Published by EMPORIA STATE UNIVERSITY
Editor: JOHN RICHARD SCHROCK
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Front cover: Triatoma gerstaeckeri, common in southern and central Texas. Photo used with permission of Mike Quinn, TexasEnto.net.
Justin O. Schmidt has a PhD. in Entomology from the University of Georgia. He runs a non-profit organization, Southwestern Biological Institute in Tucson, Arizona.
Lori Stevens is Professor of Biology at The University of Vermont. She received her M.S. and Ph.D. degrees from the University of Illinois, Chicago. Stevens is intrigued with the genetic interactions of hosts and parasites. She enjoys visiting family in Leavenworth , Kansas.
|Patricia Dorn is a Professor of Biological Sciences at Loyola University New Orleans. She received her Ph.D. from the University of Maryland and began her work on Trypanosomiais during her post-doctoral fellowship at Stanford Medical School.|
|Mack Mosbacher received his doctorate of veterinary medicine from the University of Missouri. He currently practices emergency veterinary medicine in Phoenix, Arizona.|
|John Klotz has a Ph.D. in Entomology from the University of Kansas and is an Urban Entomology Specialist Emeritus at the University of California, Riverside and lives in Sedona, Arizona.|
|Stephen A. Klotz graduated from the University of Kansas and is Chief of Infectious Diseases at the University of Arizona.|
Kissing bugs are bloodsucking insects in the order Hemiptera in the family Reduviidae. Almost all known species reside in the New World.
They are best known as vectors of Chagas disease, a disease caused by transmission of the blood parasite, Trypanosoma cruzi, through their feces. Vector transmission of Chagas disease occurs with a number of endemic kissing bugs. Chagas is largely confined to Mexico, Central America and South America.
Although only a few cases of insect-transmitted Chagas disease have occurred in the US, these bugs are common in southern, southeastern and southwestern states.
We discuss the biology of the bugs, their evolutionary history, their distribution in the United States, the risk they pose for transmission of T. cruzi to pets and other domestic animals, and the control of kissing bugs around human habitations.
EVOLUTION OF KISSING BUGS
The 140 or so species of triatomines, or "kissing bugs," evolved from a reduviid predator or "assassin bug," so called because it kills its arthropod prey by injecting potent toxins and proteases that liquefy the insides of the prey so they can be sucked out. How many times reduviids have forsaken their assassin habits to become blood sucking "kissers" has been a matter of some controversy. The fact that triatomines are found in as diverse habitats as bird and opossum nests (arboreal), and armadillo burrows and rat's nests, as well as human habitations (terrestrial) suggests that they evolved from multiple different predatory ancestors (i.e. are polyphyletic) that were already associated with arboreal or terrestrial hosts.
The two most important tribes for human infection, the Triatomini and Rhodniini, are quite divergent, suggesting distinct predatory ancestors. However, a recent, large study of the evolution of the Reduviidae using multiple genes and many morphological characters indicates that these two tribes arose from the same predatory ancestor (1) . The remaining three tribes still need to be examined but so far it appears blood sucking evolved just once, i.e. the Triatominae are monophyletic.
|Figure 1. Triatoma sanguisuga, the most common triatomine in Kansas and throughout central and southeastern US. Photo by Harold Baquet.|
One species, Triatoma rubrofosciata is found around the world, and may have spread in association with ships' rats. A few other species are found in Southeast and East Asia; however, most species (~125) are found only in the Americas. The Triatomini tribe contains two genera important for human transmission of Chagas, Triatoma and Panstrongylus, the former has the most (80) species and includes the two most important vectors for human transmission: T. infestans in South America, and T. dimidiata in Mesoamerica (Mexico, Central America, and northern South America). The Rhodniini tribe includes the genera Rhodnius and Psammolestes, with Rhodnius
prolixus being an important human vector in northern South America.
|Figure 2. Triatoma rubida, common in foothill regions of Phoenix and Tucson (female, note pointed projection from end of the abdomen).|
KISSING BUG SPECIES IN THE UNITED STATES
Ten species of Triatominae (Table 1) are native to the United States (2, 3) where their northern limit is determined by intolerance of cold temperatures. Natural infections of T. cruzi have been found in seven of these species (4). The Triatominae in the United States belong to two genera (Paratriatoma and Triatoma) and include four species complexes within the Triatoma (lecticularia, phyllosoma, protracta, rubida). The two species reported in Kansas, T. sanguisuga and T. lecticularia, are in an uncertain status and lecticularia complex, respectively (Dorn, unpublished data). They have the widest geographical distribution of the ten species found in the United States.
|Table 1. Checklist and geographic distribution of Triatominae of the United States. (Not including the cosmopolitan T. rubrofasciata.)|
|Triatoma||Uncertain||T. sanguisuga||yes||23||Alabama, Arizona, Arkansas, Florida, Georgia, Illinois, Indiana, Kansas, Kentucky, Louisiana, Maryland, Mississippi, Missouri, New Jersey, New Mexico, N.Carolina,Ohio, Oklahoma, Pennsylvania, S. Carolina, Tennessee, Texas, Virginia|
|Lectularia||T. lecticularia||yes||16||Arizona, California, Florida, Georgia, Illinois, Kansas, Louisiana, Maryland, Missouri, New Mexico, N. Carolina, Oklahoma, Pennsylvania, S.Carolina, Tennessee, Texas|
|T. indictiva||3||Arizona, New Mexico, Texas|
|Phyllosoma||T. recurva||6||Arizona, California, Colorado, Nevada, New Mexico, Texas|
|T. gerstaeckeri||2||New Mexico, Texas|
|Protracta||T. protracta||7||Arizona, California, Colorado, Nevada, New Mexico, Texas, Utah|
|Rubida||T. rubida||6||Arizona, California, Colorado, Nevada, New Mexico, Texas|
|Paratriatomo||P. hirsuta||5||Arizona, California, Colorado, Nevada, New Mexico|
The most widespread species, T. sanguisuga (Figure 1) and T. lectularia, are mostly sylvatic, however, in Manhattan, Kansas, T. sanguisuga was reported from poultry houses, barns and houses. Although there are reports of serious allergic reactions to their bite, no T. cruzi transmission to humans has been reported in Kansas. Triatoma sanguisuga is commonly associated with raccoons and opossums and has been found in large numbers around human dwellings from Florida to Texas (4).
The other kissing bug reported from Kansas, T. lecticularia, feeds on opossums, as well as wood rats (Neotoma spp.) and the rock squirrel (Spermophilus variegatus). T. indictiva is reported to feed on domestic and peridomestic animals. (See Figures 2-5 for other common triatomines in the U.S.)
All ten species in the United States are considered sylvatic and have different ecological niches. Species in the leticularia complex prefer open shrubland, woodland and wooded grassland (2). Wooded grassland is the preferred habitat for members of the protracta, rubida and phyllosoma complexes. The one species in the United States not in the Triatoma genus, Paratriatoma hirsuta, has a broad potential niche, much broader than its current geographical distribution.
BIOLOGY AND NATURAL HISTORY OF KISSING BUGS
Kissing bugs have a gradual development with five immature instars appearing similar to adults, but without wings. They are large bugs with adults ranging in length from about 12 to 36 mm. Both sexes and all five instars feed on blood of vertebrates, starring with the first instars which take a blood meal as soon as 2-3 days after hatching from the egg. They can develop from egg (Figure 5) to adult in several months in warm tropical areas when food is readily available. In temperate regions having extended cooler periods of the year, the bugs are typically univoltine with only one generation per year. In these regions bugs seek refuge in rodent burrows, cavities, caves, and other locations with moderate temperatures and pass the unfavorable times as immatures in various stages (Figure 4) . Adults live several months, occasionally a year or more (5), and feed throughout their lives. In captivity adults of Triatoma rubida, T. protracta, or T. recurva live 4-5 months on average. Mating lasts only about 10 minutes, a relatively short time compared to other hemipterans. As with other hemipterans, females readily mate with multiple males; females can store sperm for use months later and over their life span can lay up to several hundred eggs depending upon conditions (5). Active dispersal is achieved by flight in adults and by crawling in immatures (6). Passive dispersal occurs in some species by transport of attached eggs to new locations by birds or other animals, or by human transport of materials harboring eggs or free-living stages. Active dispersal of immatures can occur when a shortage of food sources stimulates bugs to crawl toward locations potentially having new hosts. Adults typically disperse by flight around dusk. Nutritional state and hunger are powerful drivers of dispersal (7). Another is the classical reproductive strategy in which gravid females retain eggs for deposition after flight (8,9). Dispersal is not a primary form of mate seeking as in many moths and other insects. Evidence against mate seeking is indicated by equal numbers of females and males captured at lights and the rapidity with which captured females oviposit fertile eggs (8).
Figure 3. Triatoma protracta, frequent home invader in California, especially the foothills around San Diego.
Figure 4. A fifth instar (nymphal stage) of T. recurva. Note the absence of wings in the nymphs.
Figure 5. Empty egg shells from T. recurva eggs.
Figure 6. A teneral of T. rubida, i.e.,newly emerged adult.
HABITAT AND HOST ASSOCIATION
Triatomine species inhabit a variety of ecological environments from generalized to highly specialized, including human domestic environments. Within these environments, they can range from opportunists feeding on a variety of host species to specialists feeding on a limited number of host types. Specialists include Cavernicola pilosa which feeds on bats, Rhodnius spp. living in palm trees where they feed on inhabiting birds and mammals, and Psammolestes spp. which live in bird nests constructed of twigs. Bird blood meals are sufficient for the bugs to survive and reproduce, but birds are not hosts of T. cruzi and thus alter the parasite transmission cycle. Somewhat more general feeders are T. rubrofosciata and members of the T. protracta complex that prefer feeding on rodents. Triatoma infestans, T. dimidiata, and R. prolixus are inhabitants of human domestic environments where they feed on people and their animals (6). Most species, irrespective of their preferred habitat, can become opportunistic feeders when other species are available. Species that are generally opportunists can also be facultative specialists preferring to feed mainly on one group of hosts if given the opportunity (10). The Triatoma living in Arizona are all non-domestic species that often feed on packrats (Neotoma spp.), yet they readily feed on a variety of vertebrate hosts they encounter, including humans. The Arizona-Sonora Desert Museum in Tucson, Arizona, is a regional educational living zoo that inadvertently supports large populations of T. rubida and T. protracta. These bugs plague many museum animals and sometimes feed so extensively that they have caused the death by chronic blood loss of animals, including a rare protected mountain rattlesnake (James L. Jarchow, DVM, pers. commun.). In Kansas, Triatoma sanguisuga like the Arizona species, feeds predominantly on Neotoma, raccoons and opossums, bur will readily feed on a variety of other hosts including humans.
When and how some species of triatomines became specialists on humans is a mystery. The subfamily is believed to have originated about 5 million years ago in the New World (11). Dares for the arrival of human beings in the New World are debated, bur their estimated arrival sometime between 14,000 to 20,000 years ago is relatively recent. Thus, shifts in some species of kissing bugs to specializing on our species are recent evolutionary events, and might well explain some of our vulnerability to the T. cruzi parasite the bugs transmit to us.
Kissing bugs rely on multiple sensory systems to locate hosts. These include gradients of carbon dioxide in the air, odors, moisture, hear, and air flow (12). They are exquisitely sensitive to carbon dioxide exhaled by mammals when breathing, being able to detect 75 parts per million above the background air levels of 350 pans per million when a trace of exhaled lactic acid, another attractant, is present. Cold blooded hosts including reptiles generate very low levels of carbon dioxide; nevertheless, kissing bugs use many other host-generated chemical cues including short chained aliphatic amines and acids, 7-to 9-carbon aldehydes and alcohols, and lactic acid to locate hosts. The bugs can also detect infrared radiation enabling them to orient toward warm blooded hosts from several meters. Finally, they anemotactically follow the movement of air currents impregnated with host odors to locate the host (12). Feeding by bugs in human domiciles usually takes place at night, with bugs hiding during the day in cracks and crevices away from the feeding areas. Much less is known about feeding times for sylvatic (non-domestic) species. Likely they adjust their activity periods to match the inactive periods of their host, thereby minimizing danger from host defenses. Triatoma rubida and T. protracta do not hesitate to approach and feed on rodents during bright midday times (13), a behavior that might well be adaptive for bugs that often feed on rodents in their burrows while the rodents are sleeping or quiescent during the day.
Once a host is located, a hungry bug extends its proboscis and inserts it into the skin of the host. Sometimes the host detects the minor sensation caused by a bug's probing and moves or shifts position. In response the bug usually retracts somewhat before continuing probing and feeding. Considering that a bug often imbibes more blood than its own weight (3), feeding is relatively rapid, lasting on average 22 minutes for T. protracta, 28 for T. rubida and between 11-28 minutes for T. infestans, T. dimidiata, and R. prolixus (13, 14). Blood is mostly water and the bulkiness of a large blood meal limits a bug's movement. To eliminate excess water, bugs often defecate during feeding, at completion of feeding, or shortly after leaving the feeding site (Figure 8). Some species, including those domestic species that frequently transmit Chagas disease, defecate rapidly and frequently, often on or near the host (14), while others defecate less rapidly and less frequently, often at a distance from the host (3). Frequency and proximity of defecation to the host are considered to be critical factors in transmitting T. cruzi and Chagas disease to humans (Figure 9).
HUMAN BITE ALLERGIES FROM KISSING BUGS
Kissing bug bites are the most common cause of insect bites that result in anaphylaxis in the United States. This medical emergency (also caused more commonly by bee stings) results from the release of chemical signals in response to proteins in the bug's saliva. Anaphylaxis usually causes the individual to rush to the emergency room where epinephrine and other interventions reverse the low blood pressure, swollen airways and rashes that often accompany anaphylaxis. Victims usually are awakened at night by shortness of breath, difficulty breathing or generalized itching. Other less ominous allergies include hives, swelling of the eyes, swelling at the site of the bite and persistent itching. Patients may experience anaphylaxis when re-bitten and one adult woman has died from the condition. The bite itself is painless, however swelling and inflammation at the site of the bite may last for weeks.
WILD AND DOMESTICATED ANIMALS INFECTED WITH Trypanosoma cruzi IN THE UNITED STATES
Kissing bugs rarely transmit Chagas to humans in the United States; only six such cases have been documented. Infection with Trypanasoma cruzi is common in several wildlife species, but rare in domestic pets. Reported cases in domestic species are limited to dogs in the warmer southern states. There are no reports of livestock, horses, or pigs being infected. Only one case report exists of infection in a domestic cat in the U.S.
The primary wildlife species in the United States that serve as host reservoirs for T. cruzi are rodents, particularly packrats in the genus Neotoma, raccoons and opossums, and to a lesser degree armadillos and skunks. T. cruzi has been reported in more than 20 different wildlife species in the United States in at least 13 states (15). Wood rats and other rodent species serve as reservoirs of infection, as rodent dens and nests may harbor the insect vectors. Infection dynamics of T. cruzi isolates appear to vary between species, with raccoons being infected with a more virulent genetic strain in which blood parasites levels peak sooner and antibodies are more quickly detected than occurs in opossums, another primary wildlife reservoir species. Additionally, mice injected with opossum derived T. cruzi isolates appear to subsequently clear the infection and survive, whereas injecting mice with the raccoon derived strains resulted in a 75% mortality rate in one study. Despite differences in virulence between the host species strains, pathologic cardiac changes induced by T. cruzi have been observed at necropsy in both raccoons and opossums.
|Figure 7. Blood smear showing Trypanosoma cruzi parasites among red blood cells. Photo by Rose Nasrazadani.|
Prevalence of T. cruzi in wildlife species varies, but infection rates as high as 62% occurred in raccoons tested in various states (16). Infection rates appear to be generally highest in coastal locations, with the elevated rates assumed to be due to the increased distribution of insect vectors secondary to the high humidity and lack of a winter freeze along the southern and eastern coasts. In contrast to the Latin American isolates that are transmitted to humans indirectly at the insect bite location by fecal contamination, T. cruzi in wildlife species in the U.S. is transmitted by oral ingestion of infected insects and to a lesser degree by placental transmission in utero.
In domestic pets, T. cruzi causing clinical health issues has been reported primarily in working dogs from southeastern Texas and foci in Louisiana, although antibody testing has confirmed T. cruzi exposure in many southern states and as far north as Minnesota. In domestic dogs as in wildlife species, infection is thought to be primarily by eating infected kissing bug vectors in response to skin irritation from the insect bite and from in utero transmission from dam to pup.
Clinical signs of infection in dogs are primarily cardiac, recognized as exercise intolerance or generalized weakness. Diagnostic testing may reveal severe heart arrythmias. And ultimately, a dilated form of heart failure develops. Treatment rarely results in a cure, and survival time in clinically affected dogs ranges from 0 to 60 months.
Prevention of Chagas disease in dogs depends on insect vector control and limiting contact with host reservoir species. In endemic kissing bug areas, animal housing and bedding should be treated with insecticide monthly, and kennels improved as needed to remove insect nesting sites.
|Figure 8 (above). Fecal smears and drops from a female T. rubida.||Figure 9 (right). Fecal smears on household wall from T. infestans in Bolivia. These deposits act as aggregation pheromones.|
PEST MANAGEMENT OF KISSING BUGS
Insecticide spraying is the cornerstone of vector control programs for triatomines in South America where domestic and peridomestic species are prevalent and can attain high population densities in and around homes. The sylvatic species found in the U.S. are only occasional invaders and thus present a different set of problems that rely on non-chemical measures for control such as habitat modification and exclusion techniques (see table below).
First and foremost is a thorough inspection of the home both inside and outside.
During the active season (around mid-spring to mid-fall) inspections should be carried out on a regular basis to find and destroy any stray bugs. During the day they typically hide in dark places in cracks and crevices or under objects. For example, in the bedroom they may hide in bed sheets or blankets or under the mattress so it is recommended that all of these potential hiding places be inspected especially before retiring. Outside during the day they hide in dark sheltered places such as beneath flowerpots or furniture emerging at night to be seen crawling or resting on surfaces. Pay special attention to areas inside and out where pets congregate or sleep.
In addition to efforts aimed at kissing bugs, control measures may be needed to remove their wild vertebrate hosts, such as packrats, which are common around homes in the Southwest. Packrats can have several dozen or more bugs inhabiting their nests. Trapping the packrats and their nests close to the house can reduce home invasions. However, it is advisable that only the nearest packrat nest and packrats be removed in the hope that the kissing bugs will move to more peripheral nests farther from the house. After the packrats have been removed, a pyrethroid dust or spray should be applied to the old nesting sites to eliminate any remaining kissing bugs. This is critical because in the absence of their natural host the bugs will seek out another source of blood, which might end up the homeowner (17).
In the case of sensitized homeowners who have become allergic to kissing bugs, a directed spray application of pyrethroid insecticides in and around the home may provide some added protection. Most effective indoors is a crack and crevice application to potential harborage sites in bedrooms and bathrooms, and outdoors a perimeter treatment along the foundation and eaves paying close attention to thoroughly treat entryways such as windows and doors to prevent their access into the home.
Sensitized individuals may also elect to sleep under a bed net (mosquito netting) that is tucked in all around the mattress for added protection and using double-sided tape placed on the legs of the bed. Beds should be kept at least one foot away from walls. Sticky trap monitors placed under and around beds may also catch bugs. wandering
homeowners might wish vacuum the bedroom and their bedroom during
the season weather-stripping
and their pets
in response to climates and as more homes encroach into their habitats. Learning ro ',","VF.HU." these and to keep them out of human habitations is an important
Table 2. Non-chemical measures to reduce risk of household infestation by triatomines.
|Install weather stripping and tight fitting insect screens on windows and doors, insect proof dog and cat entrances, and keep fireplace flues shut.|
Manage indoor and outdoor lighting at night to make homes less attractive to kissing bugs:
|Seal potential entryways into homes (e.g. foundation cracks and utility line points of entry) with caulk, silicone seal, or other appropriate materials.|
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