|This article is written like a manual or guidebook. (June 2012)|
The mosquitoes are a family of small, midge-like flies: the Culicidae. Although a few species are harmless or even useful to humanity, most are a nuisance because they consume blood from living vertebrates, including humans. The females of many species of mosquitoes are blood eating pests. In feeding on blood, some of them transmit extremely harmful human and livestock diseases, such as malaria. Some authorities argue accordingly that mosquitoes are the most dangerous animals on Earth.
Mosquitoes are members of a family of nematocerid flies: the Culicidae (from the Latin culex, genitive culicis meaning "midge" or "gnat"). The word mosquito (formed by mosca and diminutive ito) is from the Spanish or Portuguese for "little fly". Superficially, mosquitoes resemble crane flies (family Tipulidae) and chironomid flies (family Chironomidae); as a result, casual observers seldom realise the important differences between the members of the respective families. In particular, the females of many species of mosquitoes are blood eating pests and dangerous vectors of diseases, whereas members of the similar-looking Chironomidae and Tipulidae are not. Many species of mosquitoes are not blood eaters, and many of those that do create a "high to low pressure" in the blood to obtain it do not transmit disease. Also, in the bloodsucking species, only the females suck blood. Furthermore, even among mosquitoes that do carry important diseases, neither all species of mosquitoes, nor or all strains of a given species transmit the same kinds of diseases, nor do they all transmit the diseases under the same circumstances; their habits differ. For example, some species attack people in houses, and others prefer to attack people walking in forests. Accordingly, in managing public health, knowing which species, even which strains, of mosquitoes with which one is dealing is important.
Over 3,500 species of mosquitoes have already been described from various parts of the world. Some mosquitoes that bite humans routinely act as vectors for a number of infectious diseases affecting millions of people per year. Others that do not routinely bite humans, but are the vectors for animal diseases, may become disastrous agents for zoonosis of new diseases when their habitat is disturbed, for instance by sudden deforestation.
Like all flies, mosquitoes go through four stages in their life cycle: egg, larva, pupa, and adult or imago. In most species, adult females lay their eggs in stagnant water; some lay eggs near the water's edge; others attach their eggs to aquatic plants. Each species selects the situation of the water into which it lays its eggs and does so according to its own ecological adaptations. Some are generalists and are not very fussy. Some breed in lakes, some in temporary puddles. Some breed in marshes, some in salt-marshes. Among those that breed in salt water, some are equally at home in fresh and salt water up to about one third the concentration of seawater, whereas others must acclimatise themselves to the saltiness. Such differences are important because certain ecological preferences keep mosquitoes away from most humans, whereas other preferences bring them right into houses at night.
Some species of mosquitoes prefer to breed in phytotelmata (natural reservoirs on plants) such as rainwater accumulated in holes in tree trunks, or in the leaf-axils of bromeliads. Some specialise in the liquid in pitchers of particular species of pitcher plants, their larvae feeding on decaying insects that had drowned there or on the associated bacteria; the genus Wyeomyia provides such examples — the harmless Wyeomyia smithii breeds only in the pitchers of Sarracenia purpurea.
However,some species of mosquito that are adapted to breeding in phytotelmata are dangerous disease vectors. In nature they might occupy anything from a hollow tree trunk to a cupped leaf. Such species typically take readily to breeding in artificial water containers, such as the odd plastic bucket, flowerpot "saucer", or discarded bottle or tire. Such casual puddles are important breeding places for some of the most serious disease vectors, such as species of Aedes that transmit dengue and yellow fever. Some with such breeding habits are disproportionately important vectors because they are well placed to pick up pathogens from humans and pass them on. In contrast, no matter how voracious, mosquitoes that breed and feed mainly in remote wetlands and salt marshes may well remain uninfected, and if they do happen to become infected with a relevant pathogen, might seldom encounter humans to infect in turn.
The first three stages—egg, larva and pupa—are largely aquatic. These stages typically last 5–14 days, depending on the species and the ambient temperature, but there are important exceptions. Mosquitoes living in regions where some seasons are freezing or waterless spend part of the year in diapause; they delay their development, typically for months, and carry on with life only when there is enough water or warmth for their needs. For instance, Wyeomyia larvae typically get frozen into solid lumps of ice during winter and only complete their development in spring. The eggs of some species of Aedes remain unharmed in diapause if they dry out, and hatch later when they are covered by water.
Eggs hatch to become larvae, that grow until they are able to change into pupae. The adult mosquito emerges from the mature pupa as it floats at the water surface. Bloodsucking mosquitoes, depending on species, gender, and weather conditions, have potential adult lifespans ranging from as little as a week to as long as several months.
Eggs and oviposition
Mosquito habits of oviposition, the ways in which they lay their eggs, vary considerably between species, and the morphologies of the eggs vary accordingly. The simplest procedure is that followed by many species of Anopheles: like many other gracile species of aquatic insects, females just fly over the water, bobbing up and down to the water surface and dropping eggs more or less singly. The bobbing behaviour occurs among some other aquatic insects, as well, for example mayflies and dragonflies; it sometimes is called "dapping". The eggs of Anopheles species are roughly cigar-shaped and have floats down the sides. Females of many common species of mosquito can lay 100-200 eggs during the course of the adult phase of their lifecycle. Even with high egg and intergenerational mortality, over a period of several weeks a single successful breeding pair can create a population of thousands.
Some other species, for example members of the genus Mansonia, lay their eggs in arrays, attached usually to the under-surfaces of waterlily pads. Their close relatives, the genus Coquillettidia, lay their eggs similarly, but not attached to plants. Instead, the eggs form layers called "rafts" that float on the water. This is a common mode of oviposition, and most species of Culex are known for the habit, which also occurs in some other genera, such as Culiseta and Uranotaenia. Anopheles eggs may on occasion cluster together on the water, too, but the clusters do not generally look much like compactly glued rafts of eggs.
In species that lay their eggs in rafts, rafts do not form adventitiously; the female Culex settles carefully on still water with her hind legs crossed, and as she lays the eggs one by one, she twitches to arrange them into a head-down array that sticks together to form the raft.
Aedes females generally drop their eggs singly, much as Anopheles do, but not as a rule into water. Instead, they lay their eggs on damp mud or other surfaces near the water's edge. Such an oviposition site commonly is the wall of a cavity such as a hollow stump or a container such as a bucket or a discarded vehicle tire. The eggs generally do not hatch until they are flooded, and they may have to withstand considerable desiccation before that happens. They are not resistant to desiccation straight after oviposition, but must develop to a suitable degree first. Once they have achieved that, however, they can enter diapause for several months if they dry out. Clutches of eggs of the majority of mosquito species hatch as soon as possible, and all the eggs in the clutch hatch at much the same time. In contrast, a batch of Aedes eggs in diapause tends to hatch irregularly over an extended period of time. This makes it much more difficult to control such species than those mosquitoes whose larvae can be killed all together as they hatch. Some Anopheles species do also behave in such a manner, though not to the same degree of sophistication.
Larvae breathe through spiracles located on the eighth abdominal segment, or through a siphon, and therefore must come to the surface frequently. The larvae spend most of their time feeding on algae, bacteria, and other microbes in the surface microlayer. They dive below the surface only when disturbed. Larvae swim either through propulsion with their mouth brushes, or by jerky movements of their entire bodies, giving them the common name of "wigglers" or "wrigglers".
As seen in its lateral aspect the mosquito pupa is comma-shaped. The head and thorax are merged into a cephalothorax, with the abdomen curving around underneath. The pupa can swim actively by flipping its abdomen, and it is commonly called a "tumbler" because of its swimming action. As with the larvae, the pupae of most species must come to the surface frequently to breathe, which they do through a pair of respiratory trumpets on the cephalothorax. However, pupae do not feed during this stage; typically they pass their time hanging from the surface of the water by their respiratory trumpets. If alarmed, say by a passing shadow, they nimbly swim downwards by flipping their abdomens in much the same way as the larvae do. If undisturbed they soon float up again. After a few days or longer, depending on the temperature and other circumstances, the pupa rises to the water surface, the dorsal surface of its cephalothorax splits, and the adult mosquito emerges. The lower activity of the pupa is as compared to the larva is understandable, bearing in mind that it does not feed, whereas the larva feeds constantly.
The period of development from egg to adult varies among species and is strongly influenced by ambient temperature. Some species of mosquitoes can develop from egg to adult in as little as five days, but a more typical period of development in tropical conditions would be some 40 days or more for most species. The variation of the body size in adult mosquitoes depends on the density of the larval population and food supply within the breeding water.
Adult mosquitoes usually mate within a few days after emerging from the pupal stage. In most species, the males form large swarms, usually around dusk, and the females fly into the swarms to mate.
Males typically live for about a week, feeding on nectar and other sources of sugar. After obtaining a full blood meal, the female will rest for a few days while the blood is digested and eggs are developed. This process depends on the temperature, but usually takes two to three days in tropical conditions. Once the eggs are fully developed, the female lays them and resumes host-seeking.
The cycle repeats itself until the female dies. While females can live longer than a month in captivity, most do not live longer than one to two weeks in nature. Their lifespans depend on temperature, humidity, and their ability to successfully obtain a blood meal while avoiding host defenses and predators.
Length of the adult varies, but is rarely greater than 16 mm (0.6 in), and weight up to 2.5 milligrams (0.04 grains). All mosquitoes have slender bodies with three segments: head, thorax and abdomen.
The head is specialized for receiving sensory information and for feeding. It has eyes and a pair of long, many-segmented antennae. The antennae are important for detecting host odors, as well as odors of breeding sites where females lay eggs. In all mosquito species, the antennae of the males in comparison to the females are noticeably bushier and contain auditory receptors to detect the characteristic whine of the female. The compound eyes are distinctly separated from one another. Their larvae only possess a pit-eye ocellus. The compound eyes of adults develop in a separate region of the head. New ommatidia are added in semicircular rows at the rear of the eye. During the first phase of growth, this leads to individual ommatidia being square, but later in development they become hexagonal. The hexagonal pattern will only become visible when the carapace of the stage with square eyes is molted. The head also has an elongated, forward-projecting "stinger-like" proboscis used for feeding, and two sensory palps. The maxillary palps of the males are longer than their proboscises, whereas the females’ maxillary palps are much shorter. In typical bloodsucking species, the female has an elongated proboscis.
The thorax is specialized for locomotion. Three pairs of legs and a pair of wings are attached to the thorax. The insect wing is an outgrowth of the exoskeleton. The Anopheles mosquito can fly for up to four hours continuously at 1 to 2 kilometres per hour (0.6–1 mph), travelling up to 12 kilometres (7.5 mi) in a night. Males beat their wings between 450 and 600 times per second.
The abdomen is specialized for food digestion and egg development; the abdomen of a mosquito can hold three times its own weight in blood. This segment expands considerably when a female takes a blood meal. The blood is digested over time, serving as a source of protein for the production of eggs, which gradually fill the abdomen.
Feeding by adults
Typically, both male and female mosquitoes feed on nectar and plant juices, but in many species the mouthparts of the females are adapted for piercing the skin of animal hosts and sucking their blood as ectoparasites. In many species, the female needs to obtain nutrients from a blood meal before she can produce eggs, whereas in many other species, she can produce more eggs after a blood meal. Both plant materials and blood are useful sources of energy in the form of sugars, and blood also supplies more concentrated nutrients, such as lipids, but the most important function of blood meals is to obtain proteins as materials for egg production.
For females to risk their lives on blood sucking while males abstain is not a strategy limited to the mosquitoes; it also occurs in some other insect families, such as the Tabanidae. When a female reproduces without such parasitic meals, she is said to practise autogenous reproduction, as in Toxorhynchites; otherwise, the reproduction may be termed anautogenous, as occurs in mosquito species that serve as disease vectors, particularly Anopheles and some of the most important disease vectors in the genus Aedes. In contrast, some mosquitoes, for example, many Culex, are partially anautogenous; they do not need a blood meal for their first cycle of egg production, which they produce autogenously; however, subsequent clutches of eggs are produced anautogenously, at which point their disease vectoring activity becomes operative.
With regard to host location, female mosquitoes hunt their blood host by detecting organic substances such as carbon dioxide (CO2) and 1-octen-3-ol produced from the host, and through optical recognition. Mosquitoes prefer some people over others. The preferred victim's sweat simply smells better than others because of the proportions of the carbon dioxide, octenol and other compounds that make up body odor. The most powerful semiochemical that triggers the keen sense of smell of Culex quinquefasciatus is nonanal. A large part of the mosquito’s sense of smell, or olfactory system, is devoted to sniffing out blood sources. Of 72 types of odor receptors on its antennae, at least 27 are tuned to detect chemicals found in perspiration. In Aedes, the search for a host takes place in two phases. First, the mosquito exhibits a nonspecific searching behavior until the perception of host stimulants, then it follows a targeted approach.
Most mosquito species are crepuscular (dawn or dusk) feeders. During the heat of the day, most mosquitoes rest in a cool place and wait for the evenings, although they may still bite if disturbed. Some species, such as the Asian tiger mosquito, are known to fly and feed during daytime.
Prior to and during blood feeding, blood-sucking mosquitoes inject saliva into the bodies of their source(s) of blood. This saliva serves as an anticoagulant; without it one might expect the female mosquito's proboscis to become clogged with blood clots. The saliva also is the main route by which mosquito physiology offers passenger pathogens access to the hosts' interior. Not surprisingly the salivary glands are a major target to most pathogens, whence they find their way into the host via the stream of saliva.
Mosquitoes of the genus Toxorhynchites never drink blood. This genus includes the largest extant mosquitoes, the larvae of which prey on the larvae of other mosquitoes. These mosquito eaters have been used in the past as mosquito control agents, with varying success.
Mosquito mouthparts are very specialised, particularly those of the females, which in most species are adapted to piercing skin and then sucking blood. Apart from bloodsucking, the females generally also drink assorted fluids rich in dissolved sugar, such as nectar and honeydew, to obtain the energy they need. For this, their blood-sucking mouthparts are perfectly adequate. In contrast, male mosquitoes are not bloodsuckers; they only drink such sugary fluids as they can find. Accordingly, their mouthparts do not require the same degree of specialisation as those of females.
Externally, the most obvious feeding structure of the mosquito is the proboscis. More specifically, the visible part of the proboscis is the labium, which forms the sheath enclosing the rest of the mouthparts. When the mosquito first lands on a potential host, her mouthparts will be enclosed entirely in this sheath, and she will touch the tip of the labium to the skin in various places. Sometimes, she will begin to bite almost straight away, while other times, she will prod around, apparently looking for a suitable place. Occasionally, she will wander for a considerable time, and eventually fly away without biting. Presumably, this probing is a search for a place with easily accessible blood vessels, but the exact mechanism is not known. It is known that there are two taste receptors at the tip of the labium, which may well play a role.
The female mosquito does not insert her labium into the skin; it bends back into a bow when the mosquito begins to bite. The tip of the labium remains in contact with the skin of the victim, acting as a guide for the other mouthparts. In total, there are six mouthparts besides the labium: two mandibles, two maxillae, the hypopharynx, and the labrum.
The mandibles and the maxillae are used for piercing the skin. The mandibles are pointed, while the maxillae end in flat, toothed "blades". To force these into the skin, the mosquito moves its head backwards and forwards. On one movement, the maxillae are moved as far forward as possible. On the opposite movement, the mandibles are pushed deeper into the skin by levering against the maxillae. The maxillae do not slip back because the toothed blades grip the skin.
The hypopharynx and the labrum both are hollow. Saliva with anticoagulant is pumped down the hypopharynx to prevent clotting, and blood is drawn up the labrum.
To understand the mosquito mouthparts, it is helpful to draw a comparison with an insect that chews food, such as a dragonfly. A dragonfly has two mandibles, which are used for chewing, and two maxillae, which are used to hold the food in place as it is chewed. The labium forms the floor of the dragonfly's mouth, the labrum forms the top, while the hypopharynx is inside the mouth and is used in swallowing. Conceptually, then, the mosquito's proboscis is an adaptation of the mouthparts that occur in other insects. The labium still lies beneath the other mouthparts, but also enfolds them, and it has been extended into a proboscis. The maxillae still "grip" the "food" while the mandibles "bite" it. The top of the mouth, the labrum, has developed into a channeled blade the length of the proboscis, with a cross-section like an inverted "U". Finally, the hypopharynx has extended into a tube that can deliver saliva at the end of the proboscis. Its upper surface is somewhat flattened so, when pressed against it, the labrum forms a closed tube for conveying blood from the victim.
For the mosquito to obtain a blood meal, it must circumvent the vertebrate physiological responses. The mosquito, as with all blood-feeding arthropods, has mechanisms to effectively block the hemostasis system with their saliva, which contains a mixture of secreted proteins. Mosquito saliva negatively affects vascular constriction, blood clotting, platelet aggregation, angiogenesis and immunity, and creates inflammation. Universally, hematophagous arthropod saliva contains at least one anticlotting, one antiplatelet, and one vasodilatory substance. Mosquito saliva also contains enzymes that aid in sugar feeding and antimicrobial agents to control bacterial growth in the sugar meal. The composition of mosquito saliva is relatively simple, as it usually contains fewer than 20 dominant proteins. Despite the great strides in knowledge of these molecules and their role in bloodfeeding achieved recently, scientists still cannot ascribe functions to more than half of the molecules found in arthropod saliva. One promising application is the development of anticlotting drugs based on saliva molecules, which might be useful for approaching heart-related diseases, because they are more user-friendly blood clotting inhibitors and capillary dilators.
It is now well recognized that feeding ticks, sandflies, and, more recently, mosquitoes, have an ability to modulate the immune response of the animals (hosts) on which they feed. The presence of this activity in vector saliva is a reflection of the inherent overlapping and interconnected nature of the host hemostatic and inflammatory/immunological responses and the intrinsic need to prevent these host defenses from disrupting successful feeding. The mechanism for mosquito saliva-induced alteration of the host immune response is unclear, but the data have become increasingly convincing that such an effect occurs. Early work described a factor in saliva that directly suppresses TNF-α release, but not antigen-induced histamine secretion, from activated mast cells. Experiments by Cross et al. (1994) demonstrated the inclusion of Ae. aegypti mosquito saliva into naïve cultures led to a suppression of interleukin (IL)-2 and IFN-γ production, while the cytokines IL-4 and IL-5 are unaffected by mosquito saliva. Cellular proliferation in response to IL-2 is clearly reduced by prior treatment of cells with SGE. Correspondingly, activated splenocytes isolated from mice fed upon by either Ae. aegypti or Cx. pipiens mosquitoes produce markedly higher levels of IL-4 and IL-10 concurrent with suppressed IFN-γ production. Unexpectedly, this shift in cytokine expression is observed in splenocytes up to 10 days after mosquito exposure, suggesting natural feeding of mosquitoes can have a profound, enduring, and systemic effect on the immune response.
T cell populations are decidedly susceptible to the suppressive effect of mosquito saliva, showing increased mortality and decreased division rates. Parallel work by Wasserman et al. (2004) demonstrated that T- and B-cell proliferation was inhibited in a dose dependent manner with concentrations as low as 1/7 of the saliva in a single mosquito. Depinay et al. (2005) observed a suppression of antibody-specific T cell responses mediated by mosquito saliva and dependent on mast cells and IL-10 expression.
A recent study suggests mosquito saliva can also decrease expression of interferon−α/β during early mosquito-borne virus infection. The contribution of type I interferons (IFN) in recovery from infection with viruses has been demonstrated in vivo by the therapeutic and prophylactic effects of administration of IFN-inducers or IFN, and recent research suggests mosquito saliva exacerbates West Nile virus infection, as well as other mosquito-transmitted viruses.
Egg development and blood digestion
Female mosquitoes use two very different food sources. They need sugar for energy, which is taken from sources such as nectar, and they need blood as a source of protein for egg development. Because biting is risky and hosts may be difficult to find, mosquitoes take as much blood as possible when they have the opportunity. This, however, creates another problem. Digesting that volume of blood takes a while, and the mosquito will require energy from sugar in the meantime.
To avoid this problem, mosquitoes have a digestive system which can store both food types, and give access to both as they are needed. When the mosquito drinks a sugar solution, it is directed to a crop. The crop can release sugar into the stomach as it is required. At the same time, the stomach never becomes full of sugar solution, which would prevent the mosquito taking a blood meal if it had the chance.
Blood is directed straight into the mosquito's stomach. In species that feed on mammalian or avian blood, hosts whose blood pressure is high, the mosquito feeds selectively from active blood vessels where the pressure assists in filling the gut rapidly. If, instead of slapping a feeding mosquito, one stretches one's skin so that it grips the proboscis and the mosquito cannot withdraw it, the pressure will distend the gut until it breaks and the mosquito dies. In the unmolested mosquito however, the mosquito will withdraw, and as the gut fills up the stomach lining secretes a peritrophic membrane that surrounds the blood. This membrane keeps the blood separate from anything else in the stomach. However, like certain other insects that survive on dilute, purely liquid diets, notably many of the Homoptera, many adult mosquitoes must excrete unwanted aqueous fractions even as they feed. (see the photograph of a feeding Anopheles stephensi. Note that the excreted droplet patently is not whole blood, being far more dilute). As long as they are not disturbed, this permits mosquitoes to continue feeding until they have accumulated a full meal of nutrient solids. As a result, a mosquito replete with blood can continue to absorb sugar, even as the blood meal is slowly digested over a period of several days. Once blood is in the stomach, the midgut of the female synthesizes proteolytic enzymes that hydrolyze the blood proteins into free amino acids. These are used as building blocks for the synthesis of egg yolk proteins.
In the mosquito Anopheles stephensi Liston, trypsin activity is restricted entirely to the posterior midgut lumen. No trypsin activity occurs before the blood meal, but activity increases continuously up to 30 hours after feeding, and subsequently returns to baseline levels by 60 hours. Aminopeptidase is active in the anterior and posterior midgut regions before and after feeding. In the whole midgut, activity rises from a baseline of approximately 3 enzyme units (EU) per midgut to a maximum of 12 EU at 30 hours after the blood meal, subsequently falling to baseline levels by 60 hours. A similar cycle of activity occurs in the posterior midgut and posterior midgut lumen, whereas aminopeptidase in the posterior midgut epithelium decreases in activity during digestion. Aminopeptidase in the anterior midgut is maintained at a constant, low level, showing no significant variation with time after feeding. Alpha-glucosidase is active in anterior and posterior midguts before and at all times after feeding. In whole midgut homogenates, alpha-glucosidase activity increases slowly up to 18 hours after the blood meal, then rises rapidly to a maximum at 30 hours after the blood meal, whereas the subsequent decline in activity is less predictable. All posterior midgut activity is restricted to the posterior midgut lumen. Depending on the time after feeding, greater than 25% of the total midgut activity of alpha-glucosidase is located in the anterior midgut. After blood meal ingestion, proteases are active only in the posterior midgut. Trypsin is the major primary hydrolytic protease and is secreted into the posterior midgut lumen without activation in the posterior midgut epithelium. Aminoptidase activity is also luminal in the posterior midgut, but cellular aminopeptidases are required for peptide processing in both anterior and posterior midguts. Alpha-glucosidase activity is elevated in the posterior midgut after feeding in response to the blood meal, whereas activity in the anterior midgut is consistent with a nectar-processing role for this midgut region.
Mosquitoes are very widespread, occurring in all regions of the world except for Antarctica. In warm and humid tropical regions, they are active for the entire year, but in temperate regions they hibernate over winter. Arctic mosquitoes may be active for only a few weeks as pools of water form on top of the permafrost. During that time, though, they exist in huge numbers and can take up to 300ml of blood per day from each animal in a caribou herd.
Eggs from strains in the temperate zones are more tolerant to the cold than ones from warmer regions. They can even tolerate snow and subzero temperatures. In addition, adults can survive throughout winter in suitable microhabitats.
Means of dispersal
Worldwide introduction of various mosquito species over large distances into regions where they are not indigenous has occurred through human agencies, primarily on sea routes, in which the eggs, larvae, and pupae inhabiting water-filled used tires and cut flowers are transported. However, apart from sea transport, mosquitoes have been effectively carried by personal vehicles, delivery trucks, trains and aircraft. Sufficient quarantine measures have proven difficult to implement.
Mosquitoes can act as a vector for many disease-causing viruses and parasites. Infected mosquitoes carry these organisms from person to person without exhibiting symptoms themselves. Mosquito-borne diseases include:
- Viral diseases, such as yellow fever, dengue fever and Chikungunya, transmitted mostly by Aedes aegypti. Dengue fever is the most common cause of fever in travelers returning from the Caribbean, Central America, and South Central Asia. This disease is spread through the bites of infected mosquitoes and cannot be spread person to person.
Severe dengue can be fatal, but with good treatment, less than 1% of patients die from dengue.
- The parasitic diseases collectively called malaria, caused by various species of Plasmodium, carried by mosquitoes of the genus Anopheles
- Lymphatic filariasis (the main cause of elephantiasis) which can be spread by a wide variety of mosquito species
- West Nile virus is a concern in the United States, but there are no reliable statistics on worldwide cases.
- Eastern equine encephalitis virus is a concern in the eastern United States.
- Tularemia, a bacterial disease caused by Francisella tularensis, is variously transmitted, including by biting flies. Culex and Culiseta, are vectors of tularemia as well as arbovirus infections such as West Nile Virus.
Though originally transmission of HIV was a public health concern, practical considerations and studies of epidemiological patterns suggest that any transmission of the HIV virus by mosquitoes is in practice extremely unlikely at worst.
Various species of mosquitoes are estimated to transmit various types of disease to more than 700 million people annually in Africa, South America, Central America, Mexico, Russia and much of Asia, with millions of resultant deaths. At least two million people annually die of these diseases, and the morbidity rates are many times higher still.
Methods used to prevent the spread of disease, or to protect individuals in areas where disease is endemic, include:
- Vector control aimed at mosquito control or eradication
- Disease prevention, using prophylactic drugs and developing vaccines
- Prevention of mosquito bites, with insecticides, nets and repellents
Since most such diseases are carried by "elderly" female mosquitoes, some scientists have suggested focusing on these to avoid the evolution of resistance.
Many methods are used for mosquito control. Depending on the situation, the most important usually include:
- source reduction (e.g., removing stagnant water)
- biocontrol (e.g. importing natural predators such as dragonflies)
- trapping, and/or insecticides to kill larvae or adults
- exclusion (mosquito nets and window screening)
Source reduction means elimination of breeding places of mosquitoes. It includes engineering measures such as filling, levelling and drainage of breeding places, and water management (such as intermittent irrigation). Source reduction can also be done by making water unsuitable for moquitoes to breed, for example, by changing salinity of water. Some specific measures are:
- For Culex: abolition of domestic and peridomestic sources of water suitable for breeding, for example removal and disposal of sewage and other waste water
- For Aedes: eliminating incidental containers such as discarded tins, crockery, pots, broken bottles, and coconut shells
- For Anopheles: abolish breeding places by filling or drainage
- For Mansonia: removal of aquatic plants manually or by application of herbicides
Details of the biology of different species of mosquitoes differ too widely for any limited set of rules to be sufficient in all circumstances. However, the foregoing are the most economical and practical measures for most purposes. The importance of peridomestic control arises largely because most species of mosquitoes rarely travel more than a few hundred metres unless the wind is favorable.
In combination with scrupulous attention to control of breeding areas, window screens and mosquito nets are the most effective measures for residential areas. Insecticide-impregnated mosquito nets are particularly effective because they selectively kill those insects that attack humans, without affecting the general ecology of the area.
An ideal mosquito net is white in color (to allow easy detection of mosquitoes), rectangular, netted on sides and top, without a hole. The size of opening in net should not exceed 0.0475 inch in diameter (about 150 holes per square inch).
Window screens should have copper or bronze guaze with 16 meshes to an inch.
Dragonfly and damselfly nymphs and various other aquatic insect predators eat mosquitoes at all stages of development and dense populations can be useful in reducing mosquito problems. Various small fishes, such as species of Galaxias and members of the Poeciliidae, such as Gambusia (so-called mosquitofish) and guppies (Poecilia), eat mosquito larvae and sometimes may be worth introducing into ponds to assist in control. Many other types of fish are also known to consume mosquito larvae, including bass, bluegills, piranhas, Arctic char, salmon, trout, catfish, fathead minnows, goldfish, and killifish.
Although bats and purple martins can be prodigious consumers of insects, many of which are pests, less than 1% of their diet typically consists of mosquitoes. Neither bats nor purple martins are known to control or even significantly reduce mosquito populations.
Some cyclopoid copepods are predators on first-instar larvae, killing up to 40 Aedes larvae per day. Larval Toxorhynchites mosquitoes are known as natural predators of other Culicidae. Each larva can eat 10 to 20 mosquito larvae per day. During its entire development, a Toxorhynchites larva can consume an equivalent of 5,000 larvae of the first-instar (L1) or 300 fourth-instar larvae (L4). However, Toxorhynchites can consume all types of prey, organic debris,, or even exhibit cannibalistic behavior.
Bacillus thuringiensis israelensis has also been used to control them as a biological agent.
Mosquito bites and treatment
Visible, irritating bites are due to an immune response from the binding of IgG and IgE antibodies to antigens in the mosquito's saliva. Some of the sensitizing antigens are common to all mosquito species, whereas others are specific to certain species. There are both immediate hypersensitivity reactions (types I and III) and delayed hypersensitivity reactions (type IV) to mosquito bites. Both reactions result in itching, redness and swelling. Immediate reactions develop within a few minutes of the bite and last for a few hours. Delayed reactions take around a day to develop, and last for up to a week. Several anti-itch medications are commercially available, including those taken orally, such as Benadryl, or topically applied antihistamines and, for more severe cases, corticosteroids, such as hydrocortisone and triamcinolone. Using a brush to scratch the area surrounding the bite (but not the bite itself) and running hot water (around 49 °C or 120 °F) over it can alleviate itching for several hours by reducing histamine-induced skin blood flow. Tea tree oil has been shown to be an effective anti-inflammatory, reducing itching.
Insect repellents are applied on skin and give short time protection against mosquito bites. The chemical DEET repels some mosquitoes and other insects. Some CDC-recommended repellents are picaridin, Eucalyptus oil (PMD) and IR3535. Others are indalone, dimethyl pthalate, dimethyl carbate, ethyl hexanediol. Plants can also repel mosquitoes, such as citronella, catnip, marigolds, ageratum and horsemint to name a few.
The oldest known mosquito with an anatomy similar to modern species was found in 79-million-year-old Canadian amber from the Cretaceous. An older sister species with more primitive features was found in amber that is 90 to 100 million years old.
Genetic analyses indicate the Culicinae and Anophelinae clades may have diverged about 150 million years ago. The Old and New World Anopheles species are believed to have subsequently diverged about 95 million years ago.
Taxonomy of the Culicidae
Over 3,500 species of the Culicidae have already been described. They are generally divided into two subfamilies which in turn comprise some 43 genera. These figures are subject to continual change, as more species are discovered, and as DNA studies compel rearrangement of the taxonomy of the family. The two main subfamilies are the Anophelinae and Culicinae, with their genera as shown in the subsection below.
Subfamilies and genera
- Ralph Harbach (November 2, 2008). "Family Culicidae Meigen, 1818". Mosquito Taxonomic Inventory. http://mosquito-taxonomic-inventory.info/family-culicidae-meigen-1818.
- http://www.mimosq.org/mosquitoes.htm (accessed 2011/12/13)
- Jaeger, Edmund C. (1959). A Source-Book of Biological Names and Terms. Springfield, Ill: Thomas. ISBN 0-398-06179-3.
- Brown, Lesley (1993). The New shorter Oxford English dictionary on historical principles. Oxford [Eng.]: Clarendon. ISBN 0-19-861271-0.
- http://www.mosquitoes.org/LifeCycle.html Biological notes on mosquitoes
- http://www.enst.umd.edu/News/Mosquitoes/index.cfm Taking a bite out of mosquito research, Author Paul Leisnham, University of Maryland
- Molavi, Afshin (June 12, 2003). "Africa's Malaria Death Toll Still "Outrageously High"". National Geographic. http://news.nationalgeographic.com/news/2003/06/0612_030612_malaria.html. Retrieved July 27, 2007.
- "Mosquito-borne diseases". American Mosquito Control Association. http://www.mosquito.org/mosquito-borne-diseases. Retrieved October 14, 2008.
- World Health Organisation. Flooding and communicable diseases fact sheet. http://www.who.int/hac/techguidance/ems/flood_cds/en/
- Wilcox, B.A. & Ellis, B. ; Forests and emerging infectious diseases of humans. Unasylva, Vol. 57 2006/2 Pub:Food and Agriculture Organization of the United Nations ISSN 0041-6436 available at: http://www.fao.org/docrep/009/a0789e/a0789e03.htm
- Fang, Janet (July 21, 2010). "Ecology: A world without mosquitoes". Nature. doi:10.1038/466432a. http://www.nature.com/news/2010/100721/full/466432a.html. (requires registration)
- "Mosquito Eradication". Science Today - Beyond the Headlines. California Academy of Sciences. 26. http://www.calacademy.org/sciencetoday/mosquito-eradication/. Retrieved 25 August 2011.
- Wigglesworth V. B., The Adaptation of Mosquito Larvae to Salt Water. Department of Entomology, London School of Hygiene and Tropical Medicine.1932.
- Crans, Wayne J.; Wyeomyia smithii (Coquillett); Rutgers University, Center for Vector Biology. http://www.rci.rutgers.edu/~insects/sp27.htm
- Kosova, Jonida, "Longevity Studies of Sindbis Virus Infected Aedes Albopictus" (2003). All Volumes (2001-2008). Paper 94. http://digitalcommons.unf.edu/ojii_volumes/94
- Michigan Mosquito Control Association; Michigan Mosquito Manual, MMCA Edition. Pub. Michigan Department of Agriculture June 2002
- Spielman, Andrew; D'Antonio, M. (2001). Mosquito : a natural history of our most persistent and deadly foe. New York: Hyperion. ISBN 978-0-7868-6781-3.
- Huang, Juan. Walker, Edward D. Vulule, John. Miller,James R. ; Daily temperature profiles in and around Western Kenyan larval habitats of Anopheles gambiae as related to egg mortality. Malaria Journal 2006, 5:87 doi:10.1186/1475-2875-5-87
- "Mosquito". Virginia Tech. http://sites.ext.vt.edu/departments/entomology/factsheets/mosquito.html. Retrieved May 19, 2007.
- Harzsch, S.; Hafner, G. (2006). "Evolution of eye development in arthropods: Phylogenetic aspects". Arthropod Structure and Development 35 (4): 319–340. doi:10.1016/j.asd.2006.08.009. PMID 18089079. http://linkinghub.elsevier.com/retrieve/pii/S1467803906000570.
- Kaufmann C, Briegel H (June 2004). "Flight performance of the malaria vectors Anopheles gambiae and Anopheles atroparvus" (PDF). Journal of Vector Ecology 29 (1): 140–153. PMID 15266751. http://www.sove.org/Journal%20PDF/June%202004/Kaufmann.pdf. Retrieved June 21, 2009.
- Sawabe K, Moribayashi A. ; "Lipid utilization for ovarian development in an autogenous mosquito, Culex pipiens molestus (Diptera: Culicidae)." J Med Entomol. 2000 Sep;37(5):726-31. PMID 11004785
- Elissa A. Hallem; Nicole Fox, A.; Zwiebel, Laurence J.; Carlson, John R. (2004). "Olfaction: Mosquito receptor for human-sweat odorant". Nature 427 (6971): 212–213. doi:10.1038/427212a. PMID 14724626. http://www.nature.com/nature/journal/v427/n6971/full/427212a.html?lang=en.
- "Scientists identify key smell that attracts mosquitoes to humans". US News. October 28, 2009. http://www.usnews.com/science/articles/2009/10/28/scientists-identify-key-smell-that-attracts-mosquitoes-to-humans.html?s_cid=rss:scientists-identify-key-smell-that-attracts-mosquitoes-to-humans.
- Devlin, Hannah (February 4, 2010). "Sweat and blood why mosquitoes pick and choose between humans". London: The Times. http://www.timesonline.co.uk/tol/news/science/medicine/article7014046.ece. Retrieved May 13, 2010.
- R. G. Estrada-Franco & G. B. Craig (1995). Biology, disease relationship and control of Aedes albopictus. Technical Paper No. 42. Washington, D.C.: Pan American Health Organization.
- Wayne J. Crans (1989). "Resting boxes as mosquito surveillance tools". Proceedings of the Eighty-Second Annual Meeting of the New Jersey Mosquito Control Association. pp. 53–57. http://www.rci.rutgers.edu/~insects/restbox.htm.
- C. Jones & E. Schreiber (1994). "The carnivores, Toxorhynchites". Wing Beats 5 (4): 4. http://www.rci.rutgers.edu/~insects/sp2.htm.
- "Site down for maintenance". Pestscience.com. http://www.pestscience.com/PDF/BNIra56.PDF. Retrieved 2011-05-31.
- Isra Wahid, Toshihiko Sunahara, Motoyoshi Mogi; Maxillae and Mandibles of Male Mosquitoes and Female Autogenous Mosquitoes (Diptera: Culicidae); Journal of Medical Entomology vol. 40, no. 2): 150 — 158 (2003)
- Mullen, Gary; Durden, Lance (2009). Medical and Veterinary Entomology. London: Academic Press.
- Richards, O. W.; Davies, R.G. (1977). Imms' General Textbook of Entomology: Volume 1: Structure, Physiology and Development Volume 2: Classification and Biology. Berlin: Springer. ISBN 0-412-61390-5.
- Ribeiro, J. M. & Francischetti, I. M. (2003). "Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives". Annual Review of Entomology 48: 73–88. doi:10.1146/annurev.ento.48.060402.102812. PMID 12194906.
- Grossman G. L. & James, A. A. (1993). "The salivary glands of the vector mosquito, Aedes aegypti, express a novel member of the amylase gene family". Insect Molecular Biology 1 (4): 223–232. doi:10.1111/j.1365-2583.1993.tb00095.x. PMID 7505701.
- Rossignol, P. A. & Lueders, A. M. (1986). "Bacteriolytic factor in the salivary glands of Aedes aegypti". Comparative Biochemistry and Physiology B 83 (4): 819–822. doi:10.1016/0305-0491(86)90153-7. PMID 3519067.
- Valenzuela, J. G., Pham, V. M., Garfield, M. K., Francischetti, I. M. & Ribeiro, J. M. (2002). "Toward a description of the sialome of the adult female mosquito Aedes aegypti". Insect Biochemistry and Molecular Biology 32 (9): 1101–1122. doi:10.1016/S0965-1748(02)00047-4. PMID 12213246.
- Dr. Nigel Beebe, University of Technology, Sydney, Australia.
- Bissonnette, E. Y., Rossignol, P. A. & Befus, A. D. (1993). "Extracts of mosquito salivary gland inhibit tumour necrosis factor alpha release from mast cells". Parasite Immunology 15 (1): 27–33. doi:10.1111/j.1365-3024.1993.tb00569.x. PMID 7679483.
- Cross ML, Cupp EW, Enriquez FJ (1994). "Differential modulation of murine cellular immune responses by salivary gland extract of Aedes aegypti". American Journal of Tropical Medicine and Hygiene 51 (5): 690–696. PMID 7985763.
- Zeidner, N. S., Higgs, S., Happ, C. M., Beaty, B. J. & Miller, B. R. (1999). "Mosquito feeding modulates Th1 and Th2 cytokines in flavivirus susceptible mice: an effect mimicked by injection of sialokinins, but not demonstrated in flavivirus resistant mice". Parasite Immunology 21 (1): 35–44. doi:10.1046/j.1365-3024.1999.00199.x. PMID 10081770.
- Wanasen, N., Nussenzveig, R. H., Champagne, D. E., Soong, L. & Higgs, S. (2004). "Differential modulation of murine host immune response by salivary gland extracts from the mosquitoes Aedes aegypti and Culex quinquefasciatus". Medical and Veterinary Entomology 18 (2): 191–199. doi:10.1111/j.1365-2915.2004.00498.x. PMID 15189245.
- Wasserman, H. A., Singh, S. & Champagne, D. E. (2004). "Saliva of the Yellow Fever mosquito, Aedes aegypti, modulates murine lymphocyte function". Parasite Immunology 26 (6–7): 295–306. doi:10.1111/j.0141-9838.2004.00712.x. PMID 15541033.
- Depinay, N., Hacini, F., Beghdadi, W., Peronet, R., Mécheri, S. (2006). "Mast cell-dependent down-regulation of antigen-specific immune responses by mosquito bites". Journal of Immunology 176 (7): 4141–4146. PMID 16547250.
- Schneider, B. S., Soong, L., Zeidner, N. S. & Higgs, S. (2004). "Aedes aegypti salivary gland extracts modulate anti-viral and TH1/TH2 cytokine responses to sindbis virus infection". Viral Immunology 17 (4): 565–573. doi:10.1089/vim.2004.17.565. PMID 15671753.
- Taylor, J. L., Schoenherr, C. & Grossberg, S. E. (1980). "Protection against Japanese encephalitis virus in mice and hamsters by treatment with carboxymethylacridanone, a potent interferon inducer". The Journal of Infectious Diseases 142 (3): 394–399. doi:10.1093/infdis/142.3.394. PMID 6255036.
- Schneider, B. S., Soong, L., Girard, Y. A., Campbell, G., Mason, P. & Higgs, S. (2006). "Potentiation of West Nile encephalitis by mosquito feeding". Viral Immunology 19 (1): 74–82. doi:10.1089/vim.2006.19.74. PMID 16553552.
- Schneider, B. S. & Higgs, S. (May 2008). "The enhancement of arbovirus transmission and disease by mosquito saliva is associated with modulation of the host immune response". Transactions of the Royal Society of Tropical Medicine and Hygiene 102 (5): 400–408. doi:10.1016/j.trstmh.2008.01.024. PMC 2561286. PMID 18342898. http://linkinghub.elsevier.com/retrieve/pii/S0035-9203(08)00053-9.
- Billingsley, P. F. & Hecker, H. (1991). "Blood digestion in the mosquito, Anopheles stephensi Liston (Diptera: Culicidae): activity and distribution of trypsin, aminopeptidase, and alpha-glucosidase in the midgut". Journal of Medical Entomology 28 (6): 865–871. PMID 1770523.
- Fang, Janet (July 21, 2010). "Ecology: A world without mosquitoes". Nature. doi:10.1038/466432a. http://www.nature.com/news/2010/100721/full/466432a.html.
- Hawley, W. A., Pumpuni, C. B., Brady, R. H. & Craig, G. B. (March 1989). "Overwintering survival of Aedes albopictus (Diptera: Culicidae) eggs in Indiana". Journal of Medical Entomology 26 (2): 122–129. PMID 2709388.
- Hanson, S. M. & Craig, G. B. (September 1995). "Aedes albopictus (Diptera: Culicidae) eggs: field survivorship during northern Indiana winters". Journal of Medical Entomology 32 (5): 599–604. PMID 7473614.
- Romi, R., Severini, F. & Toma, L. (March 2006). "Cold acclimation and overwintering of female Aedes albopictus in Roma". Journal of the American Mosquito Control Association 22 (1): 149–151. doi:10.2987/8756-971X(2006)22[149:CAAOOF]2.0.CO;2. PMID 16646341.
- "Lymphatic Filariasis". World Health Organisation (WHO) website. World Health Organisation (WHO). http://www.who.int/mediacentre/factsheets/fs102/en/. Retrieved 24 August 2011.
- Evaluation of mosquito species (Diptera: culicidae) identified in Manisa province according to their breeding sites and seasonal differences]. Turkiye Parazitol Derg. 2011 ;35(2):100-4. doi:10.5152/tpd.2011.25.
- "Can I get HIV from mosquitoes?". CDC. October 20, 2006. http://www.cdc.gov/hiv/resources/qa/qa32.htm.
- "Resistance is Useless". The Economist. April 8, 2009. http://www.economist.com/science/displaystory.cfm?story_id=13437697.
- Singh, R. K., Dhiman, R. C. & Singh, S. P. (June 2003). "Laboratory studies on the predatory potential of dragon-fly nymphs on mosquito larvae". Journal of Communicable Diseases 35 (2): 96–101. PMID 15562955.
- Louis A. Krumholz, Reproduction in the Western Mosquitofish, Gambusia affinis affinis (Baird & Girard), and Its Use in Mosquito Control, JSTOR: Ecological Monographs, Vol. 18, No. 1 (Jan., 1948), pp. 1–43.
- Fradin, M. S. (1 June 1998). "Mosquitoes and mosquito repellents: a clinician's guide". Annals of Internal Medicine 128 (11): 931–940. doi:10.1059/0003-4819-128-11-199806010-00013. PMID 9634433. http://www.annals.org/cgi/pmidlookup?view=long&pmid=9634433.
- Marten, G. G. & Reid, J. W. (2007). "Cyclopoid copepods". Journal of the American Mosquito Control Association 23 (2 Suppl): 65–92. doi:10.2987/8756-971X(2007)23[65:CC]2.0.CO;2. PMID 17853599.
- (Steffan & Evenhuis, 1981; Focks, 1982).
- Kramer, John Paul; Entomophthora culicis (Zygomycetes, Entomophthorales) as a pathogen of adult aedes aegypti (diptera, culicidae). Aquatic Insects Volume 4, Issue 2, 1982, pages 73–79. doi:10.1080/01650428209361085.
- M.M. Shamseldean, E.G. Platzer, Romanomermis culicivorax: Penetration of larval mosquitoes, Journal of Invertebrate Pathology, Volume 54, Issue 2, September 1989, Pages 191–199, ISSN 0022-2011, doi:10.1016/0022-2011(89)90028-1.
- Clements, Alan (1992). The biology of mosquitoes - volume 1: Development, Nutrition and Reproduction. London: Chapman & Hall. ISBN 0-85199-374-5.
- Yosipovitch, Gil; Katherine Fast, Jeffrey D. Bernhard (2005). "Noxious Heat and Scratching Decrease Histamine-Induced Itch and Skin Blood Flow". Journal of Investigative Dermatology 125: 1268–1272. doi:10.1111/j.0022-202X.2005.23942.x. PMID 16354198. http://www.nature.com/jid/journal/v125/n6/pdf/5603667a.pdf. Retrieved May 30, 2009.
- "Anti-inflammatory Activity of Tea Tree Oil". Rural Industries Research and Development Corporation. February 2001. http://pandora.nla.gov.au/pan/23877/20040309-0000/www.rirdc.gov.au/reports/TTO/01-10.pdf. Retrieved 2011-06-17.
- Syed, Z.; Leal, W. S. (2008). "Mosquitoes smell and avoid the insect repellent DEET". Proceedings of the National Academy of Sciences 105 (36): 13598–13603. doi:10.1073/pnas.0805312105. PMC 2518096. PMID 18711137. //www.ncbi.nlm.nih.gov/pmc/articles/PMC2518096/.
- CDC (2009). Updated Information regarding Insect Repellents. http://www.cdc.gov/ncidod/dvbid/westnile/repellentupdates.htm.
- G. O. Poinar et al. (2000). "Paleoculicis minutus (Diptera: Culicidae) n. gen., n. sp., from Cretaceous Canadian amber with a summary of described fossil mosquitoes" (PDF). Acta Geologica Hispanica 35: 119–128. http://www.geologica-acta.com/pdf/aghv3501a12.pdf.
- A. Borkent & D. A. Grimaldi (2004). "The earliest fossil mosquito (Diptera: Culicidae), in Mid-Cretaceous Burmese amber". Annals of the Entomological Society of America 97 (5): 882–888. doi:10.1603/0013-8746(2004)097[0882:TEFMDC]2.0.CO;2. http://esa.publisher.ingentaconnect.com/content/esa/aesa/2004/00000097/00000005/art00004.
- Calvo, E., Pham, V. M., Marinotti, O., Andersen, J. F. & Ribeiro, J. M. (2009). "The salivary gland transcriptome of the neotropical malaria vector Anopheles darlingi reveals accelerated evolution of genes relevant to hematophagy" (PDF). BMC Genomics 10 (1): 57. doi:10.1186/1471-2164-10-57. PMC 2644710. PMID 19178717. http://www.biomedcentral.com/content/pdf/1471-2164-10-57.pdf. Retrieved June 21, 2009.
- Widespread Divergence Between Incipient Anopheles gambiae Species Revealed by Whole Genome Sequences
- Harbach, R.E. 2011. Mosquito Taxonomic Inventory, http://mosquito-taxonomic-inventory.info/, accessed during October 2011)
- Brunhes, J.; Rhaim, A.; Geoffroy, B.; Angel, G.; Hervy, J. P. Les Moustiques de l'Afrique mediterranéenne French/English. Interactive identification guide to mosquitoes of North Africa, with database of information on morphology, ecology, epidemiology, and control. Mac/PC Numerous illustrations. IRD/IPT  2000 CD-ROM. ISBN 2-7099-1446-8
- Davidson, Elizabeth W. (1981). Pathogenesis of invertebrate microbial diseases. Montclair, N. J.: Allanheld, Osmun. ISBN 0-86598-014-4.
- Jahn, G. C., Hall, D. W. & Zam, S. G. (1986). "A comparison of the life cycles of two Amblyospora (Microspora: Amblyosporidae) in the mosquitoes Culex salinarius and Culex tarsalis Coquillett". Journal of the Florida Anti-Mosquito Association 57: 24–27.
- Kale, H. W., II. (1968). "The relationship of purple martins to mosquito control" (PDF). The Auk 85 (4): 654–661. JSTOR 4083372. http://elibrary.unm.edu/sora/Auk/v085n04/p0654-p0661.pdf.