Discussion
In the host-parasite system we studied, chigger mites (E.
alfreddugesi ) are highly abundant in the environment, and all age- and
sex-classes (adults and juveniles; males and females) of S.
undulatus are heavily parasitized (Pollock & John-Alder, 2020).
However, we found no evidence that mites impose a growth cost, despite
very high mite loads and consistent week-to-week rank ordering of mites
on individual lizards. Indeed, within cohorts of yearlings, growth rate
is unambiguously not correlated with mite load in either sex.
Furthermore, across cohorts, both growth rate and mite loads were higher
in 2019 than in 2016, which is opposite the prediction if mites imposed
a growth cost. At any given mite load, females grow more quickly than
males, which could suggest that mites impose a sex-biased growth cost.
However, even in captivity in the complete absence of mites, SSD
develops because females grow faster to become larger than males (Duncan
et al., 2020). Thus, we find no evidence that growth rate in yearling
juveniles of S. undulatus is affected by chigger mite
ectoparasitism. It follows that the temporal correlation between the
development of SSD and the seasonal attainment of sex-biased mite loads
in July does not reflect a sex-biased growth cost of chiggers.
Our findings match those of several other studies that found no
significant effects of mite parasitism in lizards. In S.
virgatus , Abell (2000) reported no relationship between mite load and
body condition, mating success, or survivorship to the following year,
and Smith (1996) found no significant relationship between mite load and
growth rate. In the anole species Norops polylepis , Schlaepfer
(2006) found no sex differences in mite load and no growth costs
associated with mite ectoparasitism. Mite parasitism was not associated
with body condition in Gallotia atlantica lizards (García-Ramírez
et al., 2005). Patterson and Blouin-Demers (2020) found no relationships
between mite load and growth rates or survival in six different
populations of Urosaurus ornatus . One caveat worth mentioning is
that mite loads in the studies cited here were substantially lower than
those on S. undulatus in the present study (S. undulatus :
0–435mites; U. ornatus : 0–120; N. polylepis :
0–37 mites, G. atlantica : 1–28 mites).
In contrast to our findings and the studies cited above, evidence of
costs of mite parasitism has been reported in several species, including
two close congeners of S. undulatus . An experimental study onS. virgatus found twice as many mites on males as on females and
a strongly negative correlation between mite loads and growth rate (Cox
& John-Alder, 2007). This result suggests that growth costs of mite
ectoparasitism are greater in males than females (Cox & John-Alder,
2007), in contrast to what had previously been reported (Smith, 1996;
Abell, 2000). In S. woodii , Orton et al. (2020) reported that
both color quality and running endurance are negatively associated with
mite load. In collared lizards (Crotaphytus collaris ), Curtis and
Baird (2008) found evidence of a growth cost associated with heavy
parasitism during the peak growing season. That study reported high mite
loads, an average of 178.3 ± 65.2 mites on yearling male lizards, which
are comparable to what we found on S. undulatus in the
present study.
Overall, the inconsistent narrative regarding potential growth and
fitness costs of mites suggests that effects of, or correlates of, mite
parasitism can depend on which life history trait is being investigated
and the timing of the studies, as ecological conditions (i.e.,
temperature, precipitation, food abundance, etc.) can fluctuate across
the years and have different effects on life history traits.
Furthermore, effects of mite parasitism can differ not only among
species but also between populations of the same species as observed
with the studies on S. virgatus (Smith, 1996; Abell, 2000; Cox
and John-Alder, 2007). As such, it would be problematic to envision an
overall evolved strategy to mite parasitism at a species level.
Furthermore, future studies need to consider what life history trait is
being examined when investigating potential effects of ectoparasitism.
While not a major consideration in our study, we posit that future
studies on the costs of mite parasitism in lizards should consider
whether the host population in the system would be expected to have
evolved a strategy of resistance or tolerance towards the parasites in
their study design. Parasites and their hosts coevolve in an
evolutionary arms race in which parasites extract resources from their
hosts, while hosts try to prevent or minimize the fitness costs of
parasitism (May & Anderson, 1983; Restif & Koella, 2004; Carval &
Ferriere, 2010). Within this context, hosts evolve strategies of
resistance or tolerance to parasites, or some combination of the two.
The ecological relationship between the populations of S.
undulatus and E. alfreddugesi in this study (i.e., high
environmental mite abundance and high host mite loads) is typical of a
host-parasite system in which the host would be expected to have evolved
tolerance to parasites (Råberg et al., 2009; Pollock & John-Alder,
2020). Hosts can evolve tolerance so effectively that the reduction in
fitness caused by parasites may not be measurable (Råberg, 2014).
Studies that do not find a growth cost associated with parasitism may be
examining systems where the lizards have evolved a strategy of tolerance
towards the mites. For example, it has been hypothesized that mite
pockets evolved as a compensatory mechanism for reducing the harm caused
by mite ectoparasitism because they concentrate mites in areas better
equipped to heal and where they do not interfere with other functions,
such as movement and vision (Arnold, 1986; Salvador et al., 1999; de
Carvalho et al., 2006; Reed, 2014). Tolerance can be quantified using
the slope of the relationship between fitness (or its proxy) and
parasite burden (Burgan et al. 2019). Given that we found a slope of
zero in the relationship between growth rate and mite load, our
population of eastern fence lizards is highly tolerant of chiggers by
the criteria we evaluated (Råberg et al., 2007; Råberg, 2014). Ornate
tree lizards (Urosaurus ornatus ) have also been found to be
highly tolerant of mite parasites (Paterson & Blouin-Demers, 2020).
Host-parasite systems in which hosts appear to be highly tolerant of the
parasite are not well-suited for investigating sex-biased costs of
parasitism because any costs of parasitism are not easily measurable.
If chigger mites in our study population are in fact extracting a
substantial cost from yearling S. undulatus , the cost may be at
the expense of traits and functions other than growth. Rapid growth is
expected to be under strong selection to ensure that yearlings grow to
the minimum size of reproduction by the end of their first full activity
season (Adolph & Porter, 1996; Haenel & John-Alder, 2002).
Furthermore, female body size is positively correlated with clutch size,
suggesting strong fecundity selection on body size and thus yearling
growth (Angilletta et al., 2001; Haenel & John-Alder, 2002; Cox et al.,
2003; Brandt & Navas, 2011; Jiménez‐Arcos et al., 2017). Thus,
potential explanations for the absence of growth costs could include
that costs of parasitism are 1) traded off against other functions, 2)
too small to be of any consequence, or 3) compensated by increased
dietary consumption. We now consider each of these possibilities.
If mites do impose costs on juveniles of S. undulatus , it seems
likely that a potential growth cost might be traded off against other
traits (Adolph & Porter, 1996). For example, reduced activity is one of
the apparent costs of parasitism in common lizards (Lacerta
vivipara ) and Western fence lizards (Sceloporus occidentalis )
(Clobert et al., 2000; Megia-Palma et al., 2020). In the present study,
we did not quantify a specific measure of activity in S.
undulatus . However, in a 2019 companion study conducted at our study
site and on the same population of S. undulatus we found that
home range area is greater in yearling males than in females (1101 ± 327
m2 vs 233 ± 62 m2) and is not
correlated with growth rate (F2,1 = 0.14, p =
0.708), even while mite loads are greater in males than in females
(Conrad, 2019; Yawdosyn, 2019). Home range area can be used as a proxy
for energy expenditure on activity to assess the possibility of a
trade-off against activity instead of growth (Christian & Waldschmidt,
1984; Hews, 1993; Main & Bull, 2000; John-Alder et al., 2009). Thus,
our evidence suggests that mites do not impose an activity cost of mite
ectoparasitism. However, while home range area can be used as a first
approximation of activity, a study of the close congener S.
occidentalis reported that lizards infected with malarial parasites
maintained the same home range area as unparasitized lizards but showed
reduced daily activity (Schall & Houle, 1992). Thus, time-intensive
focal observations would be required for a definitive determination of
whether mites impose an energetic cost on S. undulatus as seen
through reduced activity.
Lacking evidence of costs of mite parasitism, it is possible that mites,
even in high numbers, may not impose a measureable energetic cost,
either directly or indirectly. We estimated the energetic cost of a
single chigger mite to be approximately 0.004 J/day using estimates of
chigger mite body size (body length = 0.4 mm, body mass = 0.9 μg;
Johnson & Strong, 2000) and the metabolic scaling exponent of 0.75
(West et al., 2002). Taking the mean mite loads of yearling male lizards
in June 2016 (58 mites), July 2016 (138 mites), June 2019 (93 mites),
and July 2019 (119 mites), the average energetic costs of mite
ectoparasitism for yearling male lizards would have been 0.232 J/day in
June 2016, 0.552 J/day in July 2016, 0.372 J/day in June 2019, and 0.476
J/day in July 2019. For comparison, the energetic cost of growth is
about 130 J/day for yearling males (Cox et al., 2005). Thus, in the
aggregate, mites imposed an energetic cost that was a mere
0.002–0.004% of the energy cost of growth.
The energetic cost of direct energy extraction by mites is unlikely to
be detectable as a growth cost because of its low value. These
estimations, however, do not account for the potential indirect
energetic costs of mounting an inflammatory immune response or the
accompanying stress to the lizard in response to mite ectoparasitism,
which we did not measure. However, potential energetic costs of immune
or stress responses are far from certain. A meta-analysis by van der
Most et al. (2011) found that selection for growth compromises immune
function, but selection for immune function does not appear to affect
growth. This suggests that the costs of growth are large relative to the
costs of immune function. A study of parasites in side-blotched lizards,Uta stansburiana , found increased immunocompetence associated
with parasitism, but no other measurable costs (Spence et al., 2017).
Despite the lack of measurable costs in U. stansburiana , it can
be costly for a host to up-regulate their immune system in response to
parasites, forcing life-history trade-offs over time (Sheldon &
Verhulst, 1996; Lochmiller & Deerenberg, 2000; French et al., 2009).
Overall, while there may be some energetic cost to immunity, those costs
are likely to small to be detectable as costs to growth. However, more
research is certainly needed in this area.
Finally, growth and body condition may not have been associated with
mite ectoparasitism in S. undulatus because environmental
conditions favorable for ectoparasitism were at the same time favorable
for abundant prey, including other arthropods and possibly even mites
themselves. Thus, even while they were heavily parasitized by mites,
lizards would be enabled to increase their energy consumption and
compensate for costs of a high parasite load. The spring of 2019 had
more precipitation and higher temperatures than the spring of 2016
(http://climate.rutgers.edu/stateclim_v1/nclimdiv/), and we saw an
increase in both environmental mite abundance and lizard growth in 2019
as compared to 2016. Increased precipitation would have increased soil
moisture and humidity, which are positively correlated with the
abundance of arthropods, including mites (Zippel et al., 1996; Kardol et
al., 2011; Prather et al., 2020). Temperature has also been shown to be
positively correlated with arthropod abundance (Lessard et al., 2011).
Mite activity is increased by a combination of moderately high
temperatures and high humidity (Clopton and Gold, 1993). At the same
time, higher temperatures can create opportunities for increased daily
activity in S. undulatus , while also contributing to increased
growth rates and faster maturation (Adolph and Porter, 1996). Greater
arthropod abundance may have increased food availability for S.
undulatus as well, facilitating increased growth. A greater
understanding of the ecological interactions between S.
undulatus , mites, and other arthropods could show if lizards predate
upon the mites or increase their feeding rates on other arthropods due
to increased mite ectoparasitism.
In summary, there are many possible explanations for why we did not find
a growth cost associated with mite parasitism in either sex of S.
undulatus in this study, even when males had higher mite loads than
females. Female-larger SSD still developed in our study population. So,
it is safe to conclude that sex-biased costs of mite parasitism are not
contributing to the development of SSD in our study population ofS. undulatus . The lizards in our study population appear to be
highly tolerant of mite ectoparasitism, but definitive experimental
studies are required to rule out various trade-offs and effects of
environmental food abundance. As such, while our study population also
exhibits the common male-biased pattern of ectoparasitism, it also shows
that we should be careful in making conclusions about the implications
of sex differences in parasite intensity and prevalence.