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chainfruit cholla fruit
?Chelinda vittiger
Page 2 of A Natural History of Extrafloral Nectar Collecting Ants in the Sonoran Desert:: Cactus extrafloral nectaries
How likely is it that cacti secrete extrafloral nectar to attract predators and parasitoids of their herbivorous enemies? Certainly there are a number of organisms that feed on cacti and many cause serious damage (Mann 1969; Blom and Bratz 1976). 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 species identity and density for both ants and herbivores 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 cause damage beyond the loss of nutrients or infect them with diseases.
Davidson and McKey (1993), though, point 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 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.
Interestingly, rather than altogether rejecting the "ant distraction" hypothesis, Davidson and McKey (1993) come up with their own version. They argue that ant colony growth, like plant growth, is limited by the ratio of carbon and nitrogen resources (Bloom et al. 1985). By providing extra carbohydrates to aphid-tending ants and skewing this ratio, plants "tempt"ants into feeding on their homopteran associates. In support of this idea, ant behavior toward their homopterans does appear to change with changes in the nutritional status of ant colonies (Way 1954, Anderson 1991).
While this new version of the "ant distraction" accounts for some of the problems in the old one, it also introduces some new concerns. First, as will be discussed below, some ants may use endosymbionts to create a more balanced diet from extrafloral nectar. For ants able to do this, extrafloral nectar would not necessarily tempt them into eating any homopteran associates that they might have. Second, even if plants could create carbon to nitrogen ratio imbalances in certain ants by secreting extrafloral nectar, this could lead to an additional problem. That is, such ants might be tempted into making up the deficit by turning their attention not only to homopterans but to another source of protein as well -- pollen. Actually, it would be interesting to know from a general standpoint whether the pollen of extrafloral nectar-bearing plants is on average less accessible to ants than that of plants without extrafloral nectaries.
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? The complete answer to this question requires a better understanding of ant nutritional biology than we currently have. Traditionally it has been argued that 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. As Brian (1983) pointed out, using plant sugars to satisfy worker energy requirements should help conserve proteins for larval growth.
But ants may also collect nectar for reasons other than obtaining sugars. 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).
While all this still suggests that ants collect extrafloral nectar primarily to obtain sugars, a recent study by Schröder et al. (1996) gives reason to withhold final judgement. Apparently, many ant species in the genus Camponotus (a genus whose members often collect extrafloral nectar) have endosymbiotic bacteria similar to those found in aphids. In aphids these bacteria synthesize various host-essential amino acids from plant sap. That bacterial endosymbionts in ants may play a similar role is supported by their presence in the midgut. Currently, only Camponotus, Formica, and other ants in the subfamily Formicinae have been shown to contain endosymbionts (Dasch et al. 1984).
Finally, in addition to the above reasons for collecting extrafloral nectar, 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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