Ticks and Tick Ecology in Mississippi: Implications for Human Disease Transmission.

Ticks are blood-sucking ectoparasites which may transmit a wide variety of disease organisms to humans. They feed exclusively on blood and have rather specific temperature and humidity requirements. Because of these requirements, as well as host availability, ticks tend to congregate in areas providing those factors. This leads to "clustering" of ticks in the environment. A field project was conducted at a wildlife management area to carefully document lone star tick (LST) clustering in relation to shade and soil moisture. Results of this study showed clear patterns of LST clustering, especially of nymphs, in association with shade and soil moisture. Ticks were only collected in areas with [greater than]23% soil moisture. Only three ticks out of 221 were collected in 10% or less shade. The average percent shade for areas where all adult LST's were caught was 63% in lane one and 43% in lane two. This study indicated that LST clustering in nature is real and somewhat predictable. The epidemiological implications of tick clustering are presented and discussed. Key Words: ticks, tick-borne diseases, tick control

Medical importance of ticks--Ticks are blood sucking ectoparasites capable of transmitting a wide variety of disease organisms such as protozoa (babesiosis), viruses (encephalitis and Colorado tick fever), and bacteria (Rocky Mountain spotted fever, ehrlichiosis, Lyme disease, and tularemia) (Spach, 1993). They seem to especially be associated with spotted fever group rickettsial organisms (Burgdorfer, 1977). In addition, ticks may cause paralysis in humans and animals as a result of salivary toxins injected upon feeding. In Mississippi, there are approximately 30 cases of RMSF and 20 cases of Lyme disease (LD) reported each year (Personal Communication, Dr. Mary Currier, Mississippi Department of Health, October 5, 2000). Only rarely are cases of tick-borne tularemia or ehrlichiosis reported in Mississippi. Concerning Lyme disease, there is controversy as to whether or not Mississippi cases are actually LD or another, yet undescribed, Lyme-like illness.

Tick biology--There are three families of ticks recognized in the world today: (1) Ixodidae (hard ticks), (2) Argasidae (soft ticks), and (3) Nuttalliellidae, a small, curious, little-known group with some characteristics of both hard and soft ticks (Varma, 1993). The terms hard and soft refer to the presence of a dorsal scutum or "plate" in the Ixodidae, which is absent in the Argasidae.

Hard ticks display sexual dimorphism, males and females look obviously different (Figure 1), and the blood-fed females are capable of enormous expansion. They have no true head, but their mouthparts are anteriorly attached and visible from dorsal view. If eyes are present, they are located dorsally on the sides of the scutum.

Soft ticks are leathery and nonscutate, without sexual dimorphism (Figure 2). Their mouthparts are subterminally attached in adult and nymphal stages and not visible from dorsal view. Eyes, if present, are located laterally in folds above the legs.

There are major differences in the biology of hard and soft ticks. Some hard ticks have a one-host life cycle, wherein engorged larvae and nymphs remain on the host after feeding; they then molt, and subsequent stages reattach and feed. Adults mate on the host, and only engorged females drop off to lay eggs on the ground. While some hard ticks complete their development on only one or two hosts, most commonly encountered ixodids have a three-host life cycle. In this case, adults mate on a host (except for some Ixodes spp.) and the fully fed female drops from the host animal to the ground and lays from 2,000 to 18,000 eggs, after which she dies. Eggs hatch in about 30 days into a six-legged seed tick (larval) stage, which feeds predominantly on small animals. The fully fed seed ticks drop to the ground and transform into eight-legged nymphs. These nymphs seek an animal host, feed, and drop to the ground. They then molt into adult ticks, thus completing the life cycle.

Ticks feed exclusively on blood, and begin by cutting a small hole into the host epidermis with their chelicerae and inserting the hypostome into the cut, thereby attaching to the host. Blood flow is maintained with the aid of an anticoagulant from the salivary glands. Some hard ticks secure their attachment to the host by forming a cement cone around the mouthparts and surrounding skin. Two phases are recognized in the feeding of nymphal and female hard ticks: (1) a growth feeding stage characterized by slow continuous blood uptake and (2) a rapid engorgement phase occurring during the last 24 h or so of attachment.

The biology of soft ticks differs from hard ticks in several ways. Adult female soft ticks feed and lay eggs several times during their lifetime. Soft tick species may also undergo more than one nymphal molt before reaching the adult stage. With the exception of larval stages of some species, soft ticks do not firmly attach to their hosts for several days like the Ixodidae--they are adapted to feeding rapidly and leaving the host promptly.

Many hard tick species "quest" for hosts, by climbing blades of grass or weeds and remaining attached, forelegs outstretched, awaiting a passing host. They may travel up a blade of grass (to quest) and back down to the leaf litter where humidity is high (to rehydrate) several times a day. Also, hard ticks will travel a short distance toward a [CO.sub.2] source. Adult ticks are more adept at traveling through vegetation than the minute larvae.

Tick ecology--Hard ticks and soft ticks occur in different habitats. In general, hard ticks occur in brushy, wooded, or weedy areas containing numerous deer, cattle, dogs, small mammals, or other hosts. Soft ticks are generally found in animal burrows or dens, bat caves, dilapidated or poor-quality human dwellings (huts, cabins, etc.), or animal rearing shelters. Many soft tick species thrive in hot and dry conditions, whereas ixodids are more sensitive to desiccation and, therefore, usually found in areas providing protection from high temperatures, low humidities, and constant breezes.

Most hard ticks, being sensitive to desiccation, must practice water conservation and uptake. Their epicuticle contains a wax layer which prevents water movement through the cuticle. Water can be lost through the spiracles; therefore, resting ticks keep their spiracles closed most of the time opening them only one or two times an hour. Tick movement and its resultant rise in [CO.sub.2] production cause the spiracles to open about 15 times an hour with a corresponding water loss.

Development, activity, and survival of hard ticks is influenced greatly by temperature and humidity within the tick microhabitat. Because of their temperature and high humidity requirements, as well as host availability, hard ticks tend to congregate in areas providing those factors. Ecotonal areas (interface areas between forests and fields) are excellent habitats for hard ticks. Open meadows/prairies, along with climax forest areas, support the fewest ticks. Ecotone areas and small openings in the woods are usually heavily infested. Deer and small mammals thrive in ecotonal areas, thus providing blood meals for ticks. In fact, deer are often heavily infested with hard ticks in the spring and summer months. The optimal habitat of white tail deer has been reported to be the forest ecotone, since the area supplies a wide variety of browse and frequently offers the greatest protection from their natural enemies. Many favorite deer foods are also found in the low trees of an ecotone, including greenbrier, sassafras, grape, oaks, and winged sumac.

Ticks are not evenly distributed in nature. The spatial arrangement of ticks in nature may be uniform (over-dispersed), random, or aggregated (underdispersed), depending upon tick species and ecology of the host (Korch, 1994). Hard ticks attach to a vertebrate host for several days. Host specificity varies by tick species; some ticks feed on almost any vertebrates, whereas others are closely associated with a particular rodent, bird, reptile, etc. Since engorged ticks are most likely to fall off wherever their hosts spend the most time, the presence of ticks in the environment is largely a function of host activity.

Field study--Previous tick studies in Mississippi have indicated clustering or clumping of at least two hard-tick species. A study of the ecology of adult Ixodes scapularis in a privately owned wildlife management area demonstrated clustering patterns (Goddard, 1992). Another study, 200 miles north of the first, revealed clumping of adult Amblyomma americanum, or lone star ticks (LST) (Jackson et al. 1996). The LST is an extremely aggressive pest species occurring primarily in the southeastern and south-central United States, and up the eastern seaboard to approximately New York. All three motile life stages bite humans, pets, domestic and wild animals. A field study was designed to determine whether the phenomenon of tick clustering in nature is real and predictable. Portions of this work have been previously published (Goddard, 1997).

MATERIALS AND METHODS

Field study--Lone star ticks were collected in two field plots over a period of seven months and their location within the plots studied in relation to soil moisture and shade. In late winter, 1994, two lanes 620 meters long by 2 meters wide were mowed ("bush-hogged") through the woods at the Copiah County Game Management Area in central Mississippi. The narrow lanes were mowed to facilitate careful sampling and exact numbering of each lane into 10-meter sections. The two lanes were located 1.6 kilometers apart. Each lane crossed several types of habitat (open field; creek bottoms; and forests of oak, hickory, and pine). From April 1, 1994, to October 31, 1994, each lane was sampled for ticks on a weekly basis: a 1-square-meter piece of white flannel cloth was dragged up one side of the lane all the way to the end and back down the other side. The cloth was examined for ticks every 10 meters. Spots were marked on a map drawn to scale wherever LST's (adults or nymphs) were captured. Except for voucher specimens, all ticks were returned alive to the plots. Percent shade for each 10-meter section of lane was visually estimated three times during the season (May 15, July 15, and September 15) and averaged to yield a shade value for each section. Percent soil moisture was determined (using an OSK[R] soil moisture meter from Forestry Suppliers of Jackson, Mississippi) on the same three dates and averaged to yield a moisture value for each 10-metersection.

RESULTS AND DISCUSSION

Field study--Overall, 221 LST's were collected--64 in site one and 157 in site two. Breaking down by life stage, 31 adults and 33 nymphs were collected in site one, whereas 44 adults and 113 nymphs were collected in site two. Seasonally, the peak of adult ticks in site one was June 15; the peak in site two was June 8. More nymphs were collected on May 31 and June 8 than any other date in site one, and on June 8 in site two.

Lone star ticks were clustered in the lanes (Figure 3). This was most obvious in site two (especially the nymphs, see Figure 3 D). In fact, if one calculates the area where most ticks were found and divides by total area (x 100), the percent of area where ticks were found is quite small (Table 1). This was most striking for nymphs in site one where 73% were collected in 9.7% of the lane. Overall, approximately 70% of LST's were found in approximately 10--20% of the geographic area.

Percent shade in the lanes ranged from 0--90% in both sites. Ticks were collected mostly from shaded areas. Only three ticks out of 221 were collected in 10% or less shade. This may be due to LST inability survive hot dry environments. One study in Arkansas demonstrated that LST eggs reared in an environment of[less than]75% humidity would not hatch (Lancaster, 1957). The average percent shade for areas where all adult LST's were caught was 63% in site one, and 43% in site two. The average percent shade for areas where all nymphs were collected was 61% in site one and 46% in site two. If one further breaks down the collection data into only the areas where most LST's were collected the percentages are higher (Table 2).Soil moisture in the lanes ranged from 20--66% in site one and from 27-88% in site two. Overall, site two was a wetter site. Interestingly, site two produced 30% more ticks than site one. Again, this may relate to moisture needs by lone star ticks for survival. Ticks were collected where soil moisture was [greater than]23%, with most collected where it was 37% or higher (Table 3).

This study indicated that lone star tick clustering in nature is real and somewhat predictable. Clearly definable spots in the study sites consistently produced ticks, whereas others did not. For example, almost no ticks were collected in open areas with full sunlight. Approximately 70% of ticks were collected in 10-20% of the geographic area.

Implications for disease transmission--Clustering of ticks in the woods can have important epidemiological implications. A person working or playing outdoors may encounter one of these "hot spots" and acquire numerous tick bites. I personally saw a young family with two children under age 6 having a picnic on the ground at a state park in an area where I had previously collected hundreds of lone star ticks! On the other hand, tick clustering may be a weak link which we can exploit for prevention/control purposes. If sites of clustering can be identified they can be possibly avoided or sprayed with pesticides. Since most of the ticks only occur in 10-20% of the area, then carefully placed (precision-targeted) pesticides could theoretically significantly reduce tick populations with minimal use of pesticides.

LITERATURE CITED

Burgdorfer, W. 1977. Tick-borne diseases in the United States: Rocky Mountain spotted fever and Colorado tick fever Acta Tropica 34:103-125.

Goddard, J. 1992. Ecological studies of adult Ixodes scapular is in central Mississippi: Questing activity in relation to time of year, vegetation type, and meteorologic conditions. J. Med. Entomol. 29:501-506.

Goddard, J. 1997. Clustering effects of lone star ticks in nature: Implications for control. J. Environ. Hlth. 59:8-11.

Jackson, L.K., D.M. Gaydon, and J. Goddard. 1996. Seasonal activity and relative abundance of Amblyomma americanum in Mississippi. J. Med. Entomol. 33:128-131.

Korch, G.W. Jr. 1994. Geographic dissemination of tick-borne zoonoses. Page 447 in D.E. Sonenshine and T.N. Mather, eds, Ecological Dynamics of Tick-borne Zoonoses, New York: Oxford University Press.

Lancaster, J.L. 1957. Control of the Lone Star Tick. Univ. Ark. Agric. Exp. Sta. Rep. Serv. No. 67.

Spach, D.H., W.C. Liles, G.L. Campbell, R.E. Quick, D.E. Anderson, Jr., and T.R. Fritsche. 1993. Tick-borne diseases in the United States. N. Engl. J. Med. 329:936-947.

Varma, M.G.R. 1993. Ticks and mites. Pages 597-658 in R.P. Lane and R.W. Crosskey, eds, Medical Insects and Arachnids, Chapman and Hall, London.

Clustering of lone star ticks in study sites.
                   Percent of Area
Site  Tick Stage  Where Majority of
                  Ticks Were Found
 1      Adult           17.7
 1      Nymph            9.7
 2      Adult           14.5
 2      Nymph           25.8
Percent shade in places where the majority of lone star ticks were
collected.
                      Amount       Percent
Site  Tick Stage  LST's collected   Shade
 1      Adult       21/31 (68%)      71
 1      Nymph       24/33 (73%)      65
 2      Adult       31/44 (70%)      45
 2      Nymph      81/113 (72%)      71
Percent soil moisture in places where the majority of lone star ticks
were collected.
Site  Tick Stage     Amount     Percent
                     LST's        Soil
                   Collected    Moisture
 1      Adult     21/31 (68%)      38
 1      Nymph     24/33 (73%)      37
 2      Adult     31/44 (70%)      52
 2      Nymph     81/113 (72%)     53