 90% water. Some cacti can convert water into a mucilaginous substance that does not evaporate readily and lowers the freezing point of the tissue such that the cacti can survive cold winters.

Figure 4. Two views of glochids and spines arising from areoles in Coast prickly-pear (Opuntia littoralis).

To seal in moisture, cacti have thick, waxy cuticle on the surface. To reduce transpiration loss, cacti practically have no leaves (more on this with the spines below), and the stem takes over the photosynthesis function. Even though a cactus is mostly water, it is considered a woody plant. All cacti make a vascular cambium that produces both secondary (woody) xylem and secondary phloem.3 However, the xylem does not become heartwood—the plant uses the space for water storage tissue. The secondary xylem forms instead a hard fibrous matrix. This is most 2 Given a solid object, the sphere has the smallest surface area to volume ratio. 3 New, primary growth makes xylem that does not contain lignin, the substance of woody tissue. Subsequent growth of a stem laterally makes xylem that is lignified, and is referred to as secondary xylem, or as sapwood.

4 evident with a dead and partly decomposed cholla that exposes a cylindrical chain link fence-like woody skeleton (Fig. 3).

Figure 5. Two cacti with dense spine clusters. Left: Velvet cactus ( emoryi) planted near the Lodge garden; Right: Teddy-bear cholla () at Anza-Borrego.

Areoles, spines and glochids: With cacti, we do not find recognizable . Instead, the plants bear areoles, structures unique to the Cactaceae family. An areole is a much reduced shoot (axillary bud4) that appears as either a little pad or even a slight depression or pit under dry conditions, but from which grows the spines, glochids, , stems (cladodes), and stem arms on the in the .5 In short, the small oval thing at the base of the spines of a cactus is an areole (Fig. 4). Among things that grow from an areole, spines are the most evident, and they generally appear in clusters. We can say that spines are modified leaves.6 To be more precise, cactus spines are modified scales grown from an (areole). As a young spine grows from a bud, it quickly turns into a dead lignified fiber.7 Sometimes, the spines are covered by a loose sheath formed from the dried . This is presumably common with the Cylindropuntia species, but this is not evident in the Coastal cholla. (But in Anza- Borrego, we can observe that with the Buckhorn cholla, Cylindropuntia acanthocarpa.)

4 Areole is from the French aréole, which is taken from the Latin, areola, the diminutive of area, referring to a small open space or garden. In green plants, an axillary bud is an embryonic shoot located on the upper edge at the base of a petiole. The axillary bud is one of growing shoot, and in cacti, this bud becomes the areole. The areoles contain shoot apical (see next footnote). 5 The areole has what is called the shoot apical meristem (SAM). Meristem is undeveloped plant tissue that can grow into other kinds of cells and structures. They are equivalent to stem cells in animals. Meristem can be found in the and the tip of a growing shoot (stem tip), in which case it is called the SAM. 6 Thorns are modified stems. 7 Lignified is a scientific way of saying woody. Lignification is the process by which a plant deposits lignin in the cell walls to make a rigid, woody structure. However, a cactus spine may not appear as woody to the general public, and so using the term lignified may cause less confusion.

5 The nature of the spines varies. Barrel cacti are notable for their fierce looking stout spines, and hence their genus name Ferocactus. In some cacti, the spines are so dense that they help to condense morning dew and to provide a bit of shading for the stem (Fig. 5). Spines are evolved primarily to protect the plant from animals. They are not effective against small insect herbivores like the leaf-footed bugs (family Coreidae among the true bugs ). Several cactus genera make special spines that bear secretory glands at the base. These glands make a sweet -like secretion, called extrafloral nectar, that attracts ants. These ants drive away herbivory insects. Thus the two partners form an - cactus mutualism, or a food-for-protection mutualism. Locally, the Coast barrel cactus (Fig. 1) is known to bear specialized extrafloral nectar secreting spines, and they attract as many as 18 native ant species, visiting one kind at a time.8

Figure 6. Clusters of glochids on a cladode of Beavertail cactus () at Anza-Borrego, and a closeup in the insert. Without a magnifying glass, glochids appear as an innocent looking bump.

Figure 7. Foliage leaves on a young cladode of Coast prickly-pear (Opuntia littoralis). The image on the right is a slightly older cladode showing how the spines are starting to develop just above the leaves from the areole.

8 The presence of the invasive Argentine ant can alter the mutualism. See articles listed in the bibliography.

6 Glochids are modified spines developed as tiny, thinner-than-hair bristles, and are unique to the subfamily (only opuntioids have glochids).9 They are nastier than spines in the irritation that they cause. Even a gentle touch will dislodge them, and they break at their base as a cluster together. They are so short that they are embedded entirely in our skin epidermis and are extremely difficult to remove. We can find glochids at the base of spines growing from the same areole, say, on Coastal chollas (Fig. 4). The of the Opuntia has no spines but only glochids. Indeed, this is how the name prickly- pear came about—the pear, which is the fruit, is prickly with glochids. The Beavertail cactus (Opuntia basilaris) out in Anza Borrego is so specialized that it has no spines but protected entirely by these irritating glochids (Fig. 6). Cacti do make foliage leaves, but they are small, conical-shaped, and present only on very young stems (Fig. 7). As soon as the stem expands, the tiny leaves fall off, while its axillary bud develops spines and glochids. Why do they do this? A possibility is that the leaves help to speed up the growth of a young cladode. As soon as a stem grows large enough such that the contribution from the tiny leaves is insignificant, they are shed to reduce transpiration loss.

Roots: Cacti generally have shallow but extensive root systems to capture moisture from light . Some cacti also make the so-called roots. They are tiny roots made to take up water after a good rain, but die off quickly when dry weather returns.

CAM Photosynthesis in Cactus A result of functional adaptation to survive in arid and water-stressed environments, photosynthesis in cacti is different from what we learn in introductory textbooks. Before we address that, we should review the basic principles. In very simple terms, photosynthesis is a biochemical process by which carbon dioxide (CO2) and water are converted to oxygen and glucose, a six-carbon sugar, utilizing energy in sunlight. The process involves a series of very complicated steps. In green plants, these steps take place in a cell organelle called , which contains . We know chlorophyll as the green pigment crucial to absorbing light energy and transferring it to drive subsequent steps in photosynthesis. What makes things complicated is that there are different types of chlorophyll, and different green plants can carry out the photosynthetic steps in different pathways.10 Clearly, cacti are different. Without leaves, the cactus stem is the main photosynthetic , and its skin bears stomata, the microscopic openings for gas exchange that normally are present in the leaves of green plants. To reduce water loss (transpiration loss), the density of stomata on cactus stems tends to be lower than a typical leaf. More important, in reverse temporal order of a typical green plant, the cactus stomata are

9 Opuntioideae, the opuntioids, contains 15 genera, including the prickly-pears Opuntia, and the chollas Cylindropuntia. Note that the Velvet cactus, genus Bergerocactus, is in the subfamily. 10 Details can be found in biochemistry textbooks.

7 closed during the day, and they open only at night. Hence in darkness the stomata of cacti open up and allow carbon dioxide to diffuse into the stem. However without sunlight, the plant cannot utilize carbon dioxide immediately.

So the plant converts CO2 into malic acid for storage during the night. Next day with the sun out, the malic acid is converted back to CO2 for photosynthesis. All these activities occur inside the cells that contain . This strategy to store carbon dioxide as malic acid at night is not uncommon in the leaves of succulent or xerophytic plants. In fact, this form of photosynthesis is named Crassulacean acid metabolism (CAM), after the stonecrop family, Crassulaceae. The species in the family, thus including the yucca plants, work this way too. Malic acid is what imparts the sour and tart taste in many fruits, especially unripe ones. Malic acid was first identified in apple, genus Malus. Think sour green apples. So there can be a slight taste difference depending on what time of the day one harvests a cactus pad for consumption.

Cacti grow only slowly All the aforementioned adaptations to survive in a dry climate come at a cost. There has to be a trade off and that is a slow or very slow growth rate. (It may not appear so with the Indian fig. See Bibliography.) Without foliage leaves, the photosynthetic surface is restricted to the stem and thus is very small. This limits the primary productivity of the plant. While the strategy of closing up the stomata during the day and making use of CAM photosynthesis is great in reducing transpiration loss, there is energy cost in capturing carbon dioxide first as malic acid. Here, the overall photosynthesis efficiency is compromised. As a result, cacti grow only slowly. Figure 8. Three examples of showy cactus flowers. From top: Coast prickly-pear (Opuntia There are few studies on the growth littoralis) with a , barrel cactus () with more notable rate of cacti, perhaps because the separate stigmas, and Beavertail cactus measurements would take a lot longer (Opuntia basilaris).

8 than a typical research grant. A commonly cited example is the saguaro (Carnegiea gigantea) from the National Park Service. A saguaro grows between 1 and 1.5 inches per during its first eight . During its first year, the growth is even slower; a baby saguaro is about 3 mm (a bit above 1/10 inch) tall by its first birthday. The that bear stem arms are at least 50 to 70 years old.

Conservation challenges of cacti and succulents The slow cactus growth has also led to the demise of many cacti worldwide. In addition to habitat loss due to development and agriculture, some cacti and other succulent plants are threatened by people poaching them for gardening and home decor. The Coast barrel cactus, which grows extremely slowly, is one such victim. This cactus is not on the federal or California state endangered list but the California Native Plant Society (CNPS) considers the plant to be seriously threatened in the state (code 2B.1). Elsewhere, the poaching of the saguaro in the has gotten so severe that park rangers have been inserting identification microchips into the stem to deter criminal activities. With succulent plants, the Liveforever (or Dudleya) plants in the stonecrop family are prime targets for poachers to supply the hot Asian markets. In the last couple of years, the California State Fish and Wildlife officials have caught and indicted a good handful of poachers shipping thousands of plants to Korea and China. In TPSNR, the Short-leaved Dudleya (Dudleya brevifolia) is listed as a California state endangered species. This plant is not a target of poachers because it is tiny. However, by the same token, the plant can be trampled under foot easily by the unknowing public. Thus certain areas in the main Reserve and in the Extension have been fenced off to protect them.

Cactus flowers and reproduction Cactus flowers are notable for being big and showy—key features to compete for (Fig. 8). They attract and are pollinated by a host of pollinators. In addition to , they welcome hawk-, , and . The flowers are bisexual with pistil and . Figure 9. stages on an Indian fig (Opuntia ficus-indica). At the Beyond this, cactus flowers have several unique bottom is a developing pericarpel, at features. the top a developing flower bud, and in the middle a flower starting to The flowers have many and . The bloom. Note how the pericarpel is sepals are colored and shaped like the petals, so covered by glochids.

9 much so that (collection of sepals and petals) is the term used to describe cactus flowers. The flowers have numerous stamens, almost lawn-like surrounding a stocky style. Atop the style is a that is multi-lobed, indicative of a large number of fused carpels. The cactus fruit is a many-seeded . The stigma usually matures later than the anther, making it difficult for self-. The flowers of some cacti like the saguaro (Carnegiea gigantea) are self-incompatible. In some species, the motion of an insect within the flower causes stamens to bend inward to dust the insect with . Some sources consider the stamens to be thigmotactic. But it is hard to tell the difference when we see a bee scurry energetically through a mat. The of cactus flowers is inferior, meaning that it is located below the perianth and the stamens (Fig. 9). The bases of the stamens and the perianth are fused together. The pericarpel (containing the ovary and thus the fruit) appears as if it is a new growth from a stem (cladode). The colors of the stigma, anther and the perianth are usually in strong contrast, probably a visual cue for pollinators. For flowers with a vibrant perianth, the color can be due to pigments called instead of the more common . Betalains are responsible for the deep red color of beets (genus Beta) and bougainvillea flowers. Cacti are also very capable of asexual reproduction. Vegetative propagation is most notable with the opuntioids (locally Opuntia and Cylindropuntia). They can easily make a clone of themselves from a detached stem segment. Because the covering of the fruit is essentially stem tissue, some opuntioids can regrow from the fruits, but there is no report of this happening with the local chollas and prickly-pears.

Opuntias With about 200 species, Opuntia is the largest genus in Cactaceae. Their main characteristics is flattened cladodes that are joined edge to edge. Most of them have spines, but all of them have glochids. The glochids may not be noticeable on the Coast prickly-pear (Opuntia littoralis), but they are at the base of the spines and on the fruits. Because of the adaptability of , many of their species have been introduced outside of the Americas. The most notable is the Indian fig (Opuntia ficus-indica). This is a domesticated (or cultivated) crop—why it has no spines and the pads are thicker. It was cultivated for so long and widely that its exact origin is no longer known, but it is very probable that the plant resulted from the work of the in Central .11 There are over a hundred species of opuntias endemic to Mexico, and Opuntia species hybridize easily. The name of the pad, , is taken from a word for pads, and nopales

11 Side tidbit: Archaeological studies and genetic analyses have found that corn (maize, Spanish maíz, scientific Zea mays) was domesticated from the wild, ancestral teosinte as early as 8,700 years ago by the Mesoamericans.

10 are used in a good number of Mexican dishes. Spanish conquistadors introduced the Indian fig to near the beginning of the 16th century. The plant was introduced so long ago and naturalized so well throughout southern Mediterranean regions that the etymology of Opuntia is ascribed to Opus, an Ancient Greek city during the days of Pliny and .12 Regardless, the species name ficus-indica literally means fig from . To the early European explorers, they thought they had discovered the East Indies, and the fruit of this plant sort of reminded them of the fig. (The shapes of the fruits are not the same. Fig is native to the , but it was transplanted to Europe so long ago that it was even in the Roman diet.) Today, the Indian fig is farmed commercially in more than 20 countries, primarily for the fruit, which is also called the tuna. Why? For a ripe fruit, the pulp inside is so red that it reminds people of a bluefin tuna. The Kumeyaay did not farm the Indian fig. They harvested the fruits from the variety of prickly-pear species that grew in the region. They also devised many clever ways to get rid of the glochids, including making a tong out of Mojave yucca leaves to pick the fruit. They also ate the nopal, but it was not a major food staple. Another notable Opuntia is the Erect prickly-pear () native to tropical coastal areas of the Americas and the . The British imported the plant to in the 19th century in their attempt to establish their own cochineal (genus ) red dye industry. Nonetheless, they picked the wrong Opuntia and the species of Dactylopius. Even though the experiment failed, the prickly-pear invaded some 15,000 square miles of farmland. The Australian government finally put the prickly-pear under control by importing the Cactus from in the early 20th century. On the note of the wrong species of Dactylopius, the Aztecs used a domesticated variety of cochineal. (They called cochineal nocheztli, blood of the nopal.) The cactus that this insect grew on? Primarily the Indian fig.

Annotated Bibliography ● General information related to cactus

Greenfield, Amy Butler (2006). A Perfect Red: Empire, Espionage and the Quest for the Colour of Desire (Random House).

12 The naming of Opuntia might be a misunderstanding of time and that the plant was not native. Pliny the Elder wrote about some edible plant near Opus. Theophrastus wrote about some spiny plants. But both of them lived well over a thousand years before Columbus. Many people considered Pliny indeed saw a cactus-like plant because it was written by Umberto Quattrocchi in his authoritative World Dictionary of Plant Names.

11 – An excellent historical account of the history of cochineal, including the domesticated insect and cactus.

Mauseth, James D. (2006). Structure–Function Relationships in Highly Modified Shoots of Cactaceae. Annals of Botany 98, 901–926. – A very detailed, invited review. Excellent images.

Morhardt, S. & Morhardt, E. (2004). California Desert Flowers: An Introduction to Families, Genera, and Species (University of California Press). – Has a short chapter on Cactaceae.

Rebman, Jon P. & Pinkava, Donald J. (2001). Opuntia Cacti of —An Overview, Entomologist 84, 474-493. – A review covering the morphology, adaptation, and reproduction of the opuntias.

Wilken-Robertson, Michael (2017). Kumeyaay Ethnobotany: Shared Heritage of the , pp. 159-161 (Sunbelt Publications). – On the ingenious ways that the Kumeyaay harvested and processed prickly-pear fruits. Wilken wrote that the Kumeyaay did not use the nopal as a major food source, but they did eat them. It was mentioned in Delfina Cuero’s autobiography.

● Related to growth rates

Bowers, Janice E. (1996). Growth Rate and Life Span of a Prickly Pear Cactus, , in the Northern Sonoran Desert. The Southwestern Naturalist 41, 315-318. – Bowers measured the growth rate by the number of cladodes. For Engelmann's prickly-pear, a ten-year-old plant has as few as 3 cladodes (up to about 6), but by 20-year-old, it has a bit over 100 cladodes (growth is not linear). On average, 20% of the cladodes initiated each year can be lost to abortion or predation (maybe why the young plants grow so slowly). The smallest plants capable of flowering has 6 to 13 cladodes, representing a range in ages from about 9 to 11 years— so a young plant allocates its resources to vegetative growth. de Cortazar, V. G. & Nobel, P. S. (1992). Biomass and Fruit Production for the Prickly Pear Cactus, Opuntia ficus-indica. Journal of the American Society for Horticultural Science 117, 558– 562. – An agricultural study of the Indian fig.

Drezner, T. D. & Lazarus, B. L. (2008). The Population Dynamics of Columnar and Other Cacti: A Review. Geography Compass 2, 1–29. – A review that covers columnar cacti especially the saguaro, and the impact of human activities. Also covers the history of the Indian fig a little bit.

Snyman, Hennie A. (2013). Growth Rate and Water-Use Efficiency of Cactus Pears Opuntia ficus- indica and O. robusta. Arid Land Research and Management 27, 337-348. – A study of two Opuntia introduced to South at least 250 years ago. Measured that the water content of the cladodes as around 88%. In one growing season, the growth of mean fresh mass of O. ficus-indica is about 1.3 kg per cladode. Eyeballing one of its charts (omitting all the technical details), one young O. ficus-indica plant can produce easily 2 kg of dry mass per year. Consider that as 12% weight of the plant, it makes over 16.5 kg fresh cladodes (over 36 lbs). These plants have a very high water-use efficiency. And for a cactus, O. ficus-indica grows

12 extremely fast.

National Park Service (2015, September 11). Saguaro Cactus Growth. Retrieved April 20, 2019, from https://www.nps.gov/articles/saguaro-cactus.htm – Information on the growth rate of saguaro.

● Related to extrafloral nectar food-for-protection mutualism

Aranda-Rickert, Adriana, Diez, Patricia & Marazzi, Brigitte (2014). Extrafloral nectar fuels ant life in deserts. AoB PLANTS 6, article plu068. – A detailed study of extrafloral nectary-bearing plants and relationships in a seasonal desert of northwestern . Has a good introduction with photos on different extrafloral-nectar secreting structures.

LeVan, Katherine E., Hung, Keng-Lou James, McCann, Kyle R.,Ludka, John T., & Holway, David A. (2014). Floral visitation by the Argentine ant reduces pollinator visitation and set in the coast barrel cactus, Ferocactus viridescens. Oecologia 174, 163–171. – By being aggressive, the invasive Argentine ant (Linepithema humile) is more effective in fencing off insect herbivores, but they also drive away native ant species. Areas not invaded by the Argentine ant have 18 native ant species visiting the Coast barrel cactus. The muted mutualist diversity lowers seed mass production of the cactus.

Ludka, John T., LeVan, Katherine E. & Holway, David A. (2015). Infiltration of a facultative ant– plant mutualism by the introduced Argentine ant: effects on mutualist diversity and mutualism benefits. Ecological Entomology 40, 437–443. – The presence of the invasive Argentine ant has a negative effect on floral visitation by pollinators of the Coast barrel cactus.

● News on the poaching problems

California Department of Fish and Wildlife (2018, April 6). CDFW Wildlife Officers Arrest Three for Poaching Succulents in Humboldt County. Retrieved April 20, 2019, from https://cdfgnews.wordpress.com/2018/04/06/cdfw-wildlife-officers-arrest-three-for-poaching- succulents-in-humboldt-county/ – News from the California F&W. The F&W officers arrested two Koreans and one Chinese for poaching over 2,300 Dudleya plants in Humboldt County. The overseas market value of the plants is between $40 to $50 per plant.

Carson, Erin (2018, August 29). National parks want you to stop picking them clean. Retrieved April 20, 2019, from https://www.cnet.com/news/national-parks-want-you-to-stop-picking-them- clean/ – News from cnet.com. On all the poaching problems at Saguaro National Park. The average black market value for a saguaro is $100 a foot, plus another $50 to $100 for each arm.

Goodyear, Dana (2019, February 20). Succulent-Smugglers Descend on California. Retrieved April 20, 2019, from https://www.newyorker.com/news/california-chronicles/succulent-smugglers- descend-on-california – Article from The New Yorker. Two poachers pleaded no contest to felony charges for their removal of more than eighteen hundred Powdery Liveforever (Dudleya farinosa) from Garrapata

13 State Park, in Big Sur. Goodyear touched on how succulents might have become so popular.

McCormick, Erin (2018, April 27). Stolen succulents: California hipster plants at center of smuggling crisis . Retrieved April 20, 2019, from https://www.theguardian.com/environment/2018/apr/27/stolen-succulents-california-hipster- plants-at-center-of-smuggling-crisis – News from The Guardian. On the extensive poaching and smuggling of Dudleya plants from California because of demands in China and Korea.

McGivney, Annette (2019, February 20). 'Yanked from the ground': cactus theft is ravaging the American desert. Retrieved April 20, 2019, from https://www.theguardian.com/environment/2019/ feb/20/to-catch-a-cactus-thief-national-parks-fight-a-thorny-problem – News from The Guardian. On the extensive poaching of cacti in the Southwestern . To fight the poachers, rangers in Saguaro National Park have begun to embed microchips into the plants.

Smith, Sylvia (2018, September 15). Prickly cactus species 'under threat'. Retrieved April 20, 2019, from https://www.bbc.com/news/science-environment-45438733 – News from BBC News. On the plight of cacti, which includes poaching. Interestingly Smith considers that Prickly-pear (very likely meaning Indian fig) is being devastated by cochineal in southern .

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