Pollination of plants by disease vectors: An assessment
Woodbridge A. Foster
Medical Entomologist and Insect Ethologist
Department of Evolution, Ecology & Organismal Biology, and Department of Entomology
The Ohio State University
Mosquitoes of both sexes ingest sugar from a variety of sources: flower nectar, extra-floral nectaries, hemipteran honeydew, overripe fruit, damaged plant tissue and seed pods, and even sap from undamaged plant parts in some cases.
Because they sometimes contact anthers and stigmas when extracting flower nectar, they may acquire either pollen grains or pollinia (pollen packets) on their bodies. By this means they can transfer pollen between anthers and stigmas on the same flower, on different flowers of the same plant, or on different plants that they visit.
Pollen transfer is biologically meaningful only between flowers of the same plant species. Plants that require this transfer, by whatever mechanism, will not set seed or develop fruit without it. Aside from wind, by far the most common pollinators are insects, so all species of insects that visit flowers, of which there are hundreds of thousands—either for their nectar or for excess pollen—are possible pollinators. Mosquitoes conceivably are among them. However, among the many studies of flower-mosquito associations, pollination has been inferred in a few cases, but rarely demonstrated. More often, the issue is never raised or addressed.
…among the many studies of flower-mosquito associations, pollination has been inferred in a few cases, but rarely demonstrated.
The hallmarks of good potential pollinators:
- visit flowers frequently and can pick up and deposit pollen,
- move among different individual plants frequently during a bout of foraging (vagility),
- specialize in visiting one or a few plant species (monolexy or oligolexy) during a single foraging bout (flower constancy). The most efficient pollinators exhibit flower constancy, so that pollen is not widely distributed among other plants where it would have no function.
- visit reproductive parts of the flowers and not extra-floral nectaries, leaves or stems,
- flowers are visited by only one or a few other potential pollinators, such that the plant is reliant on those particular pollinators, which in turn are likely to visit many different species of plants .
At one extreme are specialist flower visitors whose mouthparts or sensory abilities allow them to find and feed on the nectar only of one or a few plant species to which those specialists are adapted through evolved or co-evolved tactics. For example, the bee Hesperapis oraria only forages on Balduina angustifolia. Such close relationships are rare among mosquitoes, whose relatively short proboscises cannot access the nectar in long corollas or other specially configured flower structures. Narrowly targeted flower odors and the daily timing of nectar flow also can be exclusionary factors for mosquitoes (see below).
Flower constancy is sometimes behavioral, for example honey bees, which tend to concentrate on one plant species during each foraging trip. Constancy also may be incidental if, for example, large numbers of plants are in bloom in the same place at the same time. Plants can take advantage of mosquitoes for pollen transfer in these situations.
Accounts of associations between particular species of plants and the mosquitoes that visit their flowers have been reviewed by Peach & Gries (2016). The best documented of these relationships involve specific floral odors and structures that facilitate attraction and pollination for a narrow assemblage of insects. In a few cases this includes female mosquitoes. The best known are the ground orchids (Platanthera spp.) of northern North America and Spanish catchfly (Silene otites) of northern Europe (e.g.,Stoutamire 1968, Thien & Utech 1970, Brantjes & Leemans 1976, Lahondère et al. 2020), which are visited by a few culicine mosquitoes. Odor specificity as narrow as a single chemical (lilac aldehyde) holds true for hte ground orchid Platanthera obtusata and its Aedes spp. pollinators (Lahondère et al. 2020). In the Aedes-orchid relationship, the pollinia become attached to the mosquitoes’ heads. Even in some of these special cases, however, small moths appear to be more effective pollinators most of the time, either because of the greater length of their proboscises or more frequent movement among different flowers and different plants.
At the other extreme are the generalist (polylectic) flower-visiting insects that obtain nectar from plants with unspecialized (generalist syndrome) flowers. Such plants can achieve effective pollination only by inviting large numbers of a great variety of insects, including bees, wasps, butterflies, moths, and beetles. Most of the pollen that they pick up and then transfer to other flowers of various plant species is wasted unless one plant species is highly aggregated in space and time, yet genetically diverse, to promote cross fertilization. Such generalist plants typically produce large clusters of flowers or florets that have short or very short corollas and yield only small amounts of nectar, inducing the insects to move frequently over the flower cluster and between plants. Species in the plant family Asteraceae are typical examples.
Most evidence indicates that nearly all plants visited by mosquitoes fall into the generalist category. The flowers visited by mosquitoes are also visited by many other insects, indicating that mosquitoes likely would be minor pollinators. But this does not preclude their playing a role in the process. Pollen grains from various plant species frequently occur on the bodies of culicine mosquitoes (e.g., Kevan 1972), and these plants often are aggregated, offering a degree of flower constancy. Attraction to a flower, however, is seldom an indicator of a pollinator.
For example, the common pest mosquito Aedes vexans is strongly attracted to the odor of the common milkweed, Asclepias syriaca, in eastern North America and readily feeds on the nectar of its florets (Foster unpubl.). But it is incapable of detaching its pollinia and therefore cannot deliver them to another flower, pollinating functions performed by heavy-bodied insects such as bumble bees. Such cases of nectar thievery are common among flower visitors that provide no pollinating services (Inouye 1980, 2010, Kevan & Baker 1983, Peach & Gries 2016). The same is true of nectar robbers, which damage flower structures in the process, thereby allowing mosquitoes access to nectar, but again without pollinating.
Experimental demonstrations of successful mosquito pollination of either specialist or generalist flowers are rare. Two of them are the studies of Silene otites by Brantjes & Leemans (1976) and Platanthera obtusata by Lahondère et al. (2020) in northern latitudes. Direct observations and bagging experiments (covering flowers to control access by pollinators) in these and similar studies have not always been exacting, but these two studies provide convincing evidence of pollen transfer by mosquitoes from male to female floral structures and subsequent seed set. Peach & Gries (2016) conducted a rigorous series of experiments that focused on tansy (Tanacetum vulgare) inflorescences in Canada, an invasive generalist species of European origin in the family Asteraceae. They showed in the laboratory that Culex pipiens was capable of significant cross pollination of tansy leading to successful seed set. Pollen grains of the same general type were found on the bodies of field-caught Cx. pipiens. Despite this experimental demonstration of successful pollination and field inference for pollination of tansy by Cx. pipiens, this and other mosquito species were found visiting not only tansy but also other plant species in the same area. Furthermore, tansy, which like most Asteraceae, has generalist-structured flowers, was visited by a plethora of other insects, including a diversity of flies, bees, wasps, ants, lepidopterans, beetles, bugs, lacewings, and earwigs, several of which appear to be potential pollinators.
In conclusion, even in northern temperate, subarctic, and arctic regions, evidence is not strong that mosquitoes are essential pollinators, though they can play a significant or at least minor role. However, in those few especially close mosquito-flower associations, they certainly at least play a very important secondary role.
Among tropical mosquito vectors of disease, our information on even possible pollination is quite meager. What we do know mostly weakens the case for their roles as pollinators.
Their attraction to flowers or other plant parts in sub-Saharan Africa is now well documented by several studies (e.g., McCrae, et al. 1969, 1976, Müller et al. 2010, Gouagna et al. 2010, 2013), yet direct observations of the frequency of visits to, and utilization of, these plants in the field have received scant attention.
Thus, it is not always clear that the object of attraction and feeding was the flowers themselves. Gouagna et al. (2010,2013) and Müller et al. (2010) investigated sugar-feeding and potential host-plant preferences of the malaria vectors Anopheles gambiae and An. arabiensis under laboratory, semi-filed and field conditions involving many species of plants during their flowering phase in Burkina Faso, Mali, and La Reunion. Several of the plants identified as potential nectar sources in these studies have flowers with nectaries apparently accessible to mosquitoes, or related plants that have been implicated previously, but without behavioral confirmation. In Gouagna et al (2010, 2013) the choices of floral cuttings for use in attraction tests using an olfactometer were based on the proximity of fructose-positive males to the suspected plants or by the plants’ abundance near mosquito breeding sites (15 species of plants in all).
The most attractive and productive flowers were from plants are known to be visited and pollinated by bees, wasps, butterflies, large flies, and thrips. Unfortunately, neither in the field nor the laboratory were the mosquitoes observed feeding on any of these flowers or other plant parts, some of which are known to have glands producing extra-floral nectar.
As a lesson in caution when making conclusions based on attraction, flowering Acacia macrostachya has been demonstrated to be among the most attractive of many flowering plants to An. gambiae s.l. (Müller et al. 2010). Yet, direct field observations overnight on this acacia during its flowering season revealed that all feeding by mosquitoes of several species, including An. gambiae, occurred on extra-floral nectaries on the acacia’s leaves, not on its flowers whose nectaries are accissible to mosquitoes (A. McCrae pers. comm.).
If this observation is confirmed, one may conclude that despite A. macrostachya great attractiveness to mosquitoes, mosquitoes appear to play no role in its pollination. One notable case of direct observations of flower feeding is Harungana madagascarensis (Hypericaceae) in Uganda (McCrae et al. 1976), which was visited by large numbers of both sexes of An. implexus, a species of no medical importance, as well as other mosquito species during its brief blooming season. However, their role in pollination, if any, is unknown.
McCrae’s conclusion (pers comm.) that most mosquitoes in Africa utilize extra-floral nectar, and perhaps honeydew and damaged leaves, was confirmed by me and colleagues (Foster et al. unpubl). Our direct field observations of An. gambiae s.l. and other mosquito species at night in western Kenya, and also in cage and mesocosm experiments with invasive and native Kenyan plants, indicated that extra-floral nectaries and honeydew were their main sugar sources (Stone et al. 2012, Ebrahimi et al. 2017, Foster et al. unpubl. obs.), which are not connected to pollination. An exception could be Lantana camara, whose florets mosquitoes will probe, despite appearing to be unable to reach the nectar. Butterflies are considered to be L camara’s main pollinators. Instead, nectaries in the calyces under the inflorescences may be the source of their sugar (see Nikbakhtzadeh et al. 2016, Foster unpubl.)
Two well-executed recent investigations have demonstrated the utilization of local plant species by disease vectors in western and eastern Africa (Müller et al. 2017, Nyasembe et al. 2018, respectively). Müller et al. (2017) recorded a profound drop in population density of An. gambiae s.l. following experimental removal of flowering branches of the invasive species Prosopis juliflora, evidence for a strong likelihood of flower constancy and nectar dependence at the time of the experiment. The apparent constancy is likely a result of its high attractiveness and the paucity of competing sources of nectar in an arid region of Mali during the dry season.
The work of Nyasembe et al. (2018) was especially useful in showing that Ae. aegypti (a vector of dengue, yellow fever, zika, and chikungunya viruses) and An. gambiae s.l. (a vector of malaria) under natural conditions utilized at least three and five plant species, respectively, in two localities in Kenya. Host-plant identification was based on matches to nucleotide sequences of targeted plant genes found in the DNA isolated from mosquitoes that had recently fed on nectar as evidenced by the presence of fructose.
Three plant species were identified using DNA sequence analysis of nectar-fed Ae. aegypti adults (Hibiscus heterophyllus, Senna uniflora, Pithecellobium dulce), and these have flowers visited by birds, butterflies, bees, and other insects. While floral visits to these plants by mosquitoes have not been reported, Hibiscus heterophyllus and Senna uniflora have extra-floral nectaries used by mosquitoes (Foster unpubl.). ,
Using DNA sequence analysis of nectar-fed An. gambiae s.l. adults, five species of plants were identified: Ricinus communis, Senna alata, Senna tora, Leonotis nepetifolia, and Parthenium hysterophorus. Ricinus communis, Senna alata, Senna tora, are known to provide nectar to mosquitoes only from extra-floral nectaries or possibly honeydew from planthopper infestations (Foster, unpubl). Ricinus is generally self-pollinating or wind-pollinated, but bees can achieve cross-pollination. Senna spp. flowers, generally, are structured for nectar feeding and pollination by bees, though the flowers of some species conceivably could be visited by mosquitoes as well.
Leonotis nepetifolia has deep corollas with nectar inaccessible to mosquitoes, and in Africa where it is native, it is pollinated by sunbirds. Mosquitoes are able to extract sugar from the calyces of dehisced flowers (Foster unpubl.), a source unlikely to be connected to pollination at that stage. By contrast, Parthenium hysterophorus has small white composite flowers typical of generalist-pollinated plants, its odor is attractive to An. gambiae s.s. (Nyasembe et al. 2012, Nikbakhtzadeh et al. 2014), and its body often bears pollen grains after it has been probing P. hysterophorus flowers (Foster unpubl.). This plant is such a prodigious source of pollen for honey bees in India that it is considered a valuable resource for bee hives when other sources of pollen are not available, despite its many negative features (see below). Therefore, it is a reasonable candidate for anopheline and culicine pollination. Unfortunately, no flower-visitor or pollination studies have been conducted on any of the vectors’ plant hosts identified by Nyasembe et al. (2018).
One irony of these African studies is that the plant species whose blossoms or extra-floral nectaries mosquitoes most frequently visit are destructive, invasive, pest plants (Stone et al. 2018). Parthenium hysterophorus and Prosopis juliaflora, two exotic species whose flowers are very attractive to An. gambiae (Nyasembe et al. 2015, Müller et al. 2017, respectively), are notorious examples. Parthenium chokes agricultural fields and native plant communities, is toxic to livestock, and has been proposed to promote malaria transmission (Nyasembe et al. 2015). Prosopis enhances anopheline malaria-vector populations, displaces native plants, is toxic to livestock, and makes land unusable. Pithecellobium dulce, one of the Ae. aegypti-utilized plants (Nyasembe et al. 2018) whose flowers conceivably might be visited by this mosquito, also is an invasive pest.
Another irony is that with few exceptions, the mosquitoes known to visit African and American nectar sources in large numbers are not Anopheles species that vector malaria or Aedes species that vector viruses of human disease, but rather a wide assortment of culicine species of mosquitoes.
Invasive plant species in Africa
In western Kenya, An. gambiae s.l. constitutes a small minority of those mosquito species visiting plants (Foster unpubl.). The same seems to hold true in Uganda and The Gambia (McCrae et al. 1969 and pers. comm.) (cf. An. implexus on Harungana, noted above), possibly simply because anopheline population densities typically are low—even in areas of holoendemic malaria. In addition, in both temperate and tropical regions, anophelines in general and aedines in the subgenus Stegomyia (including Ae. aegypti and Ae. albopictus) usually are the mosquitoes least likely to be found carrying recent nectar meals or to be seen on mosquito-attractive flowers or extrafloral nectaries (e.g., Sandholm & Price 1962, Bidlingmayer & Hem 1973, Grimstad & DeFoliart 1974, Beier 1996, Burkett et al. 1999, H. Manda et al. in prep, A. McCrae pers. comm., Foster unpubl.). This seems to be true both in tropical Africa and in Central and South America (Foster unpubl.).
One reason for the scarcity of observations of sugar feeding by the important vector species may be that An. gambiae, at least, digests its sugar meals much more quickly than culicine species (Gary 2005, H. Manda et al. in prep.). Another reason is that the females of the most notorious anthropophilic species appear to feed on sugar less frequently than most mosquitoes. These include both An. gambiae, one of the main vectors of malaria in Africa, and Ae. aegypti, the widely distributed vector of yellow fever, dengue, chikungunya, zika, and other arboviruses. They are extraordinarily efficient at converting a large portion of each human blood meal into stored energy (Briegel 1985, Fernandes & Briegel 2005), despite the metabolic cost of a high protein diet, which shortens life (Joy et al. 2010). Instead, they ingest blood frequently, making them more efficient transmitters of disease pathogens if they can survive past the duration of the pathogen’s extrinsic cycle. A consequence of this infrequent sugar feeding may be that they are among the mosquito species least likely to serve as contributing pollinators.
Could Mosquito Vectors of Disease Be Important Pollinators?
- Flower-visiting insects are the most important pollinators of plants. Disease-spreading mosquitoes sometimes visit flowers to obtain nectar, so conceivably they are among the hundreds of thousands of insect species that might play an important cross-pollinating role.
- Sugar feeding is ubiquitous among the ~3,500 species of mosquitoes. Even though females of the anthropophilic species gambiae s.l. and Ae. aegypti, the most important tropical and subtropical vectors of human disease, may feed on plant sugar only once per reproductive cycle, their males sugar-feed every 1-2 days. Thus flower visits may be common.
- Strong circumstantial evidence indicates that a few mosquito species in northern temperate and subarctic regions serve as important, if sometimes secondary, pollinators of a few specialized plants.
- Solid experimental laboratory evidence demonstrates that mosquitoes are capable of cross-pollination of one generalist plant species in temperate regions.
- Flowers of many plant species release volatile organic compounds that are attractive to multiple species of mosquitoes, either by themselves or in blends.
- The volatile organic compounds of most flowers almost always attract multiple species of mosquitoes and many other kinds insects that also may serve as pollinators. At the same time, the great majority of mosquitoes are not known to be plant-species specific and are attracted to the flowers of many different plants.
- The vast majority of flowers from which mosquitoes can extract nectar have characteristics (visual, structural, chemical) that also cause them to be visited by a variety of insects (e.g., bees, flies, butterflies, moths, beetles) that also appear to serve as pollinators.
- Mosquitoes obtain sugar from a variety of different non-floral sources, an activity that is not involved in pollination. Among them are extra-floral nectaries, honeydew, over-ripe and rotting fruit, injured-plant sap, and guttation fluids. Mosquitoes that do visit flowers also may utilize several of these other sugar sources, when available.
- Mosquito species that transmit human diseases, such as Anopheles gambiae and Aedes aegypti, with few exceptions, are a distinct minority of the mosquito species found visiting flowers or feeding on other sugar sources in the tropics and subtropics. Unlike most other mosquito species, these seldom carry recent sugar meals, except soon after emergence, suggesting infrequent sugar feeding.
- The plant species that currently appear most likely to depend on vector mosquitoes for their pollination in Africa, or at least might play a significant role in their pollination (despite our lack of evidence), are invasive pest species, such as Parthenium hysterophorus and Prosopis juliaflora. These plants spoil communities, ruin agricultural land, drive out native plants and insects, promote malaria transmission, and are targets for elimination by environmentalists.
Given all that we know, we must conclude that the elimination of these vectors will have either no direct effect on plant communities or will have a beneficial one.
So far, the great weight of evidence for tropical and subtropical Anopheles and Aedes vectors of disease as plant pollinators points in the opposite direction: they are, at best, likely to be extremely minor contributors to pollination. The most promising prospects for mosquito pollination in the tropics are plant species considered to be destructive aliens. Experimental evidence, and even circumstantial evidence, is lacking for any tropical vector’s role as a likely effective pollinator. Given all that we know, we must conclude that the elimination of these vectors will have either no direct effect on plant communities or will have a beneficial one.
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