Modification of the Daily Activity Pattern of the Diurnal Triatomine Mepraia spinolai (Hemiptera: Reduviidae) Induced by Trypanosoma cruzi ...
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Journal of Medical Entomology, 58(6), 2021, 2474–2478
doi: 10.1093/jme/tjab118
Advance Access Publication Date: 1 July 2021
Research
Vector/Pathogen/Host Interaction, Transmission
Modification of the Daily Activity Pattern of the Diurnal
Triatomine Mepraia spinolai (Hemiptera: Reduviidae)
Induced by Trypanosoma cruzi (Trypanosomatida:
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Trypanosomatidae) Infection
G. Pérez,1 C. Muñoz-San Martín,1,2 F. Chacón,1 A. Bacigalupo,1,3, P. E. Cattan,1 and
R. Solís1,4,
Depto. Cs. Biológicas Animales, Facultad de Cs. Veterinarias y Pecuarias, Universidad de Chile, Casilla 2, Correo 15, Santiago,
1
Chile, 2Núcleo de Investigaciones Aplicadas en Ciencias Veterinarias y Agronómicas, Universidad de las Américas, Campus
Providencia, Santiago, Chile, 3Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow,
UK, 4Corresponding author, e-mail: rsolis@uchile.cl
Subject Editor: Gabriel Hamer
Received 21 February 2021; Editorial decision 31 May 2021
Abstract
Mepraia spinolai, (Porter) 1934, is a diurnal triatomine endemic to Chile and a wild vector of the protozoan
Trypanosoma cruzi, (Chagas) 1909, which causes Chagas disease. Behavioral changes in M. spinolai induced
by this parasite have been reported previously, which include detection of a potential host, defecation latency,
and some life history traits. In this study we assessed changes in locomotor and daily activity due to infection
with T. cruzi. No difference was detected in distance traveled between infected and uninfected individuals.
However, the groups differed in their daily activity patterns; infected individuals showed significant reduction
of movements during the light phase and concentrated their activity in the dark phase. Uninfected individuals
showed no differences in locomotor activity between the phases. The results suggest that T. cruzi induces a
displacement in the activity of M. spinolai toward the dark phase of the circadian cycle, which may improve its
vector competence.
Key words: triatomine, Trypanosoma, infection, behavior, activity
The ability of some parasites to manipulate the behavioral pheno- et al. 2007, Botto-Mahan et al. 2008, Botto-Mahan et al. 2010,
type of their hosts and thus facilitate their transmission has been Córdova 2010, Oda et al. 2014, Jiménez et al. 2015) and prevalence
long recognized for many species (Moore 1995, 2013, Poulin and of T. cruzi in its populations can reach up 76.1% (Coronado et al.
Maure 2015). The protozoan parasite Trypanosoma cruzi Chagas 2009). Diverse modifications in the behavior of M. spinolai induced
1909 (Trypanosomatida: Trypanosomatidae), causal agent of by T. cruzi include: latency to detect a host, defecation, and bite rate
the zoonotic Chagas disease in America, is able to induce behav- (Botto-Mahan et al. 2006), all favoring transmission of the parasite.
ioral changes in several of its hematophagous triatomine vectors Locomotor activity acquires importance, since it mediates the inter-
(Reduviidae: Triatominae) (Guarneri and Lorenzo 2017, Ramírez- action between triatomine vector and its host’s source of bloodmeal
González et al. 2019). (Marliére et al. 2015).
In Chile, the kissing bug Mepraia spinolai, Porter 1934 Recent evidence indicates that some trypanosomatid species may
(Hemiptera: Reduviidae), is mainly involved in the wild transmission modify the locomotor behavior of their triatomine hosts (Ramírez-
cycle of T. cruzi (Botto-Mahan et al. 2015, 2020) because of the size, González et al, 2019). T. cruzi-infected individuals of the triatomine
number of their populations, and geographical range of distribution vector Rhodnius prolixus Stål (Hemiptera: Reduviidae) showed
(Garrido et al. 2019). This triatomine feeds on wild and domestic significantly less locomotor activity than control insects during
mammals, including humans (Lent and Wygodzinsky 1979, Rozas scotophase and greater locomotor behavior during photophase when
© The Author(s) 2021. Published by Oxford University Press on behalf of Entomological Society of America. 2474
All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.Journal of Medical Entomology, 2021, Vol. 58, No. 6 2475
this species was infected with Trypanosoma rangeli (Marliére et al. highest activity (Canals et al. 1997). After 30 s to acclimate to the
2015). Like R. prolixus, most triatomines are nocturnal, developing arena, a continuous recording of 15 min followed. The variables
more intense activity during scotophase (Barrozo et al. 2017). In measured were speed and distance traveled by the insect during the
contrast, M. spinolai has been described as a diurnal triatomine spe- recording period.
cies (Schenone et al. 1980), with higher activity during photophase
and negligible movement in the scotophase (Canals et al. 1997). The Daily Locomotor Activity
aim of this study was to assess the effect of T. cruzi on the locomotor These tests were performed with third-instar nymphs according to
behavior and activity pattern of this diurnal triatomine. We hypoth- the availability of the different ontogenetic stages at the time of
esize that T. cruzi modifies these aspects of M. spinolai in a manner their execution. The activity exhibited during the photophase and
that increases its vectorial competence. In this respect, there is sup- scotophase of 12 uninfected and 12 T. cruzi-infected nymphs was
porting evidence showing behavioral changes other than locomotor measured. Before starting each trial (30 min), a bug was transferred
activity that have an impact on that attribute (Botto-Mahan et al. from the maintenance jar to the experimental arena. For insects of
2006, Botto-Mahan et al. 2015). In addition, these behavioral modi- both groups, activity was recorded first during photophase (12 h),
fications could facilitate an ongoing colonization process of human and then after 7 d of cycle inversion, activity during scotophase
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dwellings (Canals et al. 2000, Canals et al. 2017). (12 h) was assessed. This was done in order to adapt the measure-
ments to the work schedule of the researchers and it has been a
strategy adopted in a prior study with arthropods (Solís et al. 2018).
Materials and Methods
Photophase and scotophase began at 0900 and 2100 h local time,
Nymphs of M. spinolai were obtained from a lab-reared colony respectively.
not infected with T. cruzi maintained in a climate chamber at 27 ± Triatomine activity was quantified as the number of movement
1°C, 70% RH, and exposed to a daily cycle of light:dark of 12:12 h events (ME) made in each hour of the phases of the photoperiod. An
(Ehrenfeld et al. 1998). Insects were placed individually in plastic ME consisted of a change in position equal to or greater than the
screw cap containers provided with folded paper as shelter. Two ex- body length of the nymph.
perimental groups were formed, whose members were fed every 45
d since nymph stage III on naturally T. cruzi-infected and uninfected Statistical Analysis
rodents, Octodon degus, respectively. These rodents were captured Nonparametric statistics were used because the data did not fit
in the Region V of Chile, and the specific infecting discrete typing the normal distribution and the sample size available to study the
units of the trypanosome were unknown. However, it is probable activity pattern. The Mann–Whitney U test for two independent
that the infection consisted of a mix of T. cruzi lineages, surely con- samples was applied to compare body weight and distance trav-
taining TcI strain (Campos et al. 2007, Rojo et al. 2017). The status eled by individuals of both groups. Intragroup comparison of the
of T. cruzi infection was determined from the feces of the nymphs locomotor activity (number of ME) exhibited during photophase
and the experiments were done after about 60 d of starvation. and scotophase was done with Wilcoxon signed-rank tests. Because
To confirm the infection status of nymphs, a pool of feces from three infected nymphs died, for intergroup comparisons the number
each triatomine was spontaneously obtained after feeding and of ME was standardized by the corresponding number of individuals
each sample analyzed with quantitative polymerase chain reaction (infected = 9; uninfected = 12). After this procedure, a Friedmann
(qPCR) as previously described (Mc Cabe et al. 2019). All experi- test was applied with the following groups of insects as treat-
ments were conducted under measures approved by the Animal ments: uninfected-photophase; infected-photophase; uninfected-
Bioethics Committee of the Faculty of Veterinary Science, University scotophase, and infected-scotophase. Post-hoc pairwise multiple
of Chile (Certificate Nº 18169-VET-UCH). comparison tests were conducted to discern significantly different
pairs. All analyses were carried out with the statistical software
Behavioral Recordings InfoStat (Di Rienzo et al. 2008).
Recordings were made in an experimental chamber (0.6 m wide ×
1.3 m long × 1.5 m high) with the same environmental conditions
of rearing. A bulb producing a maximum intensity of 65 lux and Results
two infrared (IR) illuminators were used; one to record the light As shown in Table 1, no differences were determined in the dis-
phase and one for the dark phase of the cycle. The chamber was tance traveled or speed between infected and uninfected fifth-instar
fitted with a PANASONIC WV-CP 504 high resolution digital video nymphs, despite the fact that infected bugs were significantly heavier
camera connected to the Ethovision XT version 8.0 system (Noldus than the uninfected (Table 1).
Information Technology, Wageningen, The Netherlands), which The number of ME during photophase and scotophase was not
made it possible to monitor (sampling rate of one frame per second) different in uninfected triatomines. In contrast and remarkably, in-
and quantify the movements of the triatomines throughout the trials fected insects showed significantly more activity during scotophase
(Solís et al. 2018). Locomotor behavior and daily activity of the bugs than photophase (Table 2). In the dark phase they exhibited 78.9%
was measured individually. In each trial, a nymph was placed in an of the total locomotor activity.
experimental arena, which consisted of a white circular plastic con- Effects of the photoperiod and infection status were verified
tainer (18 cm × 6.5 cm) installed inside the experimental chamber. (Friedmann test: 10.76, P < 0.001). Multiple comparisons showed
differences between activity exhibited by infected nymphs during
Locomotor Behavior photophase and other status-phase conditions. However, an hour
The locomotor behavior of 27 uninfected and the same number of to hour comparison of the locomotor activity of the groups in
infected fifth-instar nymphs of M. spinolai was measured. These ex- photophase and scotophase revealed that the greatest and sig-
periments were carried out during the first 3 h of the photophase, nificant differences occurred during the first and final hours of
which corresponds to the period in which this triatomine shows the the photophase. During the first part of this phase, uninfected2476 Journal of Medical Entomology, 2021, Vol. 58, No. 6
Table 1. Summary of average values ± SD measured in the groups of uninfected and infected fifth-instar nymphs used to assess
locomotor behavior
Variables Uninfected (n = 27) Infected (n = 27) Mann–Whitney U test P level
Body mass (g) 0.09 ± 0.04 0.15 ± 0.07 965 P < 0.001
Distance traveled (cm) 19.81 ± 11.15 20.13 ± 18.88 672 P = 0.222
Speed (cm/s) 0.04 ± 0.06 0.03 ± 0.02 653 P = 0.121
Table 2. Comparisons of the locomotor activity measured as movement events (ME: a position shift not less than the body length of the
bug) of uninfected and infected third-instar nymphs of M. spinolai during photophase and scotophase. (± SD)
Variables Uninfected Infected P level
Photophase Scotophase Photophase Scotophase
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Total ME 1132 1455 P = 0.269a
255 951 P = 0.046a
Standardize average of ME 7.87 ± 2.79 2.38 ± 2.6 P < 0.001b
10.11 ± 4.81 8.79 ± 3.62 P = 0.837b
a
Wilcoxon test; bMann–Whitney U test.
(Table 1). This is striking, since taking into account the difference in
the weight of the groups, the infected insects had to spend around
40% more energy to travel the same distance in the same time than
uninfected ones. Perhaps this behavior reflects an intense appetitive
behavior driven by T. cruzi, similar to that reported in relation to
detection and orientation toward the host in M. spinolai (Botto-
Mahan et al. 2006) and other related triatomines (Ramírez-González
et al. 2019). Based on the results obtained in the daily activity ex-
periments, an alternative explanation could be that the differences
would have become apparent if the experiments had been performed
during the scotophase. In any event, because nymphs of different
instar were used in experiments of locomotor behavior (instar V)
and daily activity (instar III), this explanation must be considered
with caution.
Since starvation time was similar for both groups, the reduc-
tion in locomotor activity of infected nymphs (III) would not be ex-
plained by this variable or nutrition status (Guarneri and Lorenzo
Fig. 1. Locomotor activity pattern exhibit by uninfected (white dots) and 2017), since body condition was similar (medium abdominal disten-
infected (black dots) Mepraia spinolai nymphs during photophase and sion), which is a good estimate of the nutritional status of the insects
scotophase. Hours correspond to local time. (Estay-Olea et al. 2020).
Locomotor activity of uninfected insects did not differ be-
individuals showed negligible activity and a brief but low intense tween light and dark phases of the photoperiod, which contrasts
peak of activity afterward (Fig. 1). During scotophase a contrasting with the mostly diurnal activity seen previously in M. spinolai in
trend was observed in the groups. After significant differences be- experimental conditions (Canals et al. 1997) and suggested by suc-
tween the groups in the first hours, infected triatomines increased cessful daytime captures of this species in field studies (Estay-Olea
their activity toward the end of scotophase, reaching the maximum et al. 2020). However, experimental conditions such as temperature,
values recorded in this group 2 h before the end of this dark phase. photoperiod schedule, and the unknown infection status of adult
The highest activity values of uninfected individuals were recorded insects used in Canals’s study preclude an adequate comparison. In
in the second hour of this phase, after which a continuous and sus- addition, the long period of starvation in the current study might
tained decrease in activity followed until the end of the trial (Fig. 1). have resulted in similar host-seeking behavior during the photophase
and scotophase. In contrast, infected bugs performed almost two-
thirds of their locomotor activity during scotophase, as occurs in
Discussion typical nocturnal triatomines like Triatoma infestans Klug 1834
As has been previously established for other aspects of the behavior (Hemiptera: Reduviidae) (Lazzari 1992, Canals et al. 1997;) and
of M spinolai (i.e., foraging), in this study we show that T. cruzi has R. prolixus (Nuñez 1982, Marliére et al. 2015).
an effect on the locomotor activity of M. spinolai. Particularly, the The change in intensity of locomotor activity seems to be
protozoa modify the daily pattern of activity of their vector, making triatomine-trypanosome specific. In R. prolixus, the proto-
it more active at night. zoan T. cruzi decreases and T. rangeli increases its activity during
Although infected nymphs used in the experiments of locomotor scotophase and photophase, respectively. However, neither of
behavior were significantly heavier than uninfected ones, no differ- these parasites modified the shape of the circadian pattern of ac-
ences were detected between the groups in distance traveled or speed tivity of this triatomine (Marliére et al. 2015). In the current study,Journal of Medical Entomology, 2021, Vol. 58, No. 6 2477
T. cruzi induced a general decrease in activity of M. spinolai, but Acknowledgments
mostly at the beginning of the photophase (Fig. 1). The shape of the
We thank Carlos Cuevas for helpful idiomatic suggestions. This investigation
daily curve of activity was also altered in comparison with that of was supported by the Agencia Nacional de Investigación y Desarrollo de Chile
uninfected nymphs. (ANID)/FONDECYT grant Nº 1180940.
The remarkable differences observed between uninfected and in-
fected nymphs may be due to the action of numerous interacting fac-
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