Author: Maloof, Joan E; Inouye, David W Source:
Abstract. Nectar robbers
are birds, insects, or other flower visitors that remove nectar from flowers
through a hole pierced or bitten in the corolla. This paper is a review of the
effects of nectar robbers on pollinators, pollination, and fitness of the
plants they rob. Charles Darwin assumed that nectar robbers had a negative
impact on the plants that they visit, but research done in the last 50 years
indicates that they often have a beneficial or neutral effect. Several studies
document that robbers frequently pollinate the plants that they visit. Robbers
may also have an indirect effect on the behavior of the legitimate pollinators,
and in some circumstances, the change in pollinator behavior could result in
improved fitness through increased pollen flow and outcrossing. The effects of
nectar robbers are complex and depend, in part, on the identity of the robber,
the identity of the legitimate pollinator, how much nectar the robbers remove,
and the variety of floral resources available in the environment.
Key words: Bombus spp.
bumble bee; cheater; foraging; hummingbird; indirect effects; mutualism; nectar
robbing; plant fitness; pollination.
INTRODUCTION
Nectar robbers are birds,
insects, or other flower visitors, that remove nectar from flowers through a
hole pierced or bitten in the corolla. The last comprehensive review on nectar
robbing was by Inouye in 1983. Since then, new studies have appeared that broaden
our view of the phenomenon. The goals of this paper are to review the recent
literature on nectar robbing and to attempt an expanded understanding of the
ecological and evolutionary roles that robbers play. Understanding the effects
of nectar robbers on the plants they visit and on other flower visitors is
especially important when one considers the high rates of robbing that a plant
population may experience (Table 1) and the high percentage of all flower
visits that nectar robbers make to some species (Table 2).
The plant-pollinator
relationship is considered a mutualism because the plant benefits from the
pollinator's transport of male gametes (but see Thomson and Thomson 1992),
whereas the pollinator benefits from a reward (nectar, pollen, oil, fragrance,
etc.). Mutualisms are thought to be especially susceptible to cheaters, species
that can obtain the reward produced for the mutualist without providing service
in return (Boucher et al. 1982, Thompson 1982, Bronstein 1994). Nectar robbers
are frequently described as cheaters in the plant-pollinator mutualism (Darwin
1841, Thompson 1982, Bronstein 1994, Richardson 1995), because it is assumed
that they obtain a reward (nectar) without providing a service (pollination).
In this paper, however, we will explore the legitimacy of that assumption.
In the 18 studies we found
that measured the effect of nectar robbers on seed set, the incidences of
negative effects, neutral effects, and positive effects were equal (Table 3).
For example, Morris (1996) found that, "despite the expectation that
nectar larceny should be detrimental to plant fitness ... there were no
significant differences ... in the percent of flowers initiating fruits, the
number of nutlets initiated per successful flower, or the mass of seeds produced
by robbed and unrobbed flowers."
Why does the expectation
that nectar robbers are universally detrimental cheaters persist, in the
presence of evidence to the contrary? Perhaps it has to do with the difficulty
of changing attitudes that have been held for so long. Charles Darwin (1872)
himself wrote that, "all plants must suffer in some degree when bees
obtain their nectar in a felonious manner by biting holes through the
corolla."
We propose here a
reexamination of the attitude held by Darwin, and many others, about nectar
robbers. When the existing literature on robbers is examined as a whole, it
appears that robbers, at least bumble bee nectar robbers, are as likely to be
beneficial to the flowers they visit as they are to be detrimental. In this
paper, we discuss six questions that help to predict whether the presence of
robbers will have negative or positive fitness consequences for the plant: (1)
Are the robbers pollinating? (2) What type of organism is the robber? (3) Does
the robber change the behavior of the legitimate pollinator? (4) What is the
identity of the legitimate pollinator(s)? (5) How much nectar is left by the
robber? (6) What other resources are available to the pollinator?
Nectar theft (sensu Inouye
1983), characterized by a morphological mismatch between flower and visitor,
and not by damage to corollas, will not be addressed in this paper.
ARE THE ROBBERS
POLLINATING?
Inouye (1980) wrote that
robbers "generally are not pollinators," but in most cases, it is
merely assumed that the robbers are not pollinating; no controlled studies have
been done to explore this assumption. In fact, many studies that have examined
robbers more closely have suggested that they often do pollinate. In some
cases, this conclusion was made through observation and inference (the robbers
appear to be pollinating, e.g., Guitian et al. 1993, 1994). In other cases,
observations coupled with field experiments enable us to say conclusively that
the robbers are pollinators. Palmer-Jones et al. (1966) caged red clover
(Trifolium pratense). In cages containing long-tongued humble bees, 60-79% of
the flowers set fruit; in cages containing only short-- tongued nectar robbers
(Bombus terrestris), 10-27% of the flowers set fruit; and in cages that
excluded pollinators, 0-0.2% of the flowers set fruit. Although the
long-tongued bees were more effective as pollinators, it is also clear that the
robbers were pollinating. Similar results were found by Kendall and Smith
(1976), who studied fruit set in the bean, Phaseolus coccineus. Previously
unvisited flowers were observed for visitors and subsequent fruit set. Of the
flowers visited by the legitimate pollinators (long-tongued bumble bees and
short-tongued honey bees), 18-31% set fruit, of flowers visited only by the
robbing bees (Bombus terrestris and B. lucorum) 6.5% set fruit, whereas only
2.8% of unvisited flowers set fruit.
TABLE 1.
TABLE 2.
Waser (1979) observed
carpenter bees (Xylocopa sp.) contacting the reproductive parts of
self-incompatible desert shrubs, Fouquieria splendens, while robbing them of
nectar. The bees that he collected carried pollen from the species they were
robbing. When he excluded hummingbirds, the presumed primary pollinators, but
allowed the carpenter bees to access the plants, the flowers set seed. In
addition, he found a strong positive relationship between seed set and
carpenter bee abundance. Scott (1989), studying the same species, found that
80% of the flowers formed fruits and 54-77% of the ovules formed seeds when a
flower was visited at least twice by nectar-robbing carpenter bees. He
concluded that carpenter bees are the major pollinators of F. splendens in Big
Bend National Park, Texas, USA.
Higashi et al. (1988)
studied the behavior of bumble bee queens (Bombus hypocrita sapporensis) that
robbed nectar from Corydalis ambigua flowers. Breeding studies suggested that
the plant was self-incompatible; therefore, it was not surprising that the four
plants that were not visited by insects did not produce any seeds. However,
59.7% of the C. ambigua plants that were visited only by nectar robbers set
seed, prompting the researchers to conclude that "robbers contributed
directly to pollination." Pollination probably took place when the large
queens positioned themselves to rob the flower (Fig. 1). The authors suggest
that these humble bees are not real "robbers," but should be called
"robber-like pollinators."
Birds may also act as
"robber-like pollinators." In one example, a flower-piercer, Diglossa
sp., pollinated Tristerix longebracteatus flowers while robbing them of nectar
(Graves 1982). In the population that Graves studied, "virtually every
open flower was basally pierced by Diglossa or hummingbirds," yet the
fruit set was 87.5%. He concluded that "Diglossa appears to be a principal
pollinator of T. longebracteatus in northern Peru."
These examples document
cases in which the robber pollinates in the process of collecting nectar.
However, pollination by robbers is not always concurrent with nectar
collection. Angiosperms have a broad range of reproductive strategies, and the
morphology and phenology of the flower will influence the behavior of the
robber. For example, many short-lived flowers offer both pollen and nectar
during their entire life span (e.g., Hibiscus moscheutos; Spira 1989). Some
longer lived flowers offer both nectar and pollen on the first day, and
negligible rewards after that (e.g., Lantana camara; Barrows 1976). Other
flowers stagger their reward presentation, offering first pollen and later
nectar, or vice versa (e.g., Mertensia paniculata; Morris 1996). Because of the
di81, no. 10 (Oct 2000): p. 2651-2661fferences in reward presentation, visitors
may be differentially attracted to flowers in a particular stage of
development, and visitors may "handle" flowers differently depending
on the reward that they are seeking. This could result in a bumble bee robbing
nectar by biting a hole through the corolla, but then subsequently pollinating
while attempting to collect pollen.
TABLE 3.
FIG. 1.
An example of this bimodal
foraging behavior (see Fig. 2) is given by Meidell (1944), who described the
foraging behavior by a bumble bee to flowers of Melampyrum pratense:
"After the bee has robbed a flower of nectar, she places herself on the
edge of the upper lip, stretching her hindlegs across its mouth, and vibrates
her wings rapidly. This results in pollen being showered on to her legs. When
this same bee takes up her position on the next flower, her pollen-covered legs
touch the projecting stigma, thus probably effecting pollination."
Similar behavior, but in
the opposite order, was noted by Macior (1966); bumble bee queens (Bombus
affinis) would sometimes collect pollen from Aquilegia canadensis flowers
before climbing up the outside of the nectar spur and robbing the nectar. He
concluded that "pollination is accomplished during pollen and nectar
foraging even when nectar is secured by spur perforation." Bombus
terrestris bumble bees behave in a similar manner on Corydalis cava, first
foraging for pollen in a flower, then climbing outside the flower to rob nectar
(Olesen 1996). Koeman-Kwak (1973) also noted this pattern of pollen
collector-nectar robber. Bombus terrestris and B. jonellus first foraged for
pollen while hovering beside the Pedicularis palustris flower, and then landed
on the flower to rob the nectar. Flowers were pollinated during this process,
and "the seed production rate of flowers pollinated in this manner was
comparable to that of flowers pollinated by legitimate collectors"
(Koeman-Kwak 1973).
Morris (1996) studied the
behavior of two pollen collector-nectar robbers, Bombus mixtus and B. frigidus.
These humble bees would visit Mertensia paniculata flowers in their young (lst
day), pink, pollen-- producing stage to collect pollen, and visit the older (3rd-5th
day), blue, nectar-producing flowers as nectar robbers. Individual bumble bees
switched frequently between nectar robbing and pollen collection. Morris
postulated that the nectar reward in the blue flowers may act as a key
enticement to robbers, "which then enhance plant reproduction by
legitimately visiting early-stage flowers."
Some nectar robbers do not
bite holes in a flower's corolla. These "secondary nectar robbers"
collect nectar through holes made by previous visitors. Honey bees (Apis mellifera)
often behave as secondary nectar robbers. Rust (1979) observed that,
"During nectar foraging an individual A. mellifera might steal nectar from
several cut spurs then switch and enter the saccate sepal for nectar, only to
switch back to robbing after several pollinating visits." It is likely
that these bees, too, are both robbers and pollinators.
These examples are of
individuals that both rob and pollinate, sometimes simultaneously, and in other
cases as separate activities, but in all cases, an individual bee may do both.
In other cases, however, individual bees of the same species may only rob
nectar, or only visit a flower legitimately and pollinate. Individual honey
bees and bumble bees tend to specialize in both their choice of flowers and in their
foraging tactic on those flowers (Heinrich 1976, Waser 1986, Villalobos and
Shelly 1996). The most common explanation of this specialization is that an
early learned behavior that is successful tends to be repeated to the exclusion
of other behaviors. The species, then, could be considered as both a robber and
a pollinator, even though the individuals of that species may behave as only
one or the other. For instance, the bumble bee Bombus terrestris robs the
flowers of red clover, but Bombus terrestris can also be the most effective
pollinator of the crop (see Hawkins 1961, Free 1970). Bumble bee colony growth
is dependent upon the rate of food intake (Oster 1976) so it is likely,
although never tested, that robbers will contribute to the success of the
colony by their collection of nectar. A successful colony will produce more
bees, and if a certain percentage of these bees behave as legitimate
pollinators, then a plant with a long blooming period could, in theory, benefit
from the robbers.
FIG. 2.
WHAT TYPE OF ORGANISM IS
THE ROBBER?
It is interesting to note
that almost all of these cases of robber-like pollinators involve bees. Most,
but not all, of the pollination by robber bees is a result of the collection of
pollen, an important food source for developing larvae. Carpenter bees or
bumble bees were the robbers in 11 of the 12 studies that showed neutral or
positive effects on seed set due to robbers (Table 3).
Trigona bee robbers, on the
other hand, are always associated with negative effects on seed set (Table 3),
perhaps because of their aggressive, territorial nature. Trigona bees have been
known to chase away hummingbird pollinators, thus causing reduced seed set
(Roubik 1982). Due to their small size, and the structure of the flowers they
rob, it may take an individual Trigona bee up to 20 min to make a robbing hole;
this investment of time may be the reason for their territoriality.
Because the ability of
other types of robbers to pollinate has rarely been tested, it is unclear
whether bee robbers should be considered as unique or typical, but most birds
do not deliberately collect pollen, and so may be less likely to pollinate.
DOES THE ROBBER CHANGE THE
BEHAVIOR OF THE LEGITIMATE POLLINATOR?
In addition to, or perhaps
instead of, directly pollinating flowers, robbers may influence plant fitness
by changing the behavior of the legitimate pollinators (Heinrich and Raven
1972). Indirect effects (the effect of one species on another that occurs
through mutual interactions with a third species) such as this have been shown
to have substantial ecological consequences (Miller and Travis 1996).
Bumble bees fly longer
distances after visiting a plant low in nectar (as could occur in the presence
of robbers) and shorter distances after visiting a plant rich in nectar (Pyke
1978b, Waddington 1980, Heinrich 1983, Marden 1984, Zimmerman and Cook 1985,
Kadmon and Shmida 1992). Also, when nectar volumes drop below a certain
threshold, pollinators visit fewer flowers per inflorescence (Pyke 1982, Hodges
1985). A consequence of this change in pollinator behavior due to decreased
nectar volume could be more outcrossed pollination and higher fitness. Table 4
summarizes the possible behavioral changes in pollinators caused by nectar
robbers. The behavioral changes, and their consequences, will be discussed.
Changing the flight
distance of the pollinators
Longer pollinator flight
distances generally translate into increased pollen flow and increased
outcrossing rates (Gliddon and Saleem 1984, Fenster 1991). Many experiments
show that outcrossing leads to increased seed set and improved survival rates
of seedlings (e.g., Charlesworth and Charlesworth 1987, Fenster 1991, Husband
and Schemske 1996). If nectar robbers are the cause of longer flight distances
by the legitimate pollinators, they could be increasing the fitness of the
robbed plants by promoting outcrossing. The robbers could then be considered
mutualists. Zimmerman and Cook (1985) tested one component of this hypothesis.
They artificially robbed some flowers of Impatiens capensis by making a hole in
the nectar spur of the corolla and removing nectar with a syringe. The robbed
patch generated a greater frequency of long-distance bee flights, and the
authors concluded that pollen was transported greater distances, resulting in a
greater neighborhood size (sensu Wright 1969) in the robbed patch. In a first
test of this hypothesis on naturally robbed plants, bumble bees visiting robbed
patches flew longer distances between inflorescences (Maloof 2000).
The tropical hummingbird
Lampornis clemenciae feeds by traplining. When nectar-robbing birds (Diglossa
baritula) remove nectar from flowers, the hummingbirds must increase their
foraging area to gather the nectar they need (Hernandez and Toledo 1979).
Hernandez and Toledo conclude, "therefore, we must consider that robbers
may have a positive effect on this plant species [Erythrina leptorhiza]."
Changing the number of
flowers visited by the
pollinators
Robbers may also increase
outcrossing by creating conditions that cause legitimate pollinators to visit
fewer flowers on the same inflorescence. Bumble bees almost always work upward
on vertical inflorescences, visiting multiple flowers and departing when food
rewards fall below a critical threshold (Heinrich 1983, Hodges 1985).
Hummingbirds also leave an inflorescence when nectar rewards drop below a
certain threshold (Pyke 1978a). Visiting multiple flowers on the same plant may
lead to geitonogamy (the pollination of flowers by pollen from other flowers on
the same plant), which can have numerous deleterious effects on reproductive
success (de Jong et al. 1993). If nectar rewards are reduced by robbers, the
legitimate pollinators may depart the inflorescence sooner, thus reducing
geitonogamy and increasing the pollen dispersal distance (Klinkhamer and de
Jong 1993). This is especially important in plants that are self-fertile and
have many flowers on an inflorescence. Hodges (1995) found that individual hawk
moths visited more flowers on plants that contained more nectar, and that the
increased visitation resulted in increased selfing rates.
TABLE 4.
Changing time spent per
flower by pollinators
Besides changing flight
distances and the number of flowers visited by pollinators, nectar robbers may
change the amount of time spent by pollinators in each flower. Greater amounts
of nectar result in longer visits, and longer visits may result in greater
deposition of pollen (Thomson and Plowright 1980, Feinsinger 1983, Lanza et al.
1995, but see Mitchell and Waser 1992). How do nectar robbers figure into this
equation? It is clear that they reduce nectar levels (e.g., McDade and Kinsman
1980, Zimmerman and Cook 1985, Maloof 1999), and therefore shorten the length
of a visit (Zimmerman and Cook 1985, Thomson 1986), potentially resulting in
less pollen deposition on the stigma. Pollen deposition is related to both male
and female fitness, so it would seem that the robbers are having a detrimental
effect on the plant. One benefit of the pollinator spending a shorter time in
each flower, however, is that more flowers are visited per unit time (Cruden et
al. 1983). This could be beneficial for the plant if it causes a greater
percentage of flowers to be visited than would be visited otherwise.
Flying longer distances
between inflorescences, visiting fewer flowers per inflorescence, and visiting
more flowers per unit time all have the potential to increase pollen flow, if
the total number of visits is not reduced. The critical question then becomes:
do nectar robbers reduce the number of visits from legitimate pollinators?
There has been very little experimental work on this question, and thus far,
the results appear mixed. The response from the legitimate pollinator appears
to depend upon the identity of the pollinator, the amount of nectar left in the
flower by the robber, and the availability and quality of alternate food
sources. Each of these will be examined.
WHAT IS THE IDENTITY OF THE
LEGITIMATE
POLLINATOR(S)?
If a pollinator can tell
from a distance that a flower has been robbed, it is reasonable to assume that
the pollinator might avoid the flower because of lower expected nectar reward.
Thus, the behavior of a pollinator in the presence of nectar-robbed flowers
would be dependent upon the sensory capabilities of the pollinator. Rust (1979)
found that Bombus vagans and B. impatiens bumble bees (legitimate pollinators
of Impatiens capensis) "do not discriminate between robbed and unrobbed or
even experimentally nectarless flowers." We found a similar lack of
discrimination in Bombus appositus bumble bees visiting robbed and unrobbed
patches of Corydalis caseana flowers (Maloof 2000). Likewise, Goulson et al.
(1998) found that "bumblebees could not detect the nectar levels in
inflorescences that had not been visited, and so readily accepted inflorescences
that had been depleted of nectar artificially. Thus they are unlikely to be
using either direct vision of nectar, detection of humidity gradients, or
nectar scent to discriminate between inflorescences." Despite the bumble
bees' inability to determine nectar levels visually, there is some evidence
that bumble bees can distinguish between rewarding and nonrewarding flowers of
the same species (see Goulson et al. 1998). It appears that this discrimination
ability is the result of scent marks left on the flowers by previous bee
visitors. This area of research is in its infancy and, to date, no studies have
been done concerning the type of scent marks, if any, left by nectar-robbing
bumble bees. In a study by Richardson (1995), honey bees (Apis mellifera) avoided
Chilopsis linearis flowers robbed by carpenter bees (Xylocopa californica), but
bumble bees (Bombus sonoris) did not. It is unknown whether the divergence in
behavior of the bees reflects a difference in response to scent marking or
sensory capabilities.
There is no evidence that
butterflies avoid flowers robbed by Trigona bees (Barrows 1976). On the other
hand, there is some evidence that hummingbirds may be able to determine the
nectar status of flowers visually prior to visiting (Gass and Montgomerie
1981). One study has shown that hummingbirds visit more flowers in lightly
robbed patches than in heavily robbed patches (Irwin and Brody 1998). This
could be due to hummingbirds leaving the robbed patches because of low nectar
levels, or staying in a patch where the first visits were highly rewarding, but
the possibility exists that hummingbirds are able to determine which flowers
have been robbed before they visit. In five of the six studies in which nectar
robbing was shown to have a negative effect on fruit set, the legitimate
pollinators were hummingbirds (Roubik 1982, 1989, Roubik et al. 1985, Traveset
et al. 1998, Irwin and Brody 1999). In most cases, the reduced fruit set was
caused by reduced visitation rates, whereas in one case (Traveset et al. 1998),
it was probably caused by damage to the flowers from robbers.
How MUCH NECTAR is LEFT BY
THE ROBBER?
The nectar-removing
capabilities of the robber may strongly influence the subsequent behavior of
the legitimate pollinators, and hence affect the ultimate outcome for the
plant. In one study, in which almost 100% of the nectar was removed from
Justicia aurea flowers by robbers, the legitimate hummingbird pollinators
almost entirely ceased visiting. This clearly had a negative effect on
reproductive success. However, in another species, Aphelandra golfodulcensis,
the robbers left behind -4 (mu)L of nectar and hummingbird pollinators
continued to visit (McDade and Kinsman 1980). As the authors of that study
note, "These two different responses would result in decreased or
increased reproductive success, respectively." Increased reproductive
success might be expected in the case of Aphelandra golfodulcensis because the
legitimate pollinators were able to extract the nectar remaining after a robber
visit, but they had to visit more flowers to fulfill their energy requirements.
Bumble bee (Bombus
occidentalis) robbers on Corydalis caseana flowers leave behind an average of
20% of the original nectar volume (Maloof 1999). That may explain why
pollinator-dependent fruit set remains high (>80%) even though the flowers
are commonly (40-80%) nectar robbed.
WHAT OTHER RESOURCES ARE
AVAILABLE TO THE POLLINATOR
If pollinators are able to
determine whether or not flowers have been robbed, there are four possible responses:
(1) visit more flowers of the same species, indiscriminately, to get the
necessary nectar volume; (2) avoid those flowers that have been robbed, but
visit unrobbed flowers of the same species; (3) switch to pollen collection; or
(4) switch to species with higher rewards (see Table 4).
Switching would be possible
only if there are other flowers nearby with adequate nectar that could be
efficiently handled by the pollinator. Bumble bees may avoid switching because
learning new flowers, especially complex ones, requires an investment of time
(Laverty 1994) and there are costs involved in switching (Chittka and Thomson
1997). For butterflies, also, switching is avoided because of the learning
costs (Lewis 1989). Another, infrequently discussed, reason for not switching
is the variation in nectar chemistry, such as the amino acid content of various
nectars (Baker et al. 1978). Nectar from a particular flower may contain an
essential amino acid and, for that reason alone, a pollinator may remain
constant despite the presence of nectar robbers and low nectar volumes.
Additionally, nectar from robbed flowers may have higher concentrations of
amino acids due to diffusion from damaged tissues (Camargo et al. 1984).
More research is needed to
determine what conditions cause pollinators to switch species and how often, if
ever, nectar robbers are responsible for that switching. More research on
pollinating birds, in particular, would be useful.
EVOLUTIONARY IMPLICATIONS
Flower morphology
It is generally agreed that
legitimate pollinators may direct flower evolution by selecting for certain
shapes and colors (in addition to other traits), but the role of nectar robbers
as agents of selection on flower morphology is a promising field of study that
has virtually been ignored. If robbers have fitness effects on plants, whether
positive or negative, then they, too, may be operating as selective agents,
influencing which colors, shapes, etc., will be the most successful. In
general, flowers with long corolla tubes and nectar spurs are the ones most
likely to be robbed. The traditional view on this observation is that the long
corollas and flower spurs are selected for because they result in increased
pollen deposition on stigmas from the restricted suite of long-tongued
legitimate pollinators (Nilsson 1988); robbers simply bypass these structures
because they cannot reach the nectar any other way (Soberon and Martinez del
Rfo 1985). However, if corolla tube length and spur length, beyond some minimum,
do not affect the nectar robbers adversely, but may affect the legitimate
pollinators adversely because of constraints on proboscis or bill length, then
there may be selection on corolla morphology from the robbers. This selection
could be mediated either through the direct effects that robbers have on plant
fitness (such as pollination), or through the indirect effects that robbers
have on plant fitness by causing changes in pollinator behavior.
For instance, if a local
deme of legitimate pollinators could not reach the nectar in the bottom of a
long nectar spur, it would be logical for them to forage on a different
species, at least until nectar accumulated to a level that they could reach.
But if, in this same location, there were robbers that could get to the nectar
in the bottom of the spur, then the nectar would never accumulate to a level
accessible to the pollinators. Now suppose that these nectar robbers also
collected pollen from the flowers and pollinated in the process (as we have
mentioned earlier, bumble bees are often robber-- like pollinators). In such a
case, the robber would be the agent of selection and, most likely, there would
be positive, or at least neutral, selection for long corollas or nectar spurs,
because long corollas do not prevent robbers from collecting nectar or
pollinating. In fact, if the robbers were discriminating about which flowers
they visited, they would most likely choose those with the longest corolla
tubes, whose nectar was least available to the legitimate pollinators. Roubik
et al. (1985) found that Quassia amara corolla lengths were longer in
populations that were robbed than in an isolated population that had no
robbers. This connection between corolla length and robbers is intriguing and
should be studied further. Ocotillo (Fouquiera splendens) flowers, like many
others, exhibit large geographic variations in morphology (Henrickson 1972).
Waser (1979) believes that some of this variation may be due to evolutionary
adaptations that allow robber-pollinators, such as carpenter bees, to pollinate
in the process of nectar collection.
Flower location
Traveset et al. (1998)
found that nectar-robbing birds (Phrygilus patagonicus) were more likely to rob
Fuchsia flowers growing in a open area. These birds sometimes damaged a
flower's ovary while robbing; consequently, flowers in open areas exhibited
reduced seed set. Plants growing in the forest, on the other hand, had higher
seed set because they were more likely to be visited by the legitimate
pollinator, a hummingbird. This combination may be selecting for plants that
are shade tolerant. In another case, involving hummingbird pollination of
shrubby Centropogon valerii, the nectar-- robbing bird (Diglossa plumbea)
foraged mostly on the inner and lower flowers (Colwell et al. 1974). The
researchers noted that fruit set was lower on these inner and lower flowers
(although this was not documented) and suggested that selection might favor
plants that produce flowers only in the upper and outer part of the shrub. In
these two examples, the robbers are exerting selection against genotypes likely
to be robbed, but there may be other instances in which robbers increase plant
fitness and therefore exert positive selection.
Nectar volume
If a plant is robbed of
nectar, yet a certain volume of nectar is needed to keep the most effective
pollinators as constant visitors, then those plants, or populations, producing
enough nectar for both robber and pollinator will be the most successful in
fitness terms, and will leave the most progeny, leading to increased nectar
production. In the terminology used by Pyke (1981), optimal rates of nectar
production should be higher in the presence of nectar robbers. Barrows (1976)
wrote that, "coevolution of Lantana camara, its pollinators, and its
nectar robber, Trigona fulviven-- tris, has probably involved increased nectar
production to feed both its pollinators and its robbers." Others have
repeated the assumption that nectar production should be higher in heavily
robbed populations (Soberon and Martinez del Rfo 1985, Morris 1996), but the
only test of this idea was done by Roubik et al. (1985). They studied four
different populations of Quassia amara, some that were robbed and others that
were unrobbed. The flowers protected from visitors in an area of heavy robbing
contained an average of 45.3 iL of nectar, whereas the flowers in an area
without nectar robbers contained an average of 30.8 liL of nectar. One
explanation of this observation is that plants in heavily robbed areas may have
evolved increased nectar production, but further work should be done before
this conclusion is accepted, as alternatives are possible (e.g., robbers
preferentially use plants with higher nectar production).
Protective mechanisms
If nectar robbers had
consistently negative effects on plant fitness, we would expect protective
mechanisms to evolve. It is sometimes suggested that plants have evolved
protection mechanisms (e.g., thickened calyces, dense inflorescences, latex
sap, extrafloral nectaries; see Guerrant and Fiedler 1981, Inouye 1983, and
references therein), but to our knowledge, none of these suggestions has been
rigorously tested.
The plant genus that we
study (Corydalis) occurs throughout North America, Europe, and Asia. It is
apparently robbed throughout most of its range (Higashi et al. 1988, Olesen
1996; J. E. Maloof, personal observation), yet no protective mechanisms are
evident. More research is needed to link variations in these putative
protective mechanisms with variations in robbing rates and, ideally, plant
fitness effects, before we can assume that traits have evolved to protect
against nectar robbers.
DISCUSSION
Are nectar robbers cheaters
or mutualists? One thing we know for certain is that they cannot be assumed to
be one or the other. Mutualists benefit each other. The benefit to nectar
robbers from flowers seems obvious: they are an important, sometimes the sole,
source of food (Scott et al. 1993). As we have shown, there may also be
benefits to flowers from nectar robbers. These benefits may be direct (in the
case of "robber-like pollinators") or indirect (mediated through a
third species). Indirect benefits, especially, may be overlooked because of
their subtlety or complexity. Some patterns are beginning to emerge and the conclusions
listed here are just a beginning in our understanding of the complex ecology of
nectar robbing.
1) It should not be
automatically assumed that nectar robbers are not pollinating the flowers they
visit. In many cases, nectar robbers are pollinators, too.
2) The effects of nectar
robbers are complex and depend, in part, on four factors.
a) The identity of the
legitimate pollinator. Hummingbirds may be able to sense and avoid robbed
flowers, but insects may not. Hummingbirds do not collect pollen from plants as
a food source; bees do, and pollen transfer (pollination) may occur as a result
of this behavior.
b) The growth form of the
plant. Geitonogamy may be detrimental to a plant, and could become a problem if
there are many open flowers on an inflorescence. Nectar robbers may reduce
geiton-- ogamy by changing foraging patterns.
c) How much nectar robbers
remove. If robbers remove all of the nectar, the legitimate pollinators may
switch; if robbers leave some nectar behind, the legitimate pollinators may remain
constant.
d) Resources available in
the environment. If there is a scarcity of alternative nectar sources, the
pollinators may be more likely to remain constant. Amino acid content of a
nectar may also influence pollinator behavior.
3) Nectar robbing is a
common phenomenon that may have evolutionary implications.
4) Evidence to date shows
that robbers are often, but not always, mutualists.
We hope that this review
will stimulate a new perspective on nectar robbing, an appreciation of its
ecological and evolutionary complexities, and additional research into its
consequences. We have emphasized bees as nectar robbers because of our own
experience and the predominance of literature on bees as robbers, but the
differences between bee- and bird-pollinated and robbed flowers suggest that
additional work on robbers other than bees would be profitable.
ACKNOWLEDGMENTS
We thank Nickolas Waser,
James Thomson, Jeff Ollerton, and Jon Agren for their helpful comments on
earlier versions of this manuscript, and Earthwatch and its Research Corps, and
NSF grant IBN-98-14509, for funding. The Rocky Mountain Biological Laboratory
and Gunnison National Forest provided access to laboratory facilities and study
sites.
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JOAN E. MALOOF1,2.3,4 AND
DAVID W. INOUYE2'3
1Salisbury State
University, Department of Biological Sciences, Salisbury, Maryland 21801 USA
2Department of Biology, University of Maryland, College Park, Maryland 20742
USA 3Rocky Mountain Biological Laboratory, P.O. Box 519, Crested Butte,
Colorado 81224 USA
Manuscript received 11
March 1999; revised 16 December 1999; accepted 30 December 1999; final version
received 29 January 2000.
4 Address for
correspondence: Salisbury University, Department of Biological Sciences,
Salisbury, Maryland 21801 USA. E-mail: jemaloof@salisbury.edu