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exuding a drop of nectar |
collecting extrafloral nectar |
On this page I will discuss in turn:
In the Sonoran Desert certain ant species regularly visit cacti for a reason: they come to collect the nectar that these plants produce. This nectar, though, is not the nectar produced by flowers to attract pollinators; in fact, it probably doesn't play any role at all in cactus pollination biology. Instead, it oozes out of various parts of these plants and may play a number of roles in their biology.
Plant structures that produce nectar for reasons other than attracting pollinators are called extrafloral nectaries (hereafter referred to as EFNs). EFNs are found in at least 68 families of flowering plants (Elias 1983). But like many things defined by exclusion, EFNs are a varied lot. Structurally diverse, they range from barely discernible forms to highly vascularized cup-like organs and occur on many different plant parts including leaves, stems, petioles, stipules, flowers stalks, and even on the outside of flowers. Even within the family Cactaceae there is variation in the kinds of EFNs you find and where you find them (Blom and Clark 1980; Elias 1983). However, with the exception of saguaros (Cereus giganteus), all EFN-bearing cacti at my study site had the same type of EFN even though this "type" has probably evolved more than once. Called thorn nectaries, these EFNs are modified spines (or glochids) produced by specialized axillary buds known as areoles. Below are two photographs of the very conspicuous EFNs of barrel cacti. Note the distinct areoles from which both spines and thorn nectaries arise.
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exuding a drop of nectar |
collecting extrafloral nectar |
While the majority of EFN-bearing cactus species at my study site had thorn nectaries, these species differed in the particulars of extrafloral nectar production. Among both staghorn chollas (Opuntia versicolor ) and prickly pears (Opuntia phaecantha ), extrafloral nectar secretion was seasonal and only occurred on actively growing tissue. In contrast, chainfruit chollas (Opuntia fulgida) produced it continuously on most parts of the plant although secretion was highest on new growth. Finally, barrel cacti (Ferocactus wislizenii) also produced extrafloral nectar throughout the year. But unlike chainfruit chollas, barrel cactus EFNs appeared to require continual attendance by ants in order to remain active. Several times during my study ant colonies stopped visiting one of these plants for an extended period of time. When this happened, large droplets of viscous nectar accumulated and eventually solidified. This desiccated nectar eventually disappeared but wasn't replaced by any new droplets.
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Staghorn cholla (O. versicolor) |
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When we talk about why cacti produce extrafloral nectar we have to be aware that we are actually addressing two separate questions. This is because the selection pressures that favored its secretion may very well differ from those that currently maintains them. While we can bring to bear a variety of evidence to try to determine why various cacti or their ancestors did this in the first place, it would be at best a very involved and challenging exercise. Instead, I'll focus here on the potential selective factors that currently maintain extrafloral nectar secretion in cactus populations. In doing this I'll be making an implicit assumption; that is, secreting extrafloral nectar is a costly processes. While this is probably a reasonable assumption for most plants, the case for it seems particularly strong here; after all, most of the distinctive features that characterize cacti are evolved responses to xeric environments -- they've undergone strong selection for not giving up water, in any form, easily.
While the selection pressures against producing extrafloral nectar may be higher for cacti than other plants, they presumably do both for some of the same reasons that other plants do. Currently there are three major hypotheses for why some plants produce it. These are: (1) to excrete excess sugars; (2) to defend themselves against their herbivorous enemies; and (3) to procure additional soil nutrients.
The first hypothesis is that plants secrete extrafloral nectar to eliminate excess sugars that accumulate when they direct various non-sugar materials in the phloem toward developing plant organs (Frey-Wyssling 1955; Helder 1958; Mound 1962; Milburn 1975). To my knowledge, there has been only one solid attempt to test this hypothesis and that one did not support it (Baker et al. 1978). Still, the idea that extrafloral nectar secretion may occasionally play a role in plant physiology does not seem entirely implausible. Nevertheless, very little research continues in this area.
The second major hypothesis is that extrafloral nectar secretion functions in plant defense. In the simplest version of this hypothesis, extrafloral nectar attracts organisms that remove, attack, prey upon, or parasitize plant herbivores. Early on, most researchers believed that plants produced extrafloral nectar to attract ants. These insects are frequently attracted to extrafloral nectaries and many species remove, attack, or prey upon insect herbivores and seed predators. A number of studies do indicate that ants can reduce vegetative damage or decrease seed predation on plants with extrafloral nectaries (Janzen 1966; Elias and Gelband 1975; Bentley 1977; Deuth 1977; Keeler 1977, 1980, 1981; Tilman 1978; Koptur 1979, 1984; O'Dowd 1979; Schemske 1980; Beckman and Stucky 1981; Stephenson 1982; Horvitz and Schemske 1984; McKey 1984; Barton 1986; Kelly 1986; Smiley 1986, Del-Claro et al. 1996). However, ants don't always visit EFNs and sometimes they don't offer protection when they do (reviewed in Becerra and Venable, 1989). In part because of this, people have recently begun to explore the role that extrafloral nectar plays in attracting parasitoids to plants (Treacy et al., 1987; Pemberton and Lee 1996; Stapel et al., 1997).
How feasible an explanation is this hypothesis for explaining cactus extrafloral nectar production? Certainly there are a number of herbivorous insects that feed on cacti and can cause considerable damage (Mann, 1969). Below are photographs of some of the more conspicuous insects that fed on cacti at my field site.
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chainfruit cholla fruit |
?Chelinda vittiger |
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Also, as this website will detail, ants often visit cactus extrafloral nectaries in large numbers. While I didn't directly explore whether their presence was beneficial, at least one other group has. Pickett and Clark (1979) examined the effect that the ant Crematogaster opuntiae had on the cactus-feeding coreid bug Chelinda vittiger. Under controlled conditions these researchers showed that both juvenile and adult C. vittiger spend less time on Opuntia acanthocarpa fruit with ants than they do on those without. Some nymphs were even captured and killed by the ants. However, their field study failed to show a relationship between the number of ants per floral cup and the number of fruit set per cactus branch in the field (there was a positive but non-significant correlation).
Pickett and Clark's (1979) results alone do not reject the plant defense hypothesis for why O. acanthocarpa has EFNs. There are at least a couple of reasons why. First, attracting ants does not have to increase plant fitness in every instance; it only has to do so on average. In fact, as a number of researchers have pointed out, the effects of possessing extrafloral nectaries on plant fitness should vary over space and time (Thompson 1982, 1988; Barton 1986; Herrera 1988; Cushman and Whitham 1989; Cushman and Addicott 1991). This is because both ant density and herbivore density are likely to vary over space and time. Finally, it could also be possible that these cacti are producing extrafloral nectar to attract organisms other than ants to their defense. As shown below, other potential plant defenders were occasionally attracted to cactus EFNs at my field site.
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In addition to the first version of the plant defense hypothesis, Becerra and Venable (1989) have proposed another. Their version comes from the observation that ants, instead of protecting plants, occasionally protect their enemies. Ants do this because these plant enemies -- aphids and other homopteran insects -- suck phloem and excrete a sugary solution known as honeydew that ants collect. Becerra and Venable argue that certain plants have evolved EFNs in order to "distract" ants away from their protective duties. There are at least two ways in which this could work. First, plants could give up less nutrients than their homopteran enemies are providing ants if the costs of collecting honeydew are sufficiently higher than that for collecting extrafloral nectar. In some systems ants do put a great deal of effort into homopteran husbandry (reviewed in Hölldobler and Wilson 1990). Second, plants could be selected for providing ants even more nutrients than than their homopteran enemies are taking away if these insects also damage plants or infect them with diseases.
Davidson and McKey (1993), though, pointed out a potential problem with Becerra and Venable's idea. That is, why shouldn't ants simply collect both honeydew and extrafloral nectar? In other words, implicit in Becerra and Venable's scenario is that foraging workers can collect one or the other but not both. But certainly many ant colonies will have sufficient worker forces to collect both honeydew and extrafloral nectar. And those that don't could eventually by either redeploying workers or by increasing the size of their worker force.
With one assumption, though, Davidson and McKey (1993) were able to resurrect the ant distraction hypothesis. The assumption is that ant colony growth, like plant growth, is limited by the ratio of carbon and nitrogen resources (Bloom et al. 1985). Under this scenario plants flood ants with abundant carbohydrates but starve them for amino acids. To make up for this deficit ants might be tempted to feed on their homoptera. In support of this idea, ant behavior toward their homopteran associates does appear to change with changes in the nutritional status of ant colonies (Way 1954, Anderson 1991).
So what is the likelihood that cactus extrafloral nectaries are maintained because they distract ants? Because I never saw homopterans feeding on barrel cactus or chainfruit cholla I suspect that "ant distraction" doesn't play a role in maintaining extrafloral nectar production in these plants. Aphids do, however, attack prickly pear flowers in the spring (see photo on C. opuntiae web page), at a time when these plant's EFNs are active.
The third major hypothesis for explaining why some EFNs exist is the nutrient enhancement hypothesis (Wagner, 1997). Based on the fact that ant colonies tend to concentrate nutrients in the immediate vicinity of their nests -- through storing food, discarding debris, and defecating -- this hypothesis argues that EFNs are maintained because they attract ant nests to the base of EFN-bearing plants. This idea follows naturally from the observation that many tropical epiphytes apparently provide housing for ants in order to collect these same nutrients (Huxley, 1978; Rickson, 1979; Rico-Gray et al 1989; Treseder et al. 1995; Davidson and Epstein 1989; Joliet 1996). The particular study that produced this hypothesis suggests that it is a better explanation than the predator defense hypothesis for the maintenance of EFNs in Acacia constricta populations (Wagner, 1997).
This is an extremely new hypothesis but a particularly intriguing one with regard to some of the ants and cacti at my study site. Ants there often nested at the base of EFN-bearing cacti that produced extrafloral nectar the year around: Solenopsis aurea frequently nested at the base of both barrel cacti and chainfruit chollas while C. opuntiae often nested at the base of or even in chainfruit chollas.
So what do ants get out of collecting extrafloral nectar? Foraging ants, like many adult hymenopteran insects, collect nectar in some form. Like these insects, ants are often very active and use the sugars in nectar as a source of energy. Also, as Brian (1983) pointed out, using plant sugars to satisfy worker energy requirements helps conserve proteins for larval growth. But there may also be other reasons why ants collect it. Pickett and Clark (1979) found that the extrafloral nectar of O. acanthocarpa has a very high amino acid concentration. Not only was the concentration of amino acids much higher than that found in floral nectar from the same plant, it is one of the highest concentrations ever reported for a nectar. It is important to note, though, that not all cactus extrafloral nectar is so rich in amino acids (Ruffner and Clark 1986). The actual role that amino acids play in attracting ants to extrafloral nectar probably varies with cactus species. In the case of O. acanthocarpa, the amino acid content of its extrafloral nectar is probably high enough to create an additional nutritional incentive for nectar collecting. In cases where the amino acid concentration is likely too low to do this, people have argued that the amino acids make the extrafloral nectar "tastier" (Baker and Baker 1983) or prevent it from crystallizing (Kartashova 1965). Finally, in addition to the above reasons for collecting extrafloral nectar -- which are probably reasons why ants in general collect it-- ants living in xeric environments may have another. As Whitford et al. (1975) showed, many desert ant species that collect extrafloral nectar are just as sensitive to desiccation as species from more mesic environments. So, in this environment where water is difficult to obtain, cactus extrafloral nectar may be a major source (Ruffner and Clark 1986 and references, therein).
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Copyright (c) 1998 Barry Sullender
Rice University
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