If the 1 million described insect species, only 300-400 species feed on blood. The best known groups of bloodsucking insects are the lice, fleas, mosquitoes, sand flies, black flies, and bugs. But there are also several lesser known groups such as the nycteribiids and streblids, two families of cyclorrhaphous flies found exclusively on bats; the Rhagionidae or snipe flies, a little-studied group of brachyceran flies; some lepidopterans (e.g., Calpe eustrigata); and even some coleopterans (e.g., Platypsyllus castoris) appear to have started on the evolutionary road to hematophagy.
Bloodsucking insects are of immense importance to humans, primarily because of the diseases they transmit. They also cause huge losses in animal husbandry because of disease transmission and because of direct losses linked to the pain and irritation they cause to animals. The most spectacular example of this agricultural loss is the prevention of the development of a cattle industry worth billions of dollars a year through much of sub-Saharan Africa because of tsetse fly-transmitted trypanosomiasis, although some argue that this has been Africa’s savior because it has preserved wildlife and prevented desertification. Bloodsucking insects also cause serious losses in the tourist industry in areas as disparate as the French Camargue, the Scottish Highlands, and the state of Florida. We cannot ignore the sheer annoyance they can cause to us all.
EVOLUTION OF THE BLOODSUCKING HABIT
Although bloodsucking insects are poorly represented in the fossil record, it seems probable that they emerged along with the first nesting or communal dwelling vertebrates (reptiles) in the Mesozoic era (65-225mya). Evolution of the bloodsucking habit probably occurred in two main ways. The first route involved the attraction of insects to vertebrates, with the attraction being either to the protection of the nest environment or for the utilization of vertebrate-associated resources such as dung. The second route involved morphological preadaptations that permitted the rapid adoption of the bloodsucking habit.
Many insects would have been drawn to vertebrate nests because of the protected environment and abundance of food there. Gradually, some would have progressed to feeding on cast skin or feathers. Phoresy also would have permitted easy travel from one
nest to another. Once phoresy was adopted, the insects may have begun to feed directly on the host animal and thus established an even more permanent association with the host; mallophagan lice make a good example of this type of association. Regular accidental encounters with blood may then have led rapidly to the evolution of the bloodsucking habit because of the highly nutritious nature of blood compared to skin, fur, and feather.
Other insects are attracted to vertebrates outside the nest situation to utilize other vertebrate-associated resources, notably dung. Dung is used by a wide variety of organisms and there is strong competition to be the first to lay eggs in it. So, for example, the female horn fly Haematobia irritans lays its eggs in dung within 15 s of its deposition. To do this, the insect must remain permanently with the vertebrate; to do that, it must feed on the vertebrate. The high nutritional content of blood will then make hematophagy a favored evolutionary route.
Some insects also had morphological preadaptations for piercing surfaces, facilitating the relatively easy switch to blood feeding. Entomophagous insects (those that feed on other insects) and plant-feeding insects are prime candidates. For example, the Boreidae are a group of small apterous scorpion flies that are capable of jumping. They live in moss and feed on other insects by piercing them with their mouthparts. They are commonly found in nests because of the moss content and abundance of insects found there. It is easy to imagine such a lineage developing into fleas.
Insects that feed on plants may also have switched to the blood-feeding habit. An unusual example is a blood-feeding moth, C. eus-trigata. This moth belongs to a group of noctuids having a proboscis that is hardened and modified to allow them to penetrate fruit rinds. C. eustrigata has used the morphological preadaptation to feed on vertebrate blood.
The question of host choice is an extremely important one because it defines patterns of disease transmission and economic damage caused by bloodsucking insects. Bloodsucking insects in general feed on a range of different hosts, including birds, reptiles, mammals, and amphibians. Even invertebrates such as annelids, arachnids, and other insects are sometimes included in the diet. But any particular bloodsucking insect generally feeds only from a small segment of the available hosts. This segment of choice is preferred but it is not immutable. This can be clearly seen around zoos where the exotic animals are quickly incorporated into the diet of the local bloodsucking insects.
The determinants of host choice are complex, but probably one of the most important factors is simply host availability. Changes in host availability because of more intensive animal husbandry, coupled with decreasing rural populations of humans and improved mosquito-free housing, were a major factor in the disappearance of autochthonous malaria from northern Europe in the past century. Despite our poor understanding of the factors determining host choice, there is a direct relationship between the number of hosts that bloodsucking insects utilize and the insects. locomotory abilities (which is often reflected in the amount of time they spend with the host). Thus, ectoparasites (which have poor locomotory abilities and usually remain permanently on hosts) are often restricted to a single host species. A good example is the louse Haematomyzus elephantis, which is restricted to elephants. At the other extreme, those flying bloodsucking insects such as mosquitoes that make contact with the host only long enough to take a blood meal often display a very catholic host choice. For example, a sample population of the mosquito
Culex salinarius was shown to take 45% of its blood meals from birds, 17% from equines, and 15% from canines; moreover, 13% of the meals was a mixture of blood from more than one host.
In general terms, the most common hosts chosen are large herbivores. Large, social herbivores present an abundant, easily visible food source that is reliable and predictable from season to season. Carnivores in comparison are fewer in number, often solitary, and range unpredictably over wide areas. Another reason large herbivores are chosen is that they are poor at defending themselves from attack compared to small, agile animals that will often kill and/ or eat attacking bloodsucking insects.
For lice and other bloodsucking insects that are permanently present on the host, finding a new host is simply a matter of moving from one to the other when the hosts are in bodily contact. For bloodsucking insects that are only in temporary contact with the host, finding a host is a more difficult proposition. The following host-seeking behaviors are not rigidly patterned but they probably typically follow one another in a loose sequence. For most bloodsucking insects, olfactory stimuli are the first host-related signals perceived, and visual signals from the host probably are apt to become important at a later stage in host location. Bloodsucking insects make use of this predictability by permitting the current behavioral response to lower the threshold required for the next host signal to elicit the next behavioral response in the host location sequence. The increasing strength and diversity of host-derived signals that the bloodsucking insect receives as it moves closer to the host are thereby enhanced.
Host location is usually restricted to particular times of the day for each species of bloodsucking insect. Thus, tsetse flies tend to be crepuscular, Anopheles gambiae (the most important vector of malaria) is a night feeder, and the stable fly Stomoxys calcitrans bites during the day. As hunger increases, bouts of host location behavior intensify. For many bloodsucking insects such as the tsetse, the first behavior is often to choose a resting site where they have a good chance of encountering a host-derived signal and once there, to remain motionless and wait for a host-derived signal. This strategy combines minimal energy usage with a good chance of encountering a host. Other bloodsucking insects use more active strategies. If a gentle wind is blowing from one direction, the optimum strategy can be to fly across the wind so that the probability of contact with a host odor plume is enhanced.
Host-derived olfactory clues used include carbon dioxide, lactic acid, acetone, octenol, butanone, and phenolic compounds found in urine. These are probably used in combination by each insect’s sensitivity to different combinations of smells. For example, we can look at the power of phenolic components found in bovine urine to draw tsetse flies to a bait. Used singly, 3-n-propylphenol draws roughly equal numbers of Glossina pallidipes and G. morsitans morsitans. In contrast, when 3-n-propylphenol is used in combination with 4-methylphenol, catches of G. pallidipes increase 400%, whereas catches of G. m. morsitans decrease. The explanation for this may be that first, mixtures of odors are a stronger guide to the presence of a host than a single odor alone and so will minimize energy consumption from chasing false trails. Second, mixtures may help in host choice by guiding bloodsucking insects to particular host species.
Tracking the source of an odor plume while in flight is a major task. It is believed that many bloodsucking insects achieve this by using upwind optomotor anemotaxis. During flight, insects are blown off course by any wind that is blowing. They can use this fact to determine wind direction. To do this, they observe the perceived movements of fixed objects on the ground, and by comparing this to the direction in which they are trying to fly determine wind direction. The suggestion is that the insect flies across wind until an odor plume is encountered, when it turns upwind. If the odor plume is lost, it recommences flying across wind until it refinds the odor and turns upwind once more. This proceeds until the insect comes into the immediate vicinity of the host. It is believed that hosts can be detected by odor at about 90 m by tsetse flies and at 15-80m by some mosquitoes.
Vision is also used in host location by the majority of bloodsucking insects and is used most extensively by day-feeding insects in open habitats. In general, bloodsucking insects can detect and discriminate between objects on the basis of color contrast, relative brightness (intensity contrast), movement, and shape. Insects are quite sensitive to movement and their color vision stretches up into the UV but not down to the red. Night-feeding bloodsucking insects have relatively better intensity contrast than color contrast, whereas for day-biting bloodsucking insects, movement perception and color contrast may be particularly important. Large individual herbivores (as opposed to herds) are thought to be detected by vision at about 50m by tsetse flies and at 5-20m by some mosquitoes.
Once the bloodsucking insect is in proximity to the host, heat and humidity become important factors in location in addition to the continuing importance of vision and odor. Temperature is probably a useful guide from about 5 cm to a meter or so from the host depending on insect species. Even when they have contacted a host, bloodsucking insects will imbibe a blood meal only if it provides the correct biochemical characteristics (i.e., taste).
THE BLOOD MEAL
Bloodsucking insects take huge meals. Temporary ectoparasites such as the tsetse fly typically ingest more than their own unfed body weight in blood. The reasons are twofold. First, taking a blood meal is a very dangerous activity and taking huge blood meals minimizes the number of times an insect must associate with the host. Second, locating the host is often difficult and huge blood meals are a way of making the most of each encounter. Mouthparts are adapted to the blood-feeding habit. Typically, they are either of the piercing kind seen in mosquitoes, bugs, lice, and fleas or the cutting kind seen in tabanids, black flies, and biting flies.
The host usually responds to feeding activity, particularly the injection of saliva, by mounting an immune response that includes pruritis (itching). Typically, this begins to occur about 3 min after feeding commences. Thus, there is a selective advantage in completing the blood meal within this 3-min “safety period” after which the host will be alerted to the presence of the insect. To help achieve this, bloodsucking insects have produced a range of antihemostatic molecules in the saliva, one of the major functions of which is to minimize host contact time.
Antihemostatic molecules produced by the bloodsucking insect include anticoagulant molecules working variously, for example, on thrombin or factors VIII and X. However, platelet plugging of small wounds is probably of more importance to bloodsucking insects than blood coagulation. Consequently, they also produce antiplatelet aggregating factors such as apyrase. These are used to impede the plugging of the penetration wound in capillaries and to prevent clogging of the insect mouthparts. The insect saliva also contains powerful vasodilatory substances to increase blood flow to the wound and antihistamines that will minimize inflammation and itching, possibly extending the “safe period.” Salivary components are also important as they can facilitate the transmission of arthropod-borne pathogens. For example, the production of Leishmania-enhancing factor in the saliva of the sand fly Lutzomyia longipalpis enhances the establishment of the parasite Leishmania major in the vertebrate host. It has also been shown that such effects may be limited to naive hosts, suggesting that the history of exposure to vector saliva may influence the outcome of potentially infectious inoculations. Parasites can also manipulate the salivary glands to their own advantage. Thus, malaria sporozoites damage the salivary glands of mosquitoes, reducing anti-hemostatic effectiveness, and thus extend probing time and increase the chances they will be transmitted to a new host.
Some bloodsucking insects feed only on blood during their entire life. Examples include the tsetse flies, streblids, hippoboscids and nycteribiids, triatomine and cimicid bugs, and lice. Blood is deficient in certain nutrients such as the B-group vitamins and pantothenic acid, and the insect cannot make these itself. To make up for this deficiency, these obligate hematophages harbor symbiotic microorganisms that produce these extra nutrients. These symbionts are often housed in a specialized body compartment, traditionally called a mycetome or, more recently, a bacteriome. For example, the tsetse fly Glossina harbors three symbiotic microorganisms, including Wigglesworthia glossinia, which is from the ^-subdivision of the Proteobacteria, in the bacteriome of the anterior gut.
There are several evident morphological adaptations for a bloodsucking life. Piercing or cutting mouthparts are the clearest example. In addition, many periodic and permanent ectoparasites such as fleas and lice are laterally or dorsoventrally flattened and are wingless, which are adaptations allowing them to move easily through the pelage or feathers and to avoid being groomed by permitting them to flatten themselves against the skin. Most of these ectoparasites also have cuticular extensions in the form of spines and combs. These are longer and spinier in bird-infesting forms than in those found on mammals. The combs in particular are found covering weak spots in the body such as the articulations between body segments. The spacing of the tips of the combs correlates well with the diameter of the hairs on the body of the host. This suggests that these combs have a dual function: protecting the body from abrasion and acting as an anchoring device for the ectoparasite.
The host regulates the numbers of permanent ectoparasites by grooming, usually with both the toes and the teeth. This often limits ectoparasite distribution on the host to those areas the host can groom least efficiently, such as the head and neck. The immune response mounted against these bloodsucking insects is often very localized. It makes feeding on these protected areas of the skin difficult, with the result that the insects feed less well or move to less affected areas of the body where they are more easily groomed. The result is that the host regulates ectoparasite numbers.
The host also shows behavioral defenses to temporary ectoparasites such as mosquitoes. The level of defensive behavior is usually density dependent and thus can have important consequences for disease transmission. For example, the arbovirus eastern equine encephalitis (EEE), which is naturally found in birds, is transmitted in the United States by the mosquito Culiseta melanura. During spring and early summer, these mosquitoes feed almost exclusively on passerine birds, transmitting the virus among them. Later in the season, as mosquito
numbers increase, birds’ defensive behavior increases and mosquitoes are more willing to feed on other vertebrate hosts. This is when EEE is transmitted to other vertebrates including horses and humans.