Selective Host Attachment by Ixodes scapularis (Acari: Ixodidae): Tick-Lizard Associations in the Southeastern United States
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Journal of Medical Entomology, XX(X), 2021, 1–6
https://doi.org/10.1093/jme/tjab181
Research
Population and Community Ecology
Selective Host Attachment by Ixodes scapularis (Acari:
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Ixodidae): Tick–Lizard Associations in the Southeastern
United States
Howard S. Ginsberg,1,6, Graham J. Hickling,2 Genevieve Pang,3 Jean I. Tsao,3,
Meghan Fitzgerald,2 Breann Ross,4 Eric L. Rulison,5 and Russell L. Burke4
1
U.S. Geological Survey, Eastern Ecological Science Center, Field Station at the University of Rhode Island, Kingston, RI, USA,
2
Center for Wildlife Health, University of Tennessee Institute of Agriculture, Knoxville, TN, USA, 3Department of Fisheries and
Wildlife, Michigan State University, East Lansing, MI, USA, 4Department of Biology, Hofstra University, Hempstead, NY, USA,
5
Department of Plant Sciences and Entomology, University of Rhode Island, Kingston, RI, USA, and 6Corresponding author, e-mail:
hginsberg@usgs.gov
Subject Editor: Dina Fonseca
Received 22 July 2021; Editorial decision 4 October 2021
Abstract
Questing behavior and host associations of immature blacklegged ticks, Ixodes scapularis Say, from the south-
eastern United States are known to differ from those in the north. To elucidate these relationships we describe
host associations of larval and nymphal I. scapularis from 8 lizard species sampled from 5 sites in the south-
eastern U.S. Larvae and nymphs attached in greater numbers to larger lizards than to smaller lizards, with
differential levels of attachment to different lizard species. Blacklegged ticks are generally attached to skinks
of the genus Plestiodon in greater numbers per unit lizard weight than to anoles (Anolis) or fence lizards
(Sceloporus). The broad-headed skink, Plestiodon laticeps (Schneider), was a particularly important host for
immature I. scapularis in our study and in several previous studies of tick–host associations in the southeast.
Blacklegged ticks show selective attachment to Plestiodon lizard hosts in the southeast, but whether this results
from behavioral host preferences or from ecological factors such as timing or microhabitat distributions of tick
questing and host activity remains to be determined.
Key words: Ixodes scapularis, lizard, skink, Plestiodon, host associations
Host associations are central features of ixodid tick biology, and is one of the major reasons why Lyme disease cases are far more
they relate to aspects of tick life cycle, survival, phenology, beha- common in northern than in southern states (Ginsberg et al. 2021).
vior, population ecology, and pathogen transmission dynamics. The The importance of small mammal hosts in the natural trans-
blacklegged tick, Ixodes scapularis Say, has a broad host range, es- mission cycle of the Lyme spirochete has resulted in a substantial
pecially in its immature stages, and is the primary vector of Lyme literature on tick–host associations, especially in the northeast
disease spirochetes in the United States (Fish 1993), as well as sev- and northern midwest (Halsey et al. 2018). However, our know-
eral other important pathogens. The primary hosts of larval and ledge of tick–lizard associations in the southeast comes from just
nymphal I. scapularis in the north are small mammals (Spielman a few studies. Rogers (1953) studied host associations of ticks in
et al. 1985), but there is a general shift of host associations with lat- northern Florida, and Apperson et al. (1993) described attachment
itude, such that immature I. scapularis increasingly attach to lizards patterns of I. scapularis to rodents and lizards in the coastal plain
at more southerly sites (Rogers 1953, Apperson et al. 1993, Ginsberg of North Carolina. Three studies looked specifically at associations
et al. 2021). This latitudinal difference in host associations, with effi- of I. scapularis with lizards: Durden et al. (2002) on a coastal
cient Lyme disease spirochete reservoir host species (mice, voles, and Georgia island, Levine et al. (1997) at sample sites throughout North
shrews) in the north and poor reservoir species (lizards) in the south, Carolina, and De Jesus et al. (2021) at several sample sites in Florida.
Published by Oxford University Press on behalf of Entomological Society of America 2021. This work is written by (a) US 1
Government employee(s) and is in the public domain in the US.Journal of Medical Entomology, 2021, Vol. XX, No. XX 2
Oliver et al. (1993) documented ticks found on museum specimens each consisting of 5-gal buckets with drainage holes sunk to ground
of lizards that had been collected throughout the southeast. These level, with drift fencing made of aluminum flashing in a cross pat-
studies provide interesting information about tick–host associations tern; the 5 buckets were located at the center and at the end of each
at scattered southeastern sites, but a comprehensive picture of asso- 10-m arm of the drift fences. Lizards were also collected from the
ciations between I. scapularis and vertebrate hosts in the southeast environment by hand capture or noosing during vertebrate trapping
is still lacking. and tick sampling, which typically lasted 4 days each sample week.
A geographically broad study of host associations for I. scapularis The lizard data used in the analyses of tick numbers were from
in the eastern U.S. (Ginsberg et al. 2021) suggested that southern lizards captured in 2011 and 2012 from which complete data were
ticks showed selective attachment to lizards relative to other hosts, taken (tick numbers and lizard weight in grams). Data on numbers
but provided few details about tick–host relationships among of larval or nymphal ticks per lizard were included only from liz-
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lizard species. In the current paper we add to current knowledge ards that were collected during periods when ticks of that stage were
of southern tick–host associations by analyzing selective attachment known to be active at the site (activity periods were based on dates
patterns of ticks among lizard species, and describing tick–lizard re- when ticks were present in any of the sample types, including collec-
lationships based on 2 yr of intensive sampling efforts at 5 sites scat- tions from all hosts and from the environment; details in Ginsberg
tered throughout the southeastern U.S. et al. 2021). Each lizard was examined for up to 5 min, and ticks
collected from the lizards were placed in 95% ethanol and returned
to the lab for confirmation of identification. Tick abundance on
Materials and Methods each lizard species was quantified as the number of ticks per lizard
Lizard Sampling from Field Sites (total number of ticks of a given stage collected from a lizard spe-
cies divided by the total number of lizards of that species exam-
Lizards were sampled from 5 field sites (Fig. 1) in the south-
ined). Animals were handled in accordance with approved IACUC
eastern U.S. (south of Virginia and east of the Mississippi River):
protocols from the University of Rhode Island (protocol AN09-
Mattamuskeet National Wildlife Refuge, NC (35.48 N, −76.31 W),
04-016), University of Tennessee (1846-0512), Georgia Southern
Arnold Air Force Base, TN (35.33 N, −86.10 W), Savannah River
University (I09011, I11004), Michigan State University (06/09-094-
Site, SC (33.29 N, −81.73 W), Oakmulgee Talladega National
00), Hofstra University (08/09-7, 10/11-8, 11/12-9), and Patuxent
Forest, AL (32.96 N, −87.46 W), and Tall Timbers Research Station,
Wildlife Research Center. Research and collecting permits were
FL (30.66 N, −84.21 W). Samples were taken from 2 to 3 sampling
obtained from appropriate site, state, and federal levels, and are
arrays at each site every third week in 2011 and 2012. Each sample
available on request.
array consisted of a 7 × 7 grid of mouse traps, 15 m apart, with 4
traps for medium mammals at the edges (total array size, 1 ha; de-
tails provided by Ginsberg et al. 2021). Lizards were sampled from Statistical Analysis
these arrays using coverboards, burlap skirts on trees, pitfall traps, Numbers of ticks per lizard in the field samples (Table 3) were ana-
and by hand capture and noosing. Each array had 20 pairs of ply- lyzed with generalized linear models (SAS, version 9.4, GENMOD
wood and corrugated metal coverboards, each 0.6 × 0.6 m, distrib- procedure), using negative binomial models with the number of ticks
uted evenly on the array. Burlap skirts (20 1-m2 burlap squares) were per individual lizard as the dependent variable. Independent vari-
attached at breast height on trees near the coverboards. There were ables included site, year, and lizard species as classification variables,
4 pitfall trap arrays (1 pitfall array at each edge of the sample array), and lizard weight (in g) as a metric variable. The numbers of ticks
Fig. 1. Tick–lizard sample sites in the southeastern United States.3 Journal of Medical Entomology, 2021, Vol. XX, No. XX
numbers of ticks per lizard were related to size of the lizard (mass in
g), with the strongest models (lowest AIC) including site, year, and
lizard species as classification variables for both larvae and nymphs
(Table 3). These results suggest that tick attachment is related to
lizard size, but also that different lizard species differ in attachment
levels of I. scapularis. We tested this possibility by analyzing the
number of attached ticks per gram lizard for each of the eight lizard
species, and found higher levels of attachment to skinks (Plestiodon
spp.) than to anoles, fence lizards, or racerunners (Fig. 2). This ge-
neral result is moderated somewhat by the large variability in ticks
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per unit weight within lizard species (Fig. 2), and also because lizard
presence and abundance, and tick density varied among sample sites
(Table 2). The site with the highest tick density and multiple lizard
species was the Florida site, where the number of ticks per gram
weight was significantly greater (P < 0.05) on P. laticeps than on
S. undulatus for both larvae and nymphs. However, the sample size
for A. carolinensis was just 7 individuals, so though we found no
ticks on this species the differences to most other lizard species were
not significant.
Our results are compared to those from 6 previous studies of
ticks collected from southeastern lizards in Table 4. We did not
capture specimens of Eastern glass lizards, Ophiosaurus ventralis
(Linnaeus), but this species was present in several previous collec-
tions and is included in Table 4. Broad-headed skinks (P. laticeps)
were important hosts of immature I. scapularis at all sites where they
were present and where data on this species were available.
Discussion
Our results support the hypothesis that larval and nymphal
I. scapularis display selective attachment to different lizard taxa in
Fig. 2. Mean number of ticks per gram weight of lizard (±SE), for eight lizard the southeastern U.S. (Fig. 2). Ticks are generally more abundant on
species from five southeastern sites, 2011–2012. Species codes as in Table 1;
larger lizards (Table 3), as was reported by Hayashi and Hasegawa
N denotes sample sizes; and different letters indicate significant differences
(1984b) for I. asanumi feeding on P. okadae. Furthermore, skinks
(P = 0.05) by Tukey Multiple Comparisons.
of the genus Plestiodon tend to be utilized as hosts far more than
anoles or fence lizards (Fig. 2). Glass lizards sometimes have large
Table 1. Lizard species sampled in the southeastern U.S. numbers of attached ticks, but sample sizes of Ophiosaurus were
too low in our study to draw conclusions about their importance
Species Code Common name as hosts, and results from previous studies have varied (Table 4).
Plestiodon fasciatus (Linnaeus) PLFA Five-lined skink Ophiosaurus spp. are widespread in the southeastern and central
Plestiodon inexpectatus (Taylor) PLIN Southeastern five- U.S., but they generally occur at low densities (RLB, personal ob-
lined skink servation). Racerunners had relatively low numbers of ticks in our
Plestiodon laticeps (Schneider) PLLA Broad-headed skink samples (Fig. 2) and in several previous studies (Table 4), but most
Scincella lateralis (Say) SCLA Ground skink racerunners in our study were collected at one site with only modest
Anolis carolinensis Voigt ANCA Green anole tick numbers overall (Table 2), so the role of A. sexlineatus as a host
Sceloporus undulatus (Bosc & SCUN Eastern fence lizard for I. scapularis requires additional study.
Daudin)
These attachment patterns are compatible with those reported
Ophiosaurus attenuatus Baird OPAT Slender glass lizard
from regions outside of our sample area. Plestiodon skinks were im-
Aspidoscelis sexlineatus (Linnaeus) ASSE Six-lined racerunner
portant hosts for I. scapularis in samples from Missouri (Kollars
et al. 1999), as well as from Oklahoma and Arkansas (Garvin et al.
2015, McAllister et al. 2013), with a lesser role for fence lizards.
per gram lizard weight (Fig. 2) were analyzed using analysis of var- Studies at northern sites showed substantial numbers of ticks per
iance (SAS, version 9.4, GLM procedure), with lizard species separ- skink in Maryland and New York (Giery and Ostfeld 2007) and in
ated using Tukey Multiple Comparison tests. Wisconsin (Ginsberg et al. 2021), but low utilization of fence lizards
in Maryland and New York (Giery and Ostfeld 2007) and in New
Jersey (Rulison et al. 2014).
Results Plestiodon skinks are speciose (about 50 species) and widespread
Lizard samples from five southeastern field sites captured eight spe- (east Asia, Pacific Islands, North and South America, Caribbean) but
cies of lizards (Table 1). Mean numbers of I. scapularis ticks per lizard poorly studied in most places. We found a particularly close relation-
at these sites showed the highest numbers of larvae and nymphs at- ship between Plestiodon skinks and I. scapularis ticks in the south-
tached to skinks of the genus Plestiodon, with substantially lower east, and various species of Ixodes have been reported on Plestiodon
numbers on anoles, fence lizards, and racerunners (Table 2). The skinks elsewhere. In western North America, I. pacificus feeds on P.Journal of Medical Entomology, 2021, Vol. XX, No. XX 4
Table 2. Ticks collected from lizards at sample sites in the southeastern U.S., 2011–2012
Site Plestiodon Plestiodon Plestiodon Scincella Anolis Sceloporus Ophiosaurus Aspidoscelis
fasciatus inexpectatus laticeps lateralis carolinensis undulatus attenuates sexlineatus
Larvae
NC 1.7 (6) – 0 (1) 1.0 (1) – – – –
TN 0.5 (2) – – – – 2.0 (2) – –
SC – 1.0 (2) 1.2 (43) 0.2 (49) 0 (45) 0.2 (38) 0 (2) 0 (24)
AL 5.8 (4) 0.8 (6) 1.3 (4) – 0 (4) 0 (7) – –
FL 7.0 (5) – 5.2 (128) 0.3 (9) 0.1 (7) 0.7 (42) – –
Nymphs
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NC 0.2 (6) – 0 (1) 0 (1) – – – –
TN 0.2 (2) – – – – 0 (6) – –
SC 0.3 (3) 1.3 (16) 0.9 (58) 0(66) 0 (82) 0.1 (58) 1.0 (2) 0.04 (26)
AL 0.7 (6) 0 (1) 3.0 (2) – 0 (1) 0.4 (7) – –
FL 0.5 (6) – 3.8 (128) 0.1 (9) 0 (7) 0.2 (42) – 0 (1)
NC = Mattamuskeet National Wildlife Refuge, North Carolina, TN = Arnold Air Force Base, Tennessee, SC = Savannah River Site, South Carolina,
AL = Oakmulgee Talladega National Forest, Alabama, FL = Tall Timbers Research Station, Florida. Entries are mean numbers of ticks per lizard, with number of
lizards sampled in parentheses. Dashes indicate that there were no data on ticks of that stage from that lizard species at that site.
Table 3. Generalized linear models (negative binomial) of numbers of ticks per lizard as a function of lizard mass, 2011–2012
Stage Variables in model AIC Role of lizard mass (g)
Wald χ2 P
Larvae Site Year Species Lizard mass 1113.845 3.32 0.068
Site Year Lizard mass 1165.963 18.085 Journal of Medical Entomology, 2021, Vol. XX, No. XX
skiltonianus (Tanner 1957, Wright et al. 2011) and P. gilberti (Castro different time scales, and their interactions, which might evolve, are
and Wright 2007), and in the Izu Islands (Japan), I. asanumai is an difficult to predict.
important parasite of P. okadae (Hayashi and Hasegawa, 1983, We conclude that southern, I scapularis immatures generally
1984a,b). attach more commonly to skinks of the genus Plestiodon than to
The clear evidence of selective attachment by southern anoles or fence lizards. Research is needed to determine the reasons
I. scapularis to lizards rather than mice (Ginsberg et al. 2021) and for this pattern, and the relationship of this pattern to regional dif-
to skinks rather than to anoles or fence lizards (Fig. 2 and Table 4), ferences in tick questing behavior.
begs the question of why immature blacklegged ticks display this
pattern. Are these true behavioral preferences, where a tick given a
choice would choose one host over the other, or do they result from Acknowledgments
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ecological factors such as questing height and time of questing rela- Numerous students, technicians, and research associates contributed to this
tive to microhabitat distributions or activity patterns of the different project. In particular, we thank K. Anacito, I. M. Arsnoe, C. Chan, J. Dickson,
hosts? These are difficult distinctions to study, and our results do not R. Gerhold, K. Jackson, S. Kinsey, L. Kramer, T. Lewis, L. Maesta, T. Moody,
provide clear answers. J. Parham, C. Parmer, and C. Scott for their contributions. The staffs at our
Southern I. scapularis are known to differ in questing behavior study sites were always helpful. We thank C. De Jesus and S.M. Wisely who
from northern populations, in that they tend to stay below the leaf kindly provided data that allowed us to use their recent results (De Jesus et al.
litter while northern ticks climb to leaf tops and twigs at the litter 2021) in Table 4. We thank Scott Buchanan for constructive comments on
surface to seek hosts (Arsnoe et al. 2015, 2019; Tietjen et al. 2020). an early draft of the manuscript. This project was supported by the National
Science Foundation Ecology of Infectious Diseases Award EF-0914476 with
This behavioral difference could be related to climate, because the
additional support from the U.S. Geological Survey. Any use of trade, firm, or
higher southern temperatures increase desiccation stress above the
product names is for descriptive purposes only and does not imply endorse-
leaf litter, possibly selecting for questing sites down below the leaf
ment by the U.S. Government.
litter surface (Ginsberg et al. 2017). However, these differences could
also result from adaptation to different hosts; skinks in the south
and mice in the north. Given current knowledge, it is not clear how References Cited
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