Boophilus ollllllintus - the South Carolina Entomological Society

APPLICATION OF MODELLING TO THE ECOLOGY OF
BOOPHILUS ANNULATUS (SAY) (ACARI: IXODIDAE)','
Pete D. Teel
Associate Professor, R.P.E.
Department of Entomology
Texas A&M University
College Station, Texas 77843-2475
ABSTRACT
The ecological basis for modelling the off-host phase of the Boophilus armulatus (Say)
(Acari: Ixodidae) life cycle is examined with respect to microenvironmcnts of three pre­
dominant vegetation communities in the Tamaulipan biotic province. '!'hennal summat.ion
and biophysical modelling appro8ches are contrasted for modelling embJ)'onic development
and celosian. Applications of models to sur.:eillancc, eradication and quarantine epidemiology
are discussed. Models integrated with aerial infrared photography through a Geographic
Infonnation System (CIS) enable spatial heterogeneity of rangclnnd vcgCl8tion communities
to be characterized and analyzcd across quarantinc levels.
Kcy Words: Boophilus amwlalu.s, modelling, ecology. cattle fevcr tick. GIS, epidcmiology,
Acari, Ixodidae.
J. Agric. Entomol. 8(2): 291-296 (October 1991)
A long and arduous campaign of quarantine and eradication programs initiated
by state and federal agencies in 1907 eliminated the vectors of bovine babesiosis,
Boophilus annulatus (Say) and Bo. microplus (Canestl'ini), from 14 southern states
and established a buffer zone along the Texas-Mexico border (Graham and
Hourrigan 1977). Both tick species and the two diseuse pathogens, Babesia
bigemilla Smith and KilboulTle, and Ba. bovis Babes, remain prevalent in nOitheastern
Mexico (Tedaw et al. 1985). In the buffer zone, statutory authority and regulations
governing livestock movement help prevent the reestablishment of these ticks in
the U.S. Each month Boophilus ticks are encountered on cattle in shipment from
Mexico, as cattle cross the Rio Grande at low water points, or as the result of a
variety of human endeavors. Thus U.S. rangeland and cattle are under constant
threat of reinfestation.
Boophilus annulatus is a multivoltine, one-host. tick which attacks cattle and
other livestock, horses, and wild ungulates (Celvidae). This t.ick is a primary vector
of Ba. bigemina in temperate and subtropical regions. Tolerance of colder, drier
environments enabled this tick to occupy a much greater area of the U.S. than the
more tropical species, Bo. microplus. For this reason our modelling efforts have
focused on Bo. annu./atus.
Received for publication 17 May 1900: accepted 8 March 1991.
Presented in the Infonnal Conference. ,. Application of Computer Model9 to Medical and Veterinaf)'
Entomological Problems," at the EnlomolO1::icol Society of America Annual Conference and Centennial
Celebration. San Antonio, Texas. December 1989.
291
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J. Agric. Entomol. Vol. 8, No.4 (1991)
The buffer zone crosses the Tamaulipan thorn shl'ubland, a biotope which has
undergone conversion from grassland savanna (Archer et al. 1988). Similar vegetation
associations and meteorological influences of this biotope cross the south Texas
plains and neighboring Mexican states of Tamaulipas and Nuevo Leon, and play
important roles in the ecology of Bo. annulatus. Understanding the ecology of Bo.
annulatus in this biotope is fundamental to surveillance and eradication activities
along the buffer zone.
Aspects of the population dynamics of Bo. an.nulatus essential to surveillance
and eradication include not only the overall length of the off~host phase of the life
cycle, but also its component parts: pre oviposition, oviposition, incubation, and
larval longevity. Abiotic factors, especially temperature and relative humidity, are
principal regulators of these parameters. The duration of quarantine is set to
encompass the maximum off-host survival period from the date eradication
procedures are initiated. Two general procedures nre used: systematic dipping of
cattle in an approved acaricide at 2-wk intervals, or dipping and removal of all
cattle (pasture vacation). A table of quarantine periods was derived from ecological
studies of Bo. annuLatus conducted from 1900 to 1912 in areas ecologically
different from the south Texas plains. Modifications were made to this table in the
1970's to lengthen quarantine periods due to difficulties in eliminating ticks. By its
nature, the table cannot be sensitive to changes in seasonal weather conditions or
to the heterogeneity of rangeland vegetation communities which may lengthen or
shorten tick longevity. Modelling the off-host phase of the life cycle based upon
microclimate associations of dominant vegetation commllllities has been investigated
to offer insight into the ecological factors effecting tick survival and to develop
tools for the application of knowledge under realtime environmental conditions.
The influence of three rangeland vegetation communities on Bo. annuLat.us was
evaluated by introducing engorged female ticks into simulated microenvironmental
temperature and relative-humidity regimes from each community and monitoring
the development and sun'ival of each tick's progeny (P.D.T., D. R. Ring, Dept. of
Entomology, Texas A&M Research and Extension Center, Corpus Christi, Texas,
and M. T. Longnecker, Dept. of Statistics, Texas A&M University, College Station,
Texas, unpublished data). The three vegetation communities were uncanopied
buffelgrass, mesquite-canopied buffelgrass and mixed-brush canopied buffelgrass.
Covariate analyses performed on preoviposition and incubation using degree days
and on larval life using saturation deficit days revealed significant differences
between release dates of the ticks, and between vegetation communities. The
covariate, saturation deficit days, was calculated as the cumulative saturation deficit
above 4 mm Hg. Differences among parameters by release dates reflected the
influence of seasonal meteorological conditions. For example, winter temperatures
greatly extended preoviposition and incubation periods with hatch from over­
wintering cohorts emerging during a comparatively narrow period in spring. The
influence of vegetation community was most pronounced during spring and
summer when canopy attenuated the effects of soiaI' radiation and evapotranspiration.
Success of oviposition, hatch and length of larval life were considerably greater in
canopied compared to uncanopied habitats. Subtle effects on incubation time and
hatch between canopied communities could be ascribed to differences in seasonal
phenology of vegetation communities. Mesquite defoliates during winter and is
usually associated with less dense grass cover beneath the canopy in comparison
TEEL: Ecology of Boophilus ollnulatus
293
to some mixed-brush species which may not defoliate and whose thorns and
physical stature allow grasses to grow around basal stems, building a more
protective thermal shield.
Deterministic models for a parameter were selected from covariate analyses
with the choice for best model based on the lowest root mean square error
(RMSE) in days. Cubic models for preoviposition and incubation were driven by
degree days using thresholds of 9°C and 37°C. Cubic models for larval life and
tot.al off-host period are driven by saturation-deficit days using a threshold of
4 mm Hg. Thresholds were estimated from data inspection procedures (Ring and
Hurris 1984) which used the lowest RMSE as the threshold selection criteria. The
suggestion (Hitchcock 1955) that the amount of desiccation experienced by eggs
could influence length of larval life was upheld by a cubic model of Bo. annulatus
larval life using the saturation deficit experienced by the eggs as the covariate.
The model was highly significant (P < 0.0001) with excellent fit to the data (r2
exceeding 0.91 in all three vegetation types) but accounted for less variation as
indicated by RMSE values two to four times higher than the same model using
saturation deficit experienced by the larvae. The term for saturation deficit
experienced by eggs was significant (P < 0.01). The cubic model containing separate
covariates for saturation deficit experienced by eggs and larvae produced the
lowest RMSE.
The thennal summation (degree day) modelling approach assumes that the
development of an organism is linear over the range of temperatures at which
development occurs. This assumption may provide satisfactory estimates of life
events depending on the organism, the goal of the model, and the extent to which
the organism experiences prolonged exposures to temperatures in the extremes of
the temperature range. The nssumption of linearity for development in poikilo­
thermic organisms is generally valid only over a portion of developmental tempera­
tures (Sharpe and DeMichele 1977). Toward the low and high tempel'8tures
developmental rates become non-linear. Development rates at low temperatures
were a particular concern for attempting to predict incubation periods of 80.
amwlatus during winter, when low temperatures resulted in incubation periods up
to five times longer than those in any other season.
Based upon theoretical associations of temperature and enzyme kinetics of
poikilothermic organisms, Sharpe and DeMichele (1977) developed a biophysical
model to describe developmental rates over the full range of developmental
temperatures. Schoolfield et al. (1981) improved parameter estimation for the
biophysical model through non-linear regression techniques and \Vagner et al.
(I984b) provided a SAS (Statistical Analysis System, Cary, North Carolina)
computer program to simplify application of the model.
Strey et al. (1991) evaluated developmental rates and frequency distributions of
emergence for 80. annulatus under constant temperatures. Embryonic development
occurred from 9 to 42°C with developmental rates at 3° intervals exhibiting a
sigmoid curve. Developmental rates from 12-36 C were subjected to evaluation
and model fitting (Wagner et al. 1984b). A six-parameter biophysical model best
desctibed these developmental rates with regions characterized by low-temperature
(TL = 284.7°K or 11.7°C) and high-temperature (TH = 307.7°K or 34.7°C) enzyme
inactivation and a central linear region (RH025 = 0.049 day-I) of no temperature
Q
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J. Agric. Entomol. Vol. 8, No.4 (1991)
inhibition, Emergence data available for temperatures from 17-36°C were subjected to
a second computer program (Wagner et al. 1984a) to construct cumulative probability
distributions of tick development, normalize these distributions by their median
developmental time, identify a single representative distribution, and fit a th..I'ee­
parameter Weibull function to that singla distribution (Strey et a1. 1991). The
products of these efforts are expected to provide a better understanding of
ecological relationships regulating temporal characteristics of Bo. annulatus populations.
Rangeland quarantined for Bo. annulatus infestation is circumscribed by two
additional quarantine zones (called "adjacent quarantine" and "check-premise
quarantine") which provide for containment of the infested area through inspection
of livestock and horses. The total land area may involve thousands of hectares.
Spatial distribution of heterogenous tick habitats within and across these zones is
an impOltant epidemiologic consideration related to timing swveillance and eradication
activities. Integration of predictive models of events in the off-host phase of the
tick life cycle with spatial distribution of tick habitat-type would improve the
definition of periods of quarantine and surveillance opportunities.
Fleetwood (1985) found signatures of vegetation communities from aerial
infrared photographs of south Texas rangeland vegetation to be a reliable means
of identifying tick habitat type. Hydrologic, topographic, and physiographic features
important in defining and maintaining the physical integrity of quarantine boundaries
can also be obtained from these images. A classification system for vegetation
communities was established and tested on apriol'i infrared images at four levels of
resolution (scales of 1/5,000, 1/10,000, 1/20,000 and 1/58,000) (P.D.T., unpublished
data). Results showed photointerpretation from this source to be highly accurate
through the 1/20,000 scale for defining spatial distributions of tick habitat-types.
Tick models driven by realtime microclimate data from critical vegetation com~
munities could therefore provide both temporal and spatial characteristics of tick
populations on a scale appropriate to areas quarantined for Bo. annulatus. The
problem that remains is linking results of model determinations with spatial
attributes of tick habitat~types across quarantine zones in a manner that will
provide meaningful epidemiologic interpretations.
Models for development and survival of Bo. annulatus are being applied to the
heterogeneity of south Texas rangeland through the use of a Geographic Infonnation
System. Geographic Information Systems (GIS) are computer-based data managers
allowing multiple attributes of spatially oriented data to be indexed, processed and
stored from many sources (maps, photographs, etc,), then examined and evaluated
for criteria of newly defined theme(s} of interest which may be portrayed as visual
or tabulated products (Burrough 1988). The GIS can also communicate with
mathematical models, independent data bases, evaluation functions and statistical
analysis systems, thus opening the environment to the application of Artificial
Intelligence (AD, resulting in Intelligent GIS (IGIS) (Graham et al. 1989, Coulson
et a1. 1991). The application of models through GIS is particularly appropriate in
the Boophilus problem since the greatest proportion of the tick life cycle is
completed in association with well~defined habitats. Lessard et al. (1990) have
demonstrated the use of a GIS to study the epidemiology of cattle diseases in
Africa caused by Theileria parva (Theiler) and transmitted by the tick, Rhipicephalus
TEEL: Ecology of Boophilus annulatus
295
appendiculatus Neumann. This application has been directed at the continent, a
scale and resolution far more coarse than that encompassing a Boophilus quarantine.
We are presently using a GIS called Geographic Resources Analysis Support
System (GRASS) developed by the U.S. Army Corps of Engineers (CERL,
Champaign, Illinois) running on a SUN 386i Computer Workstation to integl'8te
our models of B. annulatus with rangeland landscape characteristics. Figure 1
illustrates the concept with which this integration is being achieved. Microclimate
temperature and humidity profiles from important vegetation communities drive
the calculations of tick development and survival. Results are depicted across the
distribution of tick habitat-types defined from maps and aerial data of the
landscape and across each of the three quarantine zones. The status of each
pasture by quarantine zone with respect to tick development and survival can be
continuously updated from realtime microenvironmental data and linked to animal
census and tick surveillance data sets to provide interpreters with critical ecological
and epidemiological information.
INTERPRETATIONS:
ECOLOGICAL AND
EPIDEMIOLOGICAL
VEOE~noN
Fig. 1.
COhlMLNTlE8
••
~
Overview of a geographic information system to integrate tick develop­
ment and survival models with spatially oriented landscape and quarantine
data, and to analyze interrelationships among specific data themes for
ecological and epidemiological goals.
One of the most difficult problems with Bo. annulatus has been understanding
whether white-tailed deer and cattle, both hosts of this tick, sufficiently interact on
south Texas rangeland to maintain tick populations. Rangeland vegetation and
other landscape features provide the resources with which hosts fulfill their
physiological needs. Their utilization of the landscape influences the distribution
and population dynamics of cattle fever ticks. The application of tick modelling
and GIS is an important fundamental step in approaching this question and
provides a research tool for integrating host-animal behavior on rangeland through
innovative modelling and computer techniques.
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J. Agric. Entomol. VoL 8, No.4 (1991)
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