Plant-animal interactions in deserts
Abstract and Keywords
Desert animals and plants interact in ways that have strongly influenced their respective evolutionary trajectories. This chapter begins with herbivory because of its widespread impacts, many of which are presumed to be negative. It then moves on to some other important aspects of desert plant—animal interactions, with a focus on pollination and seed dispersal. Of the various forms of pollination, the chapter will explore the yucca moth-yucca and senita moth-senita cactus mutualisms. With regard to the role of animals in seed predation and seed dispersal, it will consider the effects of small mammals and ants on seed abundance, and the role of large mammals in dispersing the seeds of keystone Acacia species. This selection of examples illustrates how the relatively simple nature of the desert environment has given biologists unique insights into the importance of plant—animal interactions for ecosystem function.
It is widely believed that abiotic factors have greater influence than biotic factors in determining the biodiversity of arid ecosystems. Nonetheless, desert animals and plants interact in ways which have strongly influenced their respective evolutionary trajectories. This chapter begins with herbivory because of its widespread impacts, many of which are presumed to be negative. It then moves on to some other important aspects of desert plant-animal interactions, with a focus on pollination and seed dispersal. Of the various forms of pollination, the chapter will explore the yucca moth-yucca and senita moth-senita cactus mutualisms. With regard to the role of animals in seed predation and seed dispersal, it will consider effects of small mammals and ants on seed abundance, and the role of large mammals in dispersing the seeds of keystone Acacia species (Milton et al. 1999; Munzbergova and Ward 2002). This selection of examples illustrates how the relatively simple nature of the desert environment has given biologists unique insights into the importance of plant-animal inter actions for ecosystem function.
It has been argued that herbivory by mammals does not contribute significantly to arid ecosystem functioning and biodiversity maintenance (reviewed by Noy-Meir 1973). Instead, abiotic factors such as high temporal and spatial variation in rainfall are suggested to be the most important factors for the ecology of arid ecosystems. There is a strong negative correlation between the coefficient of variation in mean annual rainfall among years and median annual rainfall of arid regions, which results in high variability in the germination of annual plants and high variability in the growth of perennial plants (Ward 2001, 2005a). Similarly, spatial (p.146) variation in rainfall is high and is not correlated with distance among sampling points (Ward et al. 2000a, 2004). This variability in rainfall results in high spatio-temporal variability in plant abundance and availability to herbivores. Ward et al. (2000a) showed that, in the Negev Desert of Israel, only 1% of plant species were present in permanent plots in all years and approximately half the plant species were found only once in 10 years (Fig. 7.1).
Temporal variation in plant species richness can also be quite large; note the relationship between the coefficient of variation in plant species richness and total plant species richness (Fig. 7.2). This relationship is an envelope effect in that there is more variability when the total number of species is small (because there may be various reasons (such as edaphic variability) why total species numbers are limited) and it decreases as species richness increases, probably being limited by precipitation (Fig. 7.2).
Further contributing to spatial variation, in some arid regions, is the pattern of ‘contracted vegetation (sensu Whittaker 1975) (Fig. 9.1), whereby plants are almost entirely restricted to ephemeral watercourses. Another confounding factor is that geological substrates vary considerably (p.147) among arid regions, particularly in their nutrient status and water retention capacities (Landsberg et al. 1999a; Ward 2005a). Patchy nutrients and water availability lead to considerable differences in plant composition and nutritional quality among habitats (Stafford Smith and Morton 1990; Ward and Olsvig-Whittaker 1993; Ward et al. 1993; Ward 2005a). The high spatio-temporal variability in the availability of plants to herbivores necessarily limits the numbers of herbivores that can be sustained in arid ecosystems, which is considered to limit their impacts on plant resources.
Milchunas et al. (1988) predicted that a long evolutionary history of grazing results in the selection for regrowth following herbivory and for prostrate growth forms. In such communities, grazing causes rapid shifts between suites of species adapted to either grazing avoidance/tolerance or competition. In their global review, Milchunas and Lauenroth (1993) showed convincingly that evolutionary history of grazing had an effect on grazing responses inside and outside herbivore exclosures in North and South America (Fig. 7.3). What does this mean? Milchunas and Lauenroth (1993) infer that species that are highly palatable have been removed from the vegetation in areas with a long evolutionary history of grazing and only non-palatable species remain. Thus, there is no clear effect of grazing on changes in plant species composition. A possible reason for this is the Narcissus effect (sensu Colwell and Winkler 1984), which means that selection in the past has resulted in the extinction of all non-resistant/ tolerant genotypes. Thus, all extant species are similarly resistant to herbivores, resulting in an absence of an effect of current herbivory on plant diversity (Ward and Olsvig-Whittaker 1993; Perevolotsky and Seligman 1998). Presumably, in such ecosystems, conditions seldom favour growth-dominated genotypes. Thus, only one (resistant/tolerant) genotype exists in these populations. Interestingly, re-examination of the same data for (p.148) Africa and Asia (Ward 2005a) shows no such effect, and indicates that grazing responses are positively correlated with mean annual rainfall in those studies (Fig. 7.3).
7.1.1 Grazing effects on species composition
Major differences between the effects of herbivores and carnivores on their food items are that herbivores seldom eat the entire food item and plants differ considerably in their quality. Plants can be of low quality because they contain low levels of energy and protein, have high levels of fibre, have high levels of defence compounds and may have lots of mechanical defences (thorns). Herbivores can alter plant community composition by selecting dominant species, causing rare species to become more common or by selecting rare species, increasing degree of dominance. However, this process usually does not affect diversity. Chesson (2000) developed a lottery model to explain how herbivores might affect plant diversity. In plant communities, spaces periodically become available when an inhabitant dies. Any species that has propagules ready at that time and place can occupy the space. This model makes the assumption that all plant species can increase when rare. Herbivores can increase the number of coexisting species by eliminating individuals of certain species, thereby freeing up space for other species that take their place opportunistically. If plants are avoided when rare, then the lottery model can explain coexistence of more species under herbivory (Fig. 5.1).
7.1.2 Long-term studies of the effects of large mammals on arid vegetation
What do field-based studies of the effects of herbivory by large mammals tell us about the effects of large mammals on vegetation of arid zones? Longer-term studies need to be considered when assessing the impact of herbivory in arid-zone vegetation because short-term studies might only show us the relatively trivial effects of differences in biomass consumption and show little in terms of changes in species composition. Although the list below is not intended to be exhaustive, such studies show inconsistent patterns in the response of arid vegetation to mammalian herbivory:
1. Goldberg and Turner (1986) analysed vegetation changes in nine permanent 100 m2 plots first established in 1906 near Tucson, Arizona, USA (mean annual rainfall = 250 mm). These plots were fenced to exclude large herbivores in 1906 and were examined periodically until 1978. There were no consistent, directional changes in vegetation composition between 1906 and 1978, despite large fluctuations in absolute cover and density of the species. For most species, and in most plots, the changes in absolute cover and density appear to have been a response to sequences of either exceptionally wet years or exceptionally dry years. Only two species, Krameria grayi and Janusia gracilis, appeared (p.149) to increase over the study period—the former species is reported to be very palatable to livestock. A study comparing vegetation inside and outside the above-mentioned fenced areas following 50 years of protection showed that the total plant density was significantly higher within the fenced areas but there were no large differences in the composition of the vegetation (Blydenstein et al. 1957). As indicated above by Chesson (2000), it is changes in vegetation composition that are required to demonstrate changes in effects of herbivory rather than changes in biomass alone.
2. Ward et al. (1998, 2000a) and Saltz et al. (1999) examined the effects of reintroduced Asiatic wild asses, Equus hemionus onager (also called onagers or kulans), in 11 pairs of permanent plots in the central Negev desert of Israel (mean annual rainfall = 56 mm) from 1992 to 1997. There has been considerable concern that the reintroduction of such a large equid (~200 kg) would cause habitat degradation through heavy grazing because large, hindgut fermenters are dependent on processing large quantities of low-quality forage. They found that fenced plots (i.e. wild asses excluded) had significantly higher plant cover than unfenced plots when differences in rainfall among plots were accounted for, although there were no significant differences in plant species richness, diversity or dominance between fenced and unfenced plots. Three plant species showed significant increases in percentage cover in the fenced plots, and one species significantly increased in cover in the unfenced plots. Eight plant species invaded the fenced plots, three species invaded the unfenced plots, and one species disappeared from the unfenced plots during the study. Unfenced plots showed a directional change away from their original species composition (although plant species richness and diversity remained the same) while vegetation in fenced plots did not change over the period (Fig. 7.4a-c) (Ward et al. 2000a). These results indicate that herbivory by wild asses is causing a change in the relative abundance of certain species (unfenced plots) and that competitive effects in the protected plots have occurred when plants are protected from grazing.
3. Ward and Saltz (1994), Ward et al. (1997, 2000a), Saltz and Ward (2000), and Ruiz et al. (2001, 2002) studied the interactions between the dorcas gazelle, Gazella dorcas, and the desert lily, Pancratium sickenbergeri, in sand dunes in the central Negev desert from 1990 to 2002. Gazelles dig in the sand to remove all or part of the bulbs of the lilies during the dry summer months, while in the winter months they consume the leaves. There are no leaves on the sand surface during the summer. From October-December they consume virtually all flowers when available-flowers have a 1:30,000 chance of surviving (Saltz and Ward 2000). They found that the gazelles entirely consume about 5% of the plants per annum, but may eat part of up to 60% of plants each year. Lily populations enclosed in 1994 (15 m X 15 m enclosures) now have about twice as many plants as populations outside the enclosures (478 vs. 255 plants per plot), indicating a significant negative impact of herbivory.
7.1.3 Effects of herbivory on relationships among plant functional types
Some of the most interesting effects of herbivory on plant diversity are through the effects of selective herbivory on the relationships among plant functional types (Noy-Meir et al. 1989; Westoby 1989, 1999). Arid regions that experience summer rainfall are usually grass-dominated (e.g. Namib (p.151) and Kalahari deserts, southern Sahara, Australia), while deserts with winter rainfall (e.g. Negev, Sonoran, and central Asian deserts) are usually dominated by asteraceous and other dicotyledonous annual plants (Louw and Seely 1982; Shmida and Darom 1986). More conventionally, the most important changes in vegetation in response to herbivory occur in the relative abundance of tall and short annual and perennial plants (Noy-Meir et al. 1989; Ward 2005a).
The ‘classical’ theory of Dyksterhuis (1949) postulates that the main effect of grazers is through differential removal of plant parts among plant species which shifts the balance of relative species abundances. This is established in the ungrazed (‘climax’) state, mainly by competition for water, light, and nutrients, to a new stable balance, which depends on differential defoliation and regrowth. The relative abundance of some plants in a community decreases consistently in response to increased grazing intensity (‘decreasers’), while that of others increases consistently (‘increasers’), and some species only appear above a certain threshold of grazing intensity (‘invaders’). Decreasers are plants with attributes that favour them in competition for space and other resources but disadvantage them under differential defoliation. Such attributes include erect tall shoots with elevated renewal buds, long growing season, and perennial life cycles, and readily palatable and available to grazers (especially grasses and legumes) (Noy-Meir et al. 1989; Westoby 1989). Increasers (and invaders) are plants with at least some of the converse attributes: low or prostrate shoots with renewal buds close to or below ground, short growing season, annual or short perennial life cycle, and lower palat-ability to grazers due to chemical or morphological ‘defensive’ characters (especially forbs (non-legume dicots)).
The responses of many species in arid zones appear to be consistent with a modified version of the ‘classical’ theory of grazing response, with its basic mechanism being a balance between competition and differential defoliation. Noy-Meir et al. (1989) and others (Diaz et al. 2001; Vesk et al. 2004; Ward 2006) have shown that height decreases under increased grazing pressure because tall species receive most grazing pressure, perennials decrease because they are more available to herbivores, leaf size decreases because larger leaves provide larger bites for grazers, and high specific leaf area (SLA) species (which have thin, soft leaves) may be favoured by selective grazers (Vesk et al. 2004). Westoby (1999) found that, under intense, non-selective grazing, all species are grazed and high-SLA species may have an advantage because they have faster regrowth, which is due to quicker leaf turnover and a greater rate of regrowth per unit of carbon invested in leaf tissue (see also Vesk et al. 2004).
In Australia, Landsberg et al. (1999a) have shown that ‘large erect tussocks branching above-ground’ and ‘small, sprawling basal tussocks’ may potentially be recognized as functional grass types that are reliable indicators of light and heavy grazing, respectively. Heavy grazing (p.152) is associated with an increased abundance of herbaceous forbs, many of which are facultative annuals in Australia. This trend is consistent with other studies that have shown increases in annual plants with heavy grazing (Noy-Meir et al. 1989; Friedel et al. 1990). The tendency towards a decrease in the relative abundance of grasses at heavily grazed sites has also been seen in other studies (James et al. 1999; Landsberg et al. 1999b). However, Landsberg et al. (1999a) note the general absence of clear patterns and pointed to the complexity of grazing effects (such as strength of selection, degree of defoliation, and variance in recruitment opportunities) and lack of evolutionary history of grazing by large mammalian herbivores in Australia as reasons for weak selective pressure for grazing-related traits (Landsberg et al. 1999a).
Contrary to the observations in Australia mentioned above, in arid Tunisian rangelands (mean annual rainfall = 100–200 mm), Jauffret and Lavorel (2003) found no decrease in the abundance of perennial grasses. This result is also in contrast with the observations in more mesic systems (Noy-Meir et al. 1989; Skarpe 1990; McIntyre and Lavorel 2001). Jauffret and Lavorel (2003) account for this due to the near or complete elimination of perennial grasses (e.g. Pennisetum elatum and Hyparrhenia hirta) and ascribed this to thousands of years of heavy grazing. This heavy grazing has left Tunisian ecosystems with a homogenized flora consisting only of species that are highly tolerant of herbivory and other forms of disturbance. Very similar results were obtained by Milchunas and Lauenroth (1993), as mentioned above.
A relative increase in woody shrubs has often been recorded in semi-arid rangelands, especially when these have a short- or light-grazing history (Archer et al. 1988; Pickup and Stafford Smith 1993; Skarpe 2000; Ward et al. 2004; Ward 2005b; Kraaij and Ward 2006). Chamaephytes (shrubs with below-ground growth structures) can resist intense or frequent disturbances by growing less tall and resprouting, and they tend to be less palatable than most grasses. The Tunisian system has apparently reached the stage where chamaephytes are the only life form remaining at abundances high enough to observe a significant response in terms of abundance and quality (also true in the Negev desert in Israel; Ward and Olsvig-Whittaker (1993)).
It has been reported in many arid ecosystems that annual species replace perennials following heavy grazing, owing to their ability to quickly invade open spaces and utilize soil resources (Kelly and Walker 1977; Cheal 1993; Freeman and Emlen 1995). Perennials are always present and thus are permanently available to browsers. The transient nature of the annual lifestyle means that herbivores are less likely to encounter them and, thus, they increase in abundance while perennials decrease with grazing. However, in a study of permanent plots from 1989 to 1996 in Namaqualand, South Africa (mean annual rainfall = 76 mm), Milton and Dean (2000) found that the reduction of perennial grasses by cattle grazing favoured annual (p.153) plants in wet years only. Dry conditions prohibited the establishment of annual plants regardless of whether perennial grasses were present or not. This pattern has also been reported by Van Rooyen et al. (1991) and Jeltsch et al. (1997) in the Kalahari desert, South Africa. Similarly, in a long-term study in a Chihuahuan desert site in southeastern Arizona (North America), Kelt and Valone (1995) found that the removal of herbivores (cattle) had little impact on the abundance and diversity of annual plants. Historical effects of herbivory may cloud our ability to detect differences in the effects of herbivory on perennial and annual plants.
Palatability was a major factor for determining the plant selection by herbivores in arid rangelands, according to the observations of Jauffret and Lavorel (2003) in Tunisia, Ward et al. (2000a) in Israel and Landsberg et al. (1999a) in Australia. Spiny plants were more frequent among grazing increasers in Tunisia. However, other studies have shown that spiny species such as Echinops polyceras and Acacia raddiana are favoured food plants of wild asses and camels, respectively (Rohner and Ward 1997; Ward et al. 1998). Some examples of reduced palatability are pertinent here:
1. Milton (1991) has shown that spinescence in plants increases with aridity, soil fertility, and mammalian herbivory at regional and local scales in the arid Karoo of southern Africa. Vegetation of moist, nutrient-rich habitats within arid areas was more spinescent than that of the surrounding dry plains. Spinescence in plants of drainage lines and pans in arid southern Africa occurs in a wide range of genera and appears to have been selected by the effect of large mammals which concentrate on these moist patches. Milton (1991) concluded that, in arid areas, moisture may be important in mediating mammalian selection of spinescence.
2. Rohner and Ward (1997) have shown that there are inducible defences in A. raddiana trees in the Negev desert of Israel because they only invest in a change of strategy when there is herbivory. In plants that are eaten, there are higher levels of condensed tannins in plants, leaves are smaller, and thorns longer (Fig. 7.5). Essentially, the thorns are hiding small leaves. Having small leaves is not a constraint because light levels are very high in deserts. However, in the absence of herbivory, larger leaves are the default condition because plants can grow faster when their light-capturing surfaces are larger. Ward et al. (2000a) and Jauffret and Lavorel (2003), among others, have shown that palatability (or lack thereof) may play an important role in determining the effects of mammalian herbivory on arid ecosystems. Jauffret and Lavorel (2003) consider the fact that long-spined species such as Astragalus armatus and toxic and highly fibrous species (such as Thymelaea hirsuta) are dominant in arid Tunisian rangelands a consequence of the long grazing history. Similarly, unpalatable shrubs such as Hammada scoparia, T. hirsuta, and Anabasis articulata are often dominant in heavily (p.154) grazed arid regions of the Middle East (Ward et al. 2000b; Ward 2005a). Geophytes, such as Urginea maritima, are also widespread and abundant in the Middle East, particularly where there is heavy grazing and trampling (Hadar et al. 1999). Similar to prostrate and rosette plants, they are close to or under the ground and unavailable to grazers for much of the year. When they produce leaves in the winter months, they are largely untouched by grazers because of the defensive chemicals in the leaves (Ward et al. 1997). Furthermore, the short reproductive period of geophytes enables early flowering, seed setting, and dispersal despite heavy grazing (Hadar et al. 1999).
7.1.4 Is Australia a special case?—a meta-analysis
Vesk et al. (2004) performed a meta-analysis of 11 lists of grazing responses from five published Australian semi-arid and arid shrubland and woodland studies in an attempt to assess the generality of the results of the Diaz et al. (2001) study mentioned above. They found that the traits shown to predict grazing responses in the Argentinian and Israeli studies did not adequately explain responses in Australian semi-arid and arid rangelands. They found no effects of plant height or leaf size on grazing. Annuals were no less likely than perennials to decrease with increased grazing pressure (see also Milton and Dean 2000). Analyses of traits within growth forms provided little evidence for relationships between traits and responses other than that annual grasses, which have high specific leaf area, tend to be increasers. Vesk et al. (2004) believe that because the Australian range-lands have lower productivity, less continuous sward, higher growth form diversity, and more bare ground than ecosystems in the Diaz et al. (2001) study, grazers can move through vegetation and taller species do not necessarily receive more grazing pressure because grazers can access short (p.155) species from the side rather than by grazing the sward down to them. In contrast with Vesk et al.’s (2004) general conclusions, an earlier study of two arid Australian shrublands (which was included in the meta-analysis of Vesk et al. (2004)) found associations between increased grazing pressure and small plant size, small leaves, high fecundity and plasticity of growth form (Landsberg et al. 1999a). However, many attributes of plants recorded in the Landsberg et al. (1999a) study varied independently of each other and grazing-related attributes were only convincingly demonstrated in grasses. Vesk et al. (2004) recognized that they could not discount evolutionary history of grazing or the ‘Australia is a “special case” argument’ for the differences between their results and those of Diaz et al. (2001).
7.1.5 Effects of insect herbivory on desert plants
It has been claimed by Crawley (1989) that plants have more impact on the population dynamics of insects than insects have on the population dynamics of plants. In general, it is probably true that monophagous desert insects have little impact on equilibrium plant abundance even when the insects are food-limited (Crawley 1983). However, several studies have suggested that herbivorous insects have a great impact on the evolution and population dynamics of desert plants (Ayal and Izhaki 1993; Ayal 1994; Becerra 1994; Wilby et al. 2005). Herbivorous insects may reduce the reproductive success of their host plants either by directly feeding on their flowers (Ayal and Izhaki 1993; Ayal 1994) and seeds (Wilby et al. 2001; Or and Ward 2003) or by indirectly feeding on other plant parts such as foliage and roots (Becerra and Venable 1990; Becerra 1994).
Two examples where insects have notable interactions (one direct and one indirect) with desert plants are as follows:
1. Ayal and Izhaki (1993) and Ayal (1994) have studied the mirid bug, Capsodes infuscatus (Hemiptera: Miridae), in a central Negev desert habitat in Israel. This bug deposits eggs inside the inflorescence stalk of its host plant Asphodelus ramosus (Fig. 7.6) in spring. Developing nymphs as well as adults feed on this plant. Different structures of A. ramosus are consumed by the bugs, including leaves, flower stalks, buds, flowers, and fruits (Ayal and Izhaki 1993). C. infuscatus nymph feeding may kill young inflorescences, or suppress the development of the inflorescence branches and kill all its flowers while adult feeding may also kill green fruits (Ayal 1994). All stages of C. infuscatus feed upon A. ramosus. Nymphs consume leaves early in the season, but as they develop, they feed on inflorescence stalks, flowers, and fruits (Ayal and Izhaki 1993). A positive correlation between the number of young nymphs of C. infuscatus per clone (A. ramosus also reproduces vegetatively) early in the season, long before fruit appearance, and consequent damage to fruit production in A. ramosus has been shown (Ayal and Izhaki 1993).
2. One example of an interesting chemical interaction in desert ecosystems is between a tree (Family: Burseraceae) and a leaf beetle (Family: Chrysomelidae). A desert tree from Tehuacan desert near Zapotitlan, Mexico, Bursera schlechtendalii, has resinous ducts in its leaves that eject an unpleasant syringe-like squirt of terpene resins, from 5 to 150 cm and may persist for a few seconds (Fig. 7.7). Some leaves do not actually squirt liquid into the air but still release large amounts of terpenes that cover the surface of the leaf (called the ‘rapid bath response’ by Becerra and Venable (1990)). The leaf beetle Blepharida sp. nov. is capable of severing the resin canals by biting the midvein of the leaf (Becerra 1994). Becerra (1994) determined the reaction of larvae to Bursera resins by allowing them to incise the leaf midveins and then moving them to intact leaves. Canals were intact in the new leaves, leaving the beetle larvae with a squirt of resins. They attempted to clean themselves and then abandoned the leaf. The larvae may even remain inactive for several hours before starting to incise another leaf. Thus, resin flow can deter this beetle if canals are not deactivated (Becerra and Venable 1990). Larvae living on plants with a higher frequency of leaf response had greater mortality or, in some cases, were smaller. Early instar larvae are incapable of severing leaf veins because of their smaller mandibles. They feed by mining the surfaces of the leaves but sometimes die when they rupture the resin canals (Becerra 1994).
Interestingly, larvae from low-response plants increased their vein-cutting time when transplanted to high-response plants. When placed on high-response plants, some larvae fed without cutting the veins and were covered with resins. After getting squirted by several leaves, they started to sever the leaves. Larvae from high-response plants continued cutting veins after (p.157) being deposited on less responsive plants although they did so for a shorter time. These differences in behaviour based on their experiences on previous plants indicate that the behaviour is plastic and that Blepharida pays a handling-time cost. Becerra and Venable (1990) showed that Blepharida larvae can take up to 1.5 h to deactivate the resin canals of a single leaf of a high-response plant yet consuming the leaf thereafter can take 10–20 min only.
3. Interspecific facultative mutualisms typically involve guilds of interacting species. Within such a guild, species may differ in their abilities to reciprocate with a particular host. For plants that secrete extrafloral nectar, visitation by a single ant species may optimize the anti-herbivore benefits that the plant may derive; ants can be very effective in biting other animals, especially mammals, that attack a plant. Ants, for their part, gain from the extrafloral nectar provided by the host plant. Multiple ant species that vary in anti-herbivore abilities may result in reduced benefits, relative to an exclusive association with a high-quality mutualist.
How do facultative ant-plant mutualisms persist? Given that extrafloral nectar is costly to produce, how do plants avoid the problem of diminishing returns as partner diversity increases? Miller (2007) tested the prediction that association with two ant partners (Crematogaster opuntiae and Liometopum apiculatum) weakens benefits to the extrafloral nectar-producing tree cholla cactus (Opuntia imbricata). He found that only one ant (L. apiculatum) provided protection against herbivores and seed predators. However, this species is associated with cacti more frequently than Crematogaster. Liometopum showed greater constancy on plants they occupied, and they more frequently colonized vacant plants of the tree cholla cactus. Furthermore, Liometopum replaced but were never replaced (p.158) by Crematogaster. Liometopum was more abundant on reproductive plants and showed greater overlap with cactus enemies. Nonetheless, Miller (2007) showed that simulations of cactus lifetime reproductive output indicated that the associations with high- and low-quality mutualists did not reduce plant benefits relative to an exclusive L. apiculatum-O. imbricata association.
The most frequent type of mutualism is plant-pollinator interactions (Fig. 7.8). Facultative mutualisms allow for co-pollination, whereas obligate mutualisms involve the complete interdependency of both partners, the best-known example being the fig-fig wasp system (Bronstein 2001). The interactions between yuccas and yucca moths and senita cactus and senita moths are obligate mutualists that naturally occur in deserts.
Waser et al. (1996) expect plant generalization (i.e. more than one pollinator per plant species) to occur as long as temporal and spatial variance in pollinator quality is appreciable, different pollinator species do not fluctuate in unison, and they are similar in their pollination effectiveness. Further, they consider pollinator generalization likely to occur when floral rewards are similar across plant species, travel is costly, constraints of behaviour and morphology are minor, and/or pollinator lifespan is long relative to flowering of individual plant species. Nevertheless, plants with highly specialized pollination systems are not uncommon in the tropics and some temperate regions (review by Johnson and Steiner 2000).
(p.159) One of the more interesting examples of pollinator specialization and diversification occurs in the guild of bees that pollinate the creosote bush Larrea tridentata. In this case, the historical biogeography (20,000 years BP to the present) of this desert plant is well understood (Minckley et al. 2000). This history, coupled with the distribution pattern of its bee fauna, suggests that the specialization for creosote bush pollen has evolved repeatedly among bees in the Lower Sonoran and Mojave deserts. In these highly xeric environments, species of specialist bees surpass generalist bees in diversity, biomass, and abundance (Minckley et al. 2000). These specialist bees can facultatively remain in diapause through resource-poor years and later emerge synchronously when their host plants bloom in resource-rich years. Repeated origins of pollen specialization to one host plant where flowering occurs least predictably is a counterexample to Waser et al.’s (1996) proposition. Host-plant synchronization, perhaps a paucity of alternative floral hosts, or even the flowering attributes of creosote bush or a combination of these factors may account for the diversity of bee specialists that depend on L. tridentata.
7.2.1 Yucca-yucca moth mutualism
Yucca plants (genus Yucca) and yucca moths (genera Tegeticula and Parategeticula; Lepidoptera, Family: Prodoxidae) are highly coevolved. Particular species of moth have evolved with particular species of yucca. The pollinator of the yucca is always female. While at the flower, the moth climbs halfway up the pistil and inserts her ovipositor into the ovary of the plant (Fig. 7.9). The moth’h eggs are laid into the plant’t ovary. She then climbs up to the top of the pistil and rubs some of her collected pollen onto the stigma of the plant, fertilizing the flower, and thereby ensuring the production of seeds (Miller 1995). As the larvae develop, they feed on the developing seeds of the yucca, but they only eat a portion of them. What is different about this relationship is that there is no immediate reward for the individual insect following the pollination process (Pellmyr 2003). In more conventional plant-pollinator interactions, the pollinator will be rewarded with nectar and pollen, which happens to fertilize the next plant visited. Here, the yucca moth collects pollen, although she does not eat it. Pellmyr’r (2003) theory about the costs of seed production and the natural selection of Tegeticula and Parategeticula moths holds that if the moths lay a greater number of eggs, then the plant would suffer because of the moth’h reproductive success (i.e. the larvae would eat almost all the fertilized seeds of the plant). Evolutionarily speaking, moths that lay too many eggs and, thus, minimize the production of the developing seeds are disadvantaged because the flower in question aborts the developing fruit and the larvae relying on it starve. This keeps the moth/yucca equilibrium stable, so the fitness increases in one species do not affect those of the other.
(p.160) When two organisms have evolved to a point where both benefit from the relationship and neither is harmed, mutualism occurs. Coevolution of stable mutualism occurs because both species have mechanisms to prevent excessive exploitation. For example, yucca flower abortion occurs if too many eggs are laid (Pellmyr and Huth 1994). A strong negative effect exists between moth egg number and probability of flower retention in yuccas. Furthermore, they showed a strong positive effect between the number of pollinations received and the probability of flower retention. Selective maturation of fruit with low egg loads and high pollen loads provides a mechanism to increase the quantity and possibly the quality of seeds produced, and simultaneously select against moths that lay many eggs per flower or provide low-quality pollinations. These results explain the stability of this type of interaction, and explain why selection for high-quality pollination also provides a mechanism to help explain the evolution of active pollination among yucca moths.
Is there also a genetic cost through selfish moth behaviour that may lead to high levels of self fertilization in the yuccas? Observations of a Tegeticula yuccasella yucca moth on Yucca filamentosa revealed that females remained (p.161) on the plant and oviposited in 66% of all instances after observed pollen collections, and 51% of all moths were observed to pollinate the same plant as well (Pellmyr et al. 1997). Manual cross-pollination and self-pollination showed equal development and retention of fruits. Subsequent trials to assess inbreeding depression revealed significant negative effects on seed weight and germination frequency in selfed progeny arrays. Cumulative inbreeding depression was about 0.48 (i.e. the fitness of selfed seeds was less than half that of outcrossed seeds; Pellmyr (1996)). Estimates of outcrossing rates based on allozyme analyses of open-pollinated progeny arrays did not differ from 1.0; thus, outcrossing was the mode of reproduction. The discrepancy between high levels of behavioural self-pollination by the moths and nearly complete outcrossing in mature seeds can be explained through selective foreign pollen use by the females, or, more likely, pollen competition or selective abortion of self-pollinated flowers during early stages of fruit development. Thus, whenever the proportion of pollinated flowers exceeds the proportion that can be matured to ripe fruit based on resource availability, the potential detrimental genetic effects imposed through self-fertilized pollinations can be avoided in the plants. Because self-pollinated flowers have a lower probability of retention, selection should act on female moths to move among plants whenever moth density is high enough to trigger abortion.
Yucca moths are the only known pollinators of the yucca (O. Pellmyr, pers. comm.). Obviously, at the time of first colonization of the yuccas (yuccas are phylogenetically older than yucca moths), another pollination agent would have existed. The key is likely to be that pollination carries an unusually high fitness consequence in insects whose larvae are seed consumers. A female moth that can increase the probability of fruit production in flowers where she has laid eggs will have higher fitness than one who is less likely to do so, which can explain the origin and maintenance of active pollination in the moths. Can a moth stop pollinating if they select flowers that have already been pollinated? In at least some moth species, female moths can tell (by hormonal means) whether a flower has been visited before, and they are less likely to pollinate again (Pellmyr, pers. comm.). The drawback is that laying more eggs per flower (a consequence of coming second) reduces the probability of fruit retention quite dramatically, so there is a big fitness loss to investing only in previously visited flowers. Another important factor is that the fitness cost (in terms of structure and time allocation) of being a pollinator is trivial, so there is not a lot of selection against it (Pellmyr, pers. comm.).
Regarding cheating behaviour, Addicott and Tyre (1995) consider there to be partial support for the flower-dependent behaviour and probabilistic behaviour hypotheses for cheating in the yucca moth T. yuccasella and the yucca Yucca kanabensis. The flower-dependent hypothesis predicts that moths will respond to previous visits to a flower by modifying their ovipo-sition and pollination behaviour. These flowers may have received sufficient (p.162) pollen for complete fertilization of their ovules and, therefore, female yucca moths could conserve their pollen. This would allow them to have more pollen available to pollinate previously unvisited flowers without having to collect more pollen and move to another infloresence. This hypothesis depends on the assumption that yucca moths are able to detect the presence of previous ovipositions and that ovipositions are a good predictor of pollen in the stigma. Addicott and Tyre (1995) do not think that yucca moths detect pollen in the stigma because they only approach the stigma for the purpose of pollination. As predicted by this hypothesis, yucca moths modified their behaviour on previously visited flowers because bouts on such flowers involved fewer ovipositions and either a lower proportion of ovipositions followed by pollination or no pollination. However, the hypothesis does not explain why some moths failed to attempt to pollinate on flowers that had not been visited. Why would some moths not collect pollen or at least not collect pollen again once their initial supply is exhausted? According to Addicott and Tyre (1995), the most probable answer to this is that the moths are risk averse and the yuccas are self-incompatible. Moths that gather pollen from an inflorescence and then pollinate flowers on that inflorescence will experience very low reproductive success because the retention rate of self-pollinated flowers is basically zero (Pellmyr 1996). Moths that collect pollen should fly to another inflorescence but this may entail considerable risk, either due to predation by bats and night hawks (Aves: Caprimulgidae) or they may struggle to find another inflorescence.
The second hypothesis addressed by Addicott and Tyre (1995), the probabilistic behaviour hypothesis, follows a mixed strategy in an Evolutionarily Stable Strategy (ESS) model of game theory (Maynard Smith 1982), in that moths might respond to the probability that a particular flower had been pollinated previously or would be visited subsequently and pollinated by at least one other moth. The probability of visitation would be a function of the density of moths relative to flowers, which could vary between years, study sites or even within seasons (James et al. 1994). Thus, there is some support for both of the above hypotheses. They are not mutually exclusive because conditional mixed strategies are possible. The probability of pollination could depend on the state of the flower (e.g. number of previous ovipositions) and the state of the moth (e.g. age), as well as the density of moths relative to flowers, which would affect the probability of future visits by other moths to a certain flower (Parker 1984).
Cheater yucca moth species have evolved at least twice. Underlying obligate mutualism is an intrinsic conflict between the parties, in that each is under selection for increased exploitation of the other. Theoretical models suggest that this conflict is a source of evolutionary instability, and that evolution of ‘cheating’ by one party may lead to reciprocal extinction. Pellmyr et al. (1996) present phylogenetic evidence for the reversal of an obligate mutualism: within the yucca moth complex, distinct cheater species derived from obligate pollinators inflict a heavy cost on their yucca (p.163) hosts. Phylogenetic data show the cheaters to have existed for a long time. Coexisting pollinators and cheaters are not sister taxa, supporting predictions that the evolution of cheating within a single pollinator is evolutionarily unstable. Several lines of evidence support an hypothesis that host shifts preceded the reversal of obligate mutualism. Host or partner shifts are mechanisms that can provide a route of evolutionary escape among obligate mutualists in general.
In another study, Marr et al. (2001) have focused on interactions between a cheater moth Tegeticula intermedia and the pollinator T. yuccasella in fruits of the host plant Y. filamentosa. They examined the effects of larval competition on the two species of moth. They found it to be weak and asymmetric, affecting the cheater larvae to a greater extent. There were insufficient larvae to cause seed limitation because no effect of pollinator larvae on either mass or mortality of cheater larvae was detected in years with the highest larval densities per fruit (yuccas abort fruits with many yucca moth larvae). This result is consistent with the hypothesis that the recent rapid radiation of species in the T. yuccasella complex (there is more than one species in this group) may be explained by the ability of multiple pollinator species (some of whom have become cheaters) to use fruits without severe competition. Pellmyr (pers. comm.) considers this to have been preceded by host shifts that led to the coexistence of two pollinator species on a host. Under such circumstances, loss of pollination can occur whether there is a fitness cost or not and becoming a cheater may not be selected for at all. Rather, there is a temporal niche shift that permits the cheater species to exploit seed resources that cannot be accessed by pollinator larvae. Therefore, there is no evidence for the selection for cheating per se, but it occurs merely as a by-product of another driver, namely, lack of access to the yucca seeds by the pollinator larvae.
7.2.2 The senita cactus-senita moth obligate mutualism
The senita moth Upiga virescens (Pyralidae, Lepidoptera) and the senita cactus Lophocereus schottii occur in the Sonoran desert in the United States and Mexico and are mostly obligate mutualists (see below; Fig. 7.10). The senita moth, similar to the yucca moth, has specialized morphological features that allow for pollen loading. Similar to other Lepidoptera, female senita moths avoided ovipositing eggs in flowers that contained an egg. Eggs hatch within three days of flower closing and larvae crawl down the wilting corolla and bore into the top of the fruit, which they consume before entering the cactus branch to pupate. However, only a fraction of eggs produced larvae that survived to become seed consumers themselves. About 20% of fruits were destroyed by larvae. Benefits of senita moths to pollination and fruit set in the senita cactus were about three to four times the costs of seed mortality induced by the larvae, which is similar to the yucca mutualism (Addicott and Tyre 1995). Although copollinators are (p.164) absent in yucca mutualisms, Fleming and Holland (1998) have shown that diurnal halictid bees may also pollinate senita flowers. However, temperature-dependent flower closing limits their effectiveness (flowers are only open for a few hours in the day, usually when it is overcast). Nonetheless, the senita cactus is not entirely dependent on the senita moth and, consequently, lies between the categories of obligate and facultative mutualist. Reduction in and lack of nectar production in the senita cactus discourage co-pollinators that visit flowers for nectar rewards only. Reduced nectar production clearly conserves energy for use in fruit production where fruit set is resource-limited.
For senita cactus and senita moth interactions, it is the great benefit to plants from pollination by moths and the low survivorship of moth larvae that maintain the high benefit-to-cost ratio of the plant. Selective abortion of fruit in yucca appears to be a mechanism inhibiting overexploitation by yucca moths (Pellmyr and Huth 1994) but senita fruits contain only one larva each (no continuum occurs as in yucca fruit). Thus, the criterion for abortion would have to be presence or absence of larva in a fruit. Holland and Fleming (1999) assume that flowers with greater pollination quality and quantity would be preferentially retained by plants where resources limit fruit production, increasing progeny survival of moths that actively pollinate.
There is a major cost associated with a mutualistic relationship, such as the yucca moth and yucca or senita moth-senita cactus relationship. If either of the species, for any reason, cannot be found at the right place at the right time, each of the species suffers reproductive failure. Bronstein (2001) found that, if yuccas bloomed late, they ended up out of synchrony with the emergence of most yucca moths. As a result, the yucca fruits which set seed were the very earliest ones; late-blooming plants failed (p.165) completely. This dependence on timing, which only spans approximately a month in the case of yucca, can easily contribute to reproductive failure in both species. In the case of senita cactus, prolonged flowering occurs, which reduces the possibility of reproductive failure for the senita moth.
Holland et al. (2002) have modelled the senita moth-senita cactus mutualism using an isocline-based phase-plane scenario. Lotka-Volterra type models have been used in this regard but lead to ‘runaway’ population densities, particularly for obligate mutualisms (Stiling 2002). In many mutualisms, the deciding factor that separates the mutualist from parasite and predator may simply be population density because increasing or decreasing population density of a species may increase or decrease the costs and benefits to its partner. Thus, net effects depend on how benefits or costs to a mutualist vary with population density of its partner species (Holland et al. 2004). Holland et al. (2002) take a population view and assume that gross benefits and costs to the cactus population are related to the rates at which moths pollinate flowers and larvae cause fruit loss. Thus, gross benefits and costs are functions of moth abundance (designated as M) relative to the rate of flower production by the plant population. Flower production is the product of the number of plants (P) and the mean number of flowers per plant per night (F). They derived a functional response for gross benefits of pollination by modelling the plant population as a fixed set of flowers over each night’t production and by modelling the pollinator population as randomly searching for and pollinating these flowers. The visitation rate per flower should be proportional to the ratio of pollinators to flowers (M/FP). Thus, a ratio-dependent functional response is derived (see also Thompson 1939).
The dynamics of the cactus population can be derived as follows:
The dynamics of the moth population is written as follows:
This phase-plane diagram results in two equilibrium points, one of which is locally stable and the other locally unstable. However, the functional response, (1 — a)αFP[1 - exp(-γ1M/FP)] × [1 — exp(—γ2M/FP)], assumes that pollination and oviposition are independent random events. In nature, however, pollination and oviposition are correlated behaviour-ally because female moths pollinate flowers as a way of provisioning their offspring with food (Fleming and Holland 1998). When this is incorporated into the functional response, the first term of the cactus equation becomes
The functional response in the first term of the moth equation becomes
Gross recruitment of new moths is the number of flowers on which effective oviposition occurs (survival from eggs to pupae). The main difference between the state plane for the functional response of this model and the original is that there is now only one line representing the moth’h zero isocline and there is at most only one nonzero equilibrium point (Holland et al. 2002). It is likely that this alteration of the model is more biologically reasonable because pollination behaviour has likely evolved in association with oviposition to increase the likelihood of egg and larval (p.167) survival (Fig. 7.11a and b). This model would probably also work for the yucca moth-yucca system.
Note that Holland et al. (2004) have also used evolutionarily stable strategy (ESS) theory to show that plants can maximize fitness by allocating resources to the production of excess flowers at the expense of fruit. Fruit abortion resulting from excess flower production reduces pre-adult survival of the pollinating moths, and maintains its density beneath a threshold that would destabilize the mutualism. Such a strategy is evolutionarily stable against invasion by cheater plants that produce fewer flowers and abort few to no fruit. This mechanism may be a general process of preserving mutualistic interactions in nature.
7.3 Seed dispersal and seed predation
The effects of seed predators, such as desert rodents, finches, sparrows, and harvester ants, are less dramatic but may be equally effective at controlling plant populations. For example, Brown and Heske (1990) removed three species of kangaroo rats (Dipodomys spp.) from plots of Chihuahuan Desert shrub habitat from 1977 to 1990, and found that the density of tall perennial and annual grasses had increased approximately 3-fold and rodent species typical of arid grassland had colonized. In the same study, Heske et al. (1993) showed that significant increases in the abundance of a tall annual grass (Aristida adscensionis) and a perennial bunch grass (Eragrostis lehmanniana) occurred. This change in vegetative cover affected the use of these plots by several other rodent species and by foraging birds. The mechanism producing this change probably involved (p.168) a combination of decreased soil disturbance and reduced predation on large-sized seeds when kangaroo rats were absent. Species diversity of summer annual dicotyledonous plants was greater on plots where kangaroo rats were present, as predicted by keystone predator models (Fig. 7.12; see also Fig. 5.18). However, Heske et al. (1993) were unclear whether this was caused directly by activities of the kangaroo rats or indirectly as a consequence of the increase in grass cover. Their study site was located in a natural transition between desert scrub and grassland, where abiotic conditions and the effects of organisms may be particularly influential in determining the structure and composition of vegetation. Under these conditions, kangaroo rats may have a dramatic effect on plant cover and species composition.
Seed dispersal by large mammalian herbivores is also important, particularly in cases where the seeds are hard (see Campos and Ojeda (1997) with regard to Prosopis, Rohner and Ward (1999) with regard to Acacia). In many cases, germination of seeds (such as of Acacia species) increases as mammal body size increases (see Fig. 11.5). This is because the mammals ingest the seeds and defaecate them later. This scarifies the seed and the greater the body mass of the animal, the longer it remains in the gut and the greater the mechanical effect of the gut’t hydrochloric acid on inducing scarification (Rohner and Ward 1999; Bodmer and Ward 2006). In Acacia species, the seeds are very hard and can only germinate once scarification occurs. This may be done by water, requiring waiting until the rains in the following year, or it can be done by large mammals. In some cases, there can be negative effects on germination, such as in ostrich Struthio camelus (Aves, Family: Ratites) in Israel (Rohner and Ward 1999) and wild boar Sus scrofa in the Monte desert in Argentina (Campos and Ojeda 1997). In these cases, all seeds are damaged and cannot germinate.
In a 17-year study in the central Negev desert highlands of Israel, Indian Crested Porcupines, Hystrix indica, were found to focus their activities in midslope areas where plant biomass was maximal due to run-off water accumulation (Shachak et al. 1991; Boeken et al. 1995). In a 5-year study of a population of Tulipa systola in the same desert highlands, herbivory by porcupines was generally low although the effects on recruitment were consistently greater than on other parts of the plant (Boeken 1989), but they do not generally limit geophyte populations. However, pits dug by porcupines accumulate organic material, including seeds and water (Gutterman and Herr 1981; Boeken and Shachak 1998; Boeken et al. 1998). As a result of this accumulation of materials, plant density, biomass, and species richness were found to be much higher in porcupine diggings than in undisturbed areas (Boeken et al. 1995). These authors showed that plant density and diversity were limited by microsite availability due to a lack of water infiltration in undisturbed areas (Fig. 7.13). In contrast, diggings remained moist throughout the growing season and diggings were only limited by seed arrival.
Granivory is an important interaction in ecological communities, especially in deserts where many plant populations exist as seeds for long periods (Davidson and Morton 1981; Morton 1985; Rissing 1986). Granivores can also be seed dispersers. Harvester ants have been shown, in a number of deserts (Australia, South Africa, and South America), to be the most important granivores and seed dispersers (Morton 1985; Kerley 1991) (Fig. 7.14), although rodents are more important in North American and Israeli deserts (Mares and Rosenzweig 1978; Abramsky 1983). Many seeds have appendages, known as elaiosomes, that are attractive to ants and encourage dispersal to ‘safe sites’ for germination and growth (Rissing 1981). Davidson and Morton (1981) have recorded myrmecochory (ant dispersal) in a wide range of Australian species, especially in diaspores of the family Chenopodiaceae. The widespread and dependable presence of ants in the Australian deserts, and the relative importance of ant species that are capable of carrying such large diaspores leads to the dependence of Australian plants on these dispersal strategies.
Rissing (1986) found that six plant species were significantly associated with nests of the desert seed-harvester ants, Veromessor pergandei and Pogonomyrmex rugosus, in the Mojave desert. Seeds of two common annuals, Schismus arabicus and Plantago insularis, have 15.6 and 6.5 times higher levels in terms of numbers of fruits or seeds growing on ant nest refuse piles compared with nearby controls. Interestingly, these two species do not have obvious appendages attractive to ants. Similar results have been recorded by Wilby et al. (2001) in the northern Negev desert, Israel, for Messor ebeninus and M. arenarius. A total of 55 plant species were found on the nest mounds as opposed to 25 in the undisturbed soil. The favoured food items of M. ebeninus are seeds of the grass Stipa capensis. (p.170) In contrast with other plant species it occurred at much lower densities on the nest mounds, probably reflecting consumption. In contrast, another common species, Reboudia pinnata, increased from about 10% of samples on the undisturbed soil to 85% of mound samples. This last-mentioned plant species has a hardened fruit wall, which protects the seeds from predation (Gutterman 1993).
7.4 Are these coevolved systems?
All mutualistic interactions can be viewed in terms of the Red Queen hypothesis (Van Valen 1977) as each mutualist needs to evolve continually to avoid being exploited by its mutualist partner. Thus, such highly coevolved systems arose despite the needs of each conflicting!
1. To the plant, an ideal pollinator or seed disperser would move quickly among individuals but retain high fidelity to a plant species so that little pollen or seed is wasted.
2. To the pollinator or seed disperser, it would be best to be a generalist and obtain nectar and pollen from flowers or seeds in a small area, minimizing energy costs.
This casts doubt on whether there is true mutualism or whether both are trying to win an arms race. One way in which the plant can ensure the pollinator’r/seed disperser’r fidelity is to have sequential flowering among species within years and simultaneous flowering within a species. How is it generally done? Here are some examples.
(p.171) 7.4.1 Senita and yucca systems
There are a large number of similarities in the independently derived mutualisms in the senita cactus-senita moth and yucca-yucca moth systems, suggesting that they have evolved in response to similar selection pressures, including selection for reduced nectar production in the plants and specialized pollen-collecting structures and active pollination behaviour in the moths. Both systems feature pollinators whose life cycles are intimately associated with long-lived plants with seasonal flowering cycles. Fleming and Holland (1998) propose that three of their common features, namely, nocturnal flower opening, self-incompatibility, and resource-limited fruit set, have been important during the evolution of obligate mutualisms. Nocturnal flower opening is important for these mutualisms because it limits the number of potential flower visitors to moths only (Thompson and Pellmyr 1992) and excludes other co-pollinators. Self-incompatibility selects for pollinators that visit flowers on different plants and, thus, both yucca moths and senita moths are under strong natural selection to be effective outcrossers. Resource-limited fruit set and reduced nectar production characterize the yucca and senita systems. Reduced nectar production may be selected for, especially when unfertilized ovules rather than nectar or pollen is the primary reward attracting pollinators, which favours the evolution of specialized pollination. Pollen limitation does not appear to be important for fruit set in either the yucca or the senita cactus. Pellmyr et al. (1996) have suggested that differences among flower visitors in pollination quality (the genetic contribution to fruit set) can favour the evolution of obligate mutualisms through selective abortion of fruits of low genetic quality.
7.4.2 Why Negev flowers are often red
There are about 15 species of large, bowl-shaped flowers of six genera from three families in the Mediterranean region of Israel (Heinrich 1994). It is dominated by poppies (Ranunculus spp.) of two genera. Most species in this group have other colours in other parts of the world. Ranunculus has about 400 species worldwide, most of which are white or yellow (Heinrich 1994). Only three, all in the Mediterranean, are red. All of these species have cup-shaped flowers that are far broader than those in other countries. Wild tulips (Tulipa spp.) are mostly yellow, yet in Israel they are red. The species in this convergent guild do not flower simultaneously. Anemones usually flower first, followed by tulips, buttercups, and poppies (Heinrich 1994). These flowers are seldom pollinated by bees. Rather, they are mostly pollinated by scarab beetles (Family Scarabeidae) of the genus Amphiocoma. Dafni et al. (1990) distributed unscented, flower-shaped plastic cups of various colours in the field to act as beetle traps. Of the beetles trapped in the variously coloured flower models, 127 of 148 were caught in red flower models. Amphiocoma do most of the pollination of (p.172) the red flowers, although the red colour also advertises sex. Once they detected a red flower, they stayed to mate. The antennae are microscopic in size. Their scent organs seem almost atrophied (Heinrich 1994) but their eyes are not. Their attraction to red flowers finds mates for them (Heinrich 1994). Dafni et al. (1990) showed that these Amphiocoma beetles could see the colour red. This resulted in enhanced mating for them. It is not known how the red flower guild evolved but a probable scenario is that the plants imitated one another, and that many species used the same red signal in their advertising campaigns that served to attract pollinators (Heinrich 1994). The pollinators in turn apparently preferred red over other colours (Heinrich 1994).
7.4.3 Blepharida chrysomelid beetles and Bursera tree systems
As it was first applied in plant-animal interactions by Ehrlich and Raven (1964), the hypothesis that rates of diversification in plants and plant-feeding insects is higher than in other taxa has been successfully applied (see also Thompson (1998) for more complex versions of this hypothesis). Several such studies have shown that plants and plant-feeding insects often have increased rates of diversification compared to sister groups with different life histories (Becerra 1997; Pellmyr 2003). Clearly, such claims are dependent on appropriate phylogenies. An exception to the lack of phylogenies is the study by Becerra (2003). Judy Becerra worked on 38 species of Bursera trees and their associated Blepharida leaf beetles (Family Chrysomelidae). Please note that not all species of Blepharida and Bursera occur in deserts or other arid systems; many occur in dry thickets and dry forests. Becerra (1997, 2003) reported evidence for convergent evolution of a combination of terpenoid defences and the force with which they are released upon attack. Species that produce simple chemical mixtures (one to a few monoterpenes) release the compounds with a forceful squirt upon damage (Fig. 7.7).
Species that use complex mixtures of monoterpenes and diterpenes (up to 12 compounds) do not have a forceful squirt. In Fig. 7.15, Bursera species (solid lines) are highly squirting species. Blepharida species (solid lines) have evolved the ability to counterattack their host’t squirt defence by cutting the canals to stop the flow of resins. The Bursera flavocostata group (dashed lines) produce chemically similar complex mixtures that include between 7 and 12 terpene compounds. Beetles of the Blepharida flavocostata complex (dashed lines) are able to metabolize the complex mixtures of defensive chemicals present in these hosts.
Speciation events that appear synchronous among plants and herbivores lend further support to cospeciation owing to joint allopatry Judy Becerra demonstrated that shared host plant defensive chemistry can be more important than phylogenetic association in host shifts of leaf beetles (Chrysomelidae). In other words, host shifts by the beetles on to distantly (p.173) related plant species were coincident with a shared chemistry with the former host plant species.
7.4.4 Dorcas gazelle—lily system
There is at least one case where coevolution can be claimed in a mammal system. Owing to the almost complete removal of all flowers of the lilies by dorcas gazelles (Fig. 7.16) (there is no vegetative reproduction in this species) mentioned above, the lily populations in the dunes can only be maintained by seed dispersal from source populations outside the dunes where gazelles are rare or absent (owing to low lily densities in the compact loess substrate).
There is strong selection on lilies to minimize the effects of gazelle herbivory: lilies that have their bulbs partially consumed in one year are less likely to produce flowers and produce fewer, smaller leaves in the following season. Ward and Saltz (1994) found that the gazelles select lilies (p.174) according to their size in a manner consistent with an optimal foraging model (Fig. 7.17).
As predicted by this model, contrary to popular expectation that gazelles should prefer the largest plants, gazelles should prefer the smallest plants, and not completely consume large plants. This is indeed what they do because the cost of sand removal is high (Fig. 7.17). Furthermore, when searching for leaves (leaves are available on the surface for a few months only and gazelles do not bother to dig when there are leaves), gazelles do not follow a Markov model (which assumes that there is no effect of previous search history on the gazelles) in searching for plants, and instead, focus on high densities of lilies and eat the largest lily leaves once there.
Lilies also grow in ways that are consistent with coevolution. These lilies grow their bulbs down deeper into the sand (pulling them down with contractile roots) to minimize the effects of herbivory in populations where (p.175) gazelles are common but have bulbs under the surface in populations where gazelles are absent (Ward et al. 1997, 2000a). Lilies protect their leaves with calcium oxalate crystals (called ‘raphides’)—gazelles eat only the unprotected tips (Fig. 7.18a and b).
Lily populations where gazelles are common have more crystals in their leaves than where gazelles are absent (Ward et al. 1997; Ruiz et al. 2002). Ruiz et al. (2002) considered this to be a form of constitutive defence (i.e. unlike inducible defences, the strategy does not change when there is herbivory), because adding more calcium to the sand did not increase investment in defence (Fig. 7.19).
(p.176) This study demonstrated that calcium oxalate is produced in leaves to protect them against herbivory—raphides in geophytes had previously been assumed to have developed as a consequence of excessive calcium uptake from the soil (Franchesci and Horner 1980). The close coevolution of the gazelle (optimal foraging behaviour both in terms of size of plant consumed and search behaviour, and avoidance of chemically defended parts of leaves) and the lily (evolution of deeper bulbs and chemical investment in leaves) indicates that strong biotic interactions between herbivore and plant can and do develop in arid regions in spite of the great impact of abiotic factors on plant populations.