Mosquito control practices and perceptions: An analysis of economic stakeholders during the Zika epidemic in Belize, Central America
Mosquito control practices and perceptions: An analysis of economic stakeholders during the Zika epidemic in Belize, Central America
Molly Duman-Scheel 0 1
Kathleen K. Eggleson 1
Nicole L. Achee 1
John P. Grieco 1
Limb K. Hapairai 0 1
0 Department of Medical and Molecular Genetics, Indiana University School of Medicine , South Bend, Indiana , United States of America, 2 Eck Institute for Global Health, University of Notre Dame, Notre Dame, Indiana, United States of America, 3 Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana, United States of America, 4 Department of Medicine, Indiana University School of Medicine , South Bend, Indiana , United States of America
1 Editor: Imelda K. Moise, University of Miami , UNITED STATES
The tourist-based economy of Belize, a tropical hub for eco-tourism, is at high risk to be disproportionately impacted by established and emerging mosquito-borne diseases such as Zika. An online survey was used to probe economic stakeholders working in the Belize tourism industry about their mosquito control practices and perceptions. Responses demonstrated that the respondents have good working knowledge of mosquitoes and mosquitoborne illnesses. Most businesses surveyed engage in some means of mosquito control, either through larval source reduction or use of insecticides on the premises. Larvicide use was significantly correlated with a general willingness to use insecticides, as well as belief that treatment of water will reduce mosquito densities and disease transmission. A majority of the respondents agreed that they would be interested in buying a new larvicide to be used on the business premises if it were shown to be safe and effective. The safety of mosquito control products for humans, animals, plants, and the environment in general, followed by product effectiveness, are the most critical determinants of mosquito control purchasing decisions. A majority of respondents agreed that control of mosquitoes and mosquito-borne illnesses is central to the success of their tourist-based industry. Respondents expressed significant concern that the Zika epidemic was over-sensationalized by the media, and that this negatively impacted their livelihoods. The respondents, many of whom are associated with eco/sustainable businesses, also voiced concerns that chemical pesticides could have a negative impact on human health and the environment and expressed a desire for balance between effective mosquito control and preservation of the rich biodiversity of Belize. This study provided a framework for further engagement activities in Belize and other Caribbean nations, uncovered both concerns and support for emerging mosquito control technologies, and revealed opportunities for further debate and educational outreach efforts.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Funding: This study was funded by the United
States Agency for International Development
#AID-OAA-F-1600097 to MDS. The funders had no role in study
design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Mosquito-borne illnesses such as dengue and Zika are spread primarily through the bite of
infected female Aedes mosquitoes. Dengue is one of the most significant mosquito-borne
illnesses in the tropics and subtropics. More than a third of the world's population is at risk for
contracting dengue virus, and as many as 400 million people are infected annually. Belize has
an ongoing risk of dengue transmission, with 2,958 cases of dengue being confirmed in Belize
in 2017 [
], and dengue is a leading cause of febrile illness among travelers returning from the
]. Zika was designated a public health emergency of international concern in
2016. In addition to being transmitted by mosquitoes, Zika virus can be transmitted sexually,
and it can be passed from a pregnant woman to her fetus. Fetal infection with Zika virus can
result in severe birth defects, including microcephaly. Cases of Zika, which have also been
linked to Guillain-BarreÂ syndrome, a serious neurological disorder, are currently occurring in
many countries in the Americas, including Belize [
In 2016, a U.S. traveler returning from Belize reported an imported case of Zika virus in
epidemiological week 14 (EW 14) [
]. In 2017, the number of reported/suspected cases of Zika
peaked during EWs 7 and 8, with ~165 cases suspected and 45 cases confirmed. Although no
reported cases of Guillain-BarreÂ syndrome have yet been associated with Zika in Belize, two
suspected cases of congenital syndromes associated with Zika have been reported by the Belize
]. Belize has both air and sea travel for tourists. Five cruise lines that offer tours to
the islands and the mainland visit weekly , and beaches are frequented by tourists who can
become infected with Zika virus and take it home to the United States, Europe, and other
]. In April 2016, the CDC issued an alert Level 2 warning for travelers to Belize,
indicating that pregnant women should not travel to Belize, an area with risk of Zika, and that
partners of pregnant women and couples planning pregnancy should take preventive steps to
avoid being infected [
]. There are presently no medicines to cure or human vaccines to
prevent Zika, dengue, or most other mosquito-borne illnesses. Consequently, controlling
mosquitoes is the primary means of preventing mosquito-borne diseases [
The Belize Ministry of Health (MOH) [
] oversees a large vector control program that
aims to protect both the citizens of Belize and visitors to the country from mosquito-borne
illnesses. Mosquito surveillance is conducted weekly using standard immature indices  to
monitor need for control measures . Aedes mosquitoes lay eggs in water-filled containers
located within or close to human residences [
], and larviciding, the treatment of container
breeding sites with chemical or microbial agents that kill Aedes larvae, is therefore a major
component of integrated Aedes mosquito control and disease prevention programs .
Mosquito control measures employed by the Belize MoH include use of the larvicide Abate1 to
target immatures and ultra-low volume truck mounted spraying for adult control. Thermal
fogging inside homes is used for index disease cases and the 30 homes surrounding the case
house . The Belize MoH also conducts monthly health fairs to help educate people about
mosquito control and vector-borne illnesses [
]. Unfortunately, due to insecticide resistance
and escalating concerns for the negative effects of pesticides on non-target species, mosquitoes
are becoming increasingly difficult to control [
]. New strategies for combating established
and emerging arthropod-borne infectious diseases are vitally necessary in Belize and
We recently developed interfering RNA larvicides that kill up to 100% of mosquito larvae
in laboratory trials [
]. We have identified several potential delivery systems for these
] and are evaluating their efficacy in semi-field trials. The input of intended
users is crucial for the ultimate acceptability and practical efficacy of proposed interventions as
they are being developed [
]. To this end, we have adapted an approach that epitomizes
2 / 25
pursuit of Responsible Research and Innovation (RRI) [
], a transparent, interactive process
by which societal actors and innovators become mutually responsive to each other with a view
to the acceptability, sustainability, and societal desirability of the innovation process and its
marketable products. As described by Lavery et al. [
], effective community engagement in
global health studies serves to provide investigators an opportunity to ensure that the purpose
and goals of the research are clear to the community, establish relationships and commitments
to build trust with relevant community authorities, and allow researchers to understand the
community, its diversity, changing needs, and assets. Engagement also serves to maximize
opportunities for stewardship, ownership, and shared control by the community, provide a
platform for expression of dissenting opinions or in extreme cases, prohibition of the research,
and give the researchers an opportunity to modify the proposed research strategies, as needed.
Here, we report the findings from an internet-based assessment survey of economic
stakeholders in the Belize tourism industry. The study had four primary aims: 1) to understand the
importance of mosquito control to putative economic stakeholders in the Belize tourism
industry, especially with respect to the recent Zika virus epidemic, 2) to assess, in general, current
mosquito control practices of these stakeholders, 3) to evaluate current uses and perceptions of
larviciding in Belize, and 4) to examine attitudes toward new mosquito control technologies,
including new larvicidal biocontrol agents in a Zika endemic country. The results of this
investigation provided insight into existing levels of mosquito knowledge and control efforts in Belize,
as well as attitudes toward the Zika epidemic, larviciding, and the potential for new control
measures. This study design provides a framework for further engagement activities in Belize and
additional field sites and revealed opportunities for additional educational outreach efforts.
Materials and methods
This study was approved by the Belize Ministry of Health and the Indiana University Office of
Research Compliance (Study #1608074907).
The survey (S1 File), including extension of invitations to participate and collection of informed
consent, was administered online through the Qualtrics platform. Survey invitations were sent
via email to 1,073 adults who held senior/executive positions in for-profit businesses associated
largely or primarily with the tourism industry in Belize. The Belize Board of Tourism provided
the list of relevant businesses and email addresses. Invitations were sent on March 29, 2017, and
reminders were issued through April 26, 2017. The survey, which consisted of a combination of
40 five-point Likert scale items, fill-ins, and open-ended writing prompts intended to probe the
concerns, current practices, and anticipated future needs of economic stakeholders with respect
to mosquito control in general, and more specifically, regarding use of larvicides and new
mosquito control technologies. Routine demographic data were electronically collected along with
survey responses. No individually identifying information was collected. Although a Spanish
translation of the survey was offered (S2 File), only one survey respondent opted to use it. His/
her responses to open questions were translated into English for subsequent textual analyses.
Results were filtered to exclude responses from individuals who did not complete the survey.
Likert scale responses were subjected to statistical and factor analyses with Qualtrics Stats iQ
software. Statistical comparisons were conducted between responses to each individual survey
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question (variable) and all other questions (variables) in the data set. All statistically significant
results observed among these comparisons are reported and discussed herein. The Stats iQ
software makes a recommendation as to the most appropriate statistical test for the data being
analyzed; the statistical comparisons reported herein adhered to these recommendations. Moreover,
the Stats iQ software program alerts users when the size of the data set is too small for reliable
statistical comparisons. Importantly, no such alerts were noted for the analyses reported here.
Responses to open questions on the importance of mosquito control and the impact of Zika
were coded as negative or positive and weighted 1±5 using the Likert scale, with strongly
disagree corresponding to 1 and strongly agree corresponding to 5. Coded data were uploaded and
statistically evaluated in conjunction with responses to the other survey questions using
Qualtrics Stats iQ software. Word count analyses of all open-ended response questions were
performed using TextAnalyzer [
], and the results of these analyses, in addition to inspection of
the open-ended responses by the researchers, were used as a basis to further code positive and
negative responses. Moreover, representative quotes were selected to illustrate the general
sentiments found among each set of coded responses and are discussed herein. Analysis of the fourth
open-ended response question, which asked responders to comment further on any areas of
their choice, did not uncover any additional findings that were not identified through analysis
of the rest of the open-ended responses or survey data, and was excluded from this report.
Results and discussion
Business and respondent demographics
Subjects for this study consisted of adults who held senior/executive positions in for-profit
businesses dependent in part or entirely upon Belize tourism for financial sustainability. 228
individuals of the 1,073 subjects invited initiated the survey, and 168 of these individuals
completed the survey (16% completion rate, median completion time = 16 minutes). The
businesses represented in this study included hotels and resorts, restaurants, and tour operators
(Fig 1A and Table 1), and over 80% were supported primarily through a tourist-based
customer base (Fig 1B and Table 1). A third of the businesses were eco/sustainable, and 57% were
associated with athletic or recreational based activities that occurred both on land and in water
(Fig 1B and Table 1). Over half of the respondents worked in hotels or resorts, the majority of
which had a two to five star ranking (Fig 1D and Table 1), and 73% of which had 5±20 rooms
for rent (Fig 1E and Table 1). Nearly 70% of the respondents were owners, general managers,
or directors with management or executive duties (Fig 2F and Table 2). 81% of the respondents
were over the age of 40 (Fig 2B and Table 2), and 76% of the respondents had 13 or more years
of formal education (Fig 2C and Table 2). Just over half of the respondents were female (Fig
2A and Table 2), and >75% were white and non-Hispanic/Latino (Fig 2E and Table 2). Given
that the target subject population was rather select, the small number of survey respondents is
not unexpected, but may not be representative of all of Belize. Despite the small sample size,
the proportion of respondents working for a particular business type correlated well with the
proportion of invited subjects who worked for a particular type of business. For example, the
percentage of respondents working in hotels and resorts (55%, Fig 1D and Table 1)
corresponded to the proportion of invited subjects who worked for hotels and resorts (53% of the
1,073 total invitees). Thus, despite the small sample size, it is does not appear that respondents
working for a particular business type were over- or under-represented in this study.
Mosquito knowledge and control practices
Respondents were first provided with a set of questions that assessed their basic knowledge of
mosquitoes/mosquito-borne illnesses and which examined mosquito control practices on their
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Fig 1. Summary of business demographic data. Summaries of respondent-supplied information regarding the businesses that they owned or in which they were
employed are shown: A) Type of business, B) Proportion of business that is tourist-based, C) Description of business, D) Star rating, E) Number of guest rooms, F)
Number of guest rooms vs. total annual U.S. dollars spent by the establishment for mosquito control. Percentages in A-E correspond to the percentage of the total
respondents that provided the indicated answer (respondent count numbers are provided in Table 1).
properties. Given the prevalence of mosquito-borne illnesses in Belize [
], it was hypothesized
that the survey respondents would have a reasonably good knowledge of mosquito biology and
disease-causing pathogen transmission, and that most of the businesses surveyed would take
some actions to reduce mosquitoes on their properties. A total of 86% of the respondents agreed
(defined in this study as individuals who checked either somewhat agree or strongly agree) that
mosquitoes transmit viruses that cause dengue, Zika, chikungunya, and yellow fever (Fig 3A
and Table 3). Likewise, 84% of the respondents agreed that treating water where mosquitoes
breed will reduce disease transmission (Fig 3B and Table 3). 87% of the respondents said that
they or someone at their business regularly took action to remove standing water around the
property to control mosquitoes (Fig 3C and Table 3), and 88% of these individuals indicated
that they did so at least once a month or more during the rainy season (Fig 3D and Table 3).
58% of the survey respondents indicated that they used insecticides around the property (Fig 3E
and Table 3). Combined, these results suggest that most economic stakeholders surveyed had
reasonable knowledge of disease vector mosquitoes and made some efforts, either through larval
source reduction or use of insecticides, to control mosquitoes on their properties.
Use of insecticides
The survey probed more deeply into the use of insecticides at Belize tourist-related businesses.
Given the substantial mosquito control program operated by the Belize MoH, it was hypothesized
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Hotel or resort
Eco / sustainable
Athletic or recreational activities on land
Nature exploration on land
Rated, but do not know
5 to 10
11 to 20
Mean = 8 rooms, C.I. = 9±13 rooms
A very small part
At least half
All or almost all
Business Demographic Data. Related survey questions, as well as the percentages/counts of respondents with the indicated answers are shown. C.I. = Confidence
that smaller tourist-based businesses may not spend their own additional private funds for
mosquito control on their properties. However, of the 58% of respondents who agreed that they use
insecticides on the property (Table 3 and Fig 3E), 75% of these businesses indicated that the
insecticides were used to control mosquitoes (Table 3 and Fig 4A). Respondents were asked to indicate
how much money was spent on mosquito control by their business annually. The average among
the 64 establishments that responded was $559±118/year (results were converted to U.S. dollars).
The amount spent per guest room was $71/year (Fig 4B). Regression analysis indicated that there
was a significant positive correlation between the amount of money spent annually and the
number of guest rooms (p<0.00001), and that the amount spent annually increased by $28.70 per
additional guest room (Fig 4B). Thus, the amount of money spent annually for mosquito control
was dependent on the size of the hotel.
A wide variety of mosquito control products were reported to be used on the business
properties (Table 4). 32% of the businesses used a liquid formulation sprayed or fogged in the air
6 / 25
Fig 2. Demographics of the survey respondents. Self-reported demographic data provided by the respondents is shown: A) Gender, B) Age in years, C) Years of formal
education, D) Race, E) Ethnicity (note that race and ethnicity categories correspond to those of the U.S. census), and F) Job title. Percentages in A-F correspond to the
percentage of the total respondents that provided the indicated answer (respondent count numbers are provided in Table 2).
(Table 4); this was the most commonly used formulation for mosquito control, with 91% (58
of 64) of the businesses using an insecticide for mosquito control selecting this formulation.
Likewise, while a variety of products were used, malathion, the chemical pesticide most
commonly noted in the survey responses, was used on 30% of the properties and 20 of the 62
properties (32%) using an insecticide for mosquito control. Resistance to malathion has been
observed in Anopheles albimanus strains in Belize, though it has not yet been assessed in Belize
strains of Aedes. Given the high incidence of its use noted in the survey responses, in addition
to its widespread use in the Belize agriculture sector, the potential for widespread resistance is
of concern [
7 / 25
Demographic questions, as well as the percentages/counts of respondents with the indicated answers are shown. C.I. = Confidence interval.
It was hypothesized that businesses might opt out of insecticide use as a result of a desire to
protect the environment. In support of this hypothesis, a disproportionately high percentage of
the survey respondents who strongly disagreed that they would use insecticides on their
properties (90%, 28 of 31) represented eco/sustainable businesses (Fig 4C, p<0.05, Χ2 = 12.3, d.f. = 4).
Likewise, respondents representing businesses associated with athletic or recreational activities
on land were significantly less likely to strongly agree to insecticide use on their properties (Fig
4B, 15% or 7 of the 46 users; p<0.05, Χ2 = 9.80, d.f. = 4). Businesses associated with nature
exploration on land were significantly less likely to use pesticides, with only 22% (16 of 72) indicating
that they strongly agreed with using insecticides for mosquito control on their properties (Fig
8 / 25
Fig 3. Responses to mosquito knowledge and mosquito control questions. The respondents were queried regarding
their general knowledge of mosquitoes and typical mosquito control practices on their properties. Likert-scale
responses concerning their agreement with the following are included: A) Mosquitoes transmit disease-causing
viruses; B) Treating water where mosquitoes breed reduces disease transmission; C) Removal of standing water on the
premises; D) Frequency of water removal; E) Use of insecticides on the premises. Percentages in A-E correspond to the
percentage of the total respondents that provided the indicated answer (respondent count numbers are provided in
4B, p<0.05, Χ2 = 9.76, d.f. = 4). Belize is a haven for ecotourism and exploration, and ecotourism
is one of the country's largest industries. More than 27% of land in Belize is protected, and the
Survey questions and the percentages/counts of respondents with the indicated answers are shown.
10 / 25
Fig 4. Purchase and use of insecticides. A) The percentage of insecticide-using businesses that use insecticides to kill the indicated pests.
Count numbers are reported in Table 4. B) Survey-taker reported data on annual expenditures for mosquito control (converted to U.S.
dollars) plotted as a function of the number of guest rooms available for rent. Annual expenditures increase as the number of rooms
increases (p<0.00001). Mean = $71 spent on mosquito control per room annually. C) Likert-scale responses from representatives of the
indicated types of businesses regarding the use of insecticides on their properties. The percentages (graph at top) and numbers (lower graph)
of the X-axis category respondents providing the answers indicated are shown. >>> = very highly significant, >> = very significant, > =
significant, with green corresponding to a higher than expected percentage/number of respondents for a given X-axis category and red
corresponding to a lower than expected percentage/number of respondents for a given X-axis category. See text for additional details
regarding statistical analyses and a discussion of significant results.
preservation of rich biodiversity is a critical component of the ecotourism industry. This
emphasis on ecotourism has unintentionally led to environmental degradation, and there is a strong
movement to reverse this degradation [
]. Thus, it is perhaps not surprising that many
eco/sustainable and ecotourist associated businesses are opposed to pesticide use in Belize.
The amount of money the business spends on
mosquito control is ________ (currency amount)
Survey questions and the percentages/counts of respondents with the indicated answers are shown.
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% of Responses
Larviciding: Knowledge and practice
The survey included a series of questions regarding the respondents' knowledge and use of
larviciding, a crucial component of integrated Aedes control and disease prevention programs .
74% of those surveyed agreed that larvicides will reduce the number of mosquitoes (Table 5),
and 85% agreed that treating water where mosquitoes breed will reduce disease transmission
(Fig 3B). Despite these responses, only 31% agreed that they would plan to use larvicides on the
premises in the next year (Table 5). A possible explanation for these findings is that the Belize
MoH regularly employs larviciding for vector control , and perhaps the businesses did not
find the need to pursue further larviciding. Furthermore, at least one respondent indicated in the
open-ended response questions that he/she did not know where to find larvicides, which suggests
that they may not be readily available throughout the country.
The data were further evaluated in an effort to gain a better understanding of the factors
that influence the use of larvicides. It was hypothesized that larvicide use would correlate with
the belief that it would reduce mosquito numbers and prevent mosquito-borne illnesses. 92%
(23 of 25) of respondents who strongly agreed with larvicide use also strongly agreed that use
of larvicides would reduce the number of mosquitoes (Fig 5A, p<0.001, Χ2 = 41.2, d.f. = 16),
and 100% (25 of 25) of these individuals strongly agreed that treating water where mosquitoes
breed would reduce disease transmission (Fig 5B, p<0.001, Χ2 = 42.6, d.f. = 16). Thus,
significantly higher proportions of individuals who used larvicides on the premises believed that they
would reduce the number of mosquitoes and the amount of disease transmission. Of those 46
individuals who agreed they would use larvicides on the premises, 42% indicated that they
would use the larvicides to treat water stored in drums and used for purposes other than
drinking, cooking, or bathing (Table 5); this was the most commonly selected use of larvicides
among the positive respondents. A study in Trinidad and Tobago indicated that such larger
containers were the most productive Aedes breeding sites [
]. Primary containers for Aedes
breeding are yet to be fully characterized in Belize; however, drums are typical larval sources
Survey questions and the percentages/counts of respondents with the indicated answers are shown.
Fig 5. Assessment of respondents' willingness to use larvicides on the premises. Likert-scale responses to the question of whether the business plans to use larvicides on
the premises in the next year (X-axes) vs. A) Agreement that larvicide use will reduce the number of mosquitoes, B) Agreement that treatment of water where mosquitoes
breed will reduce disease, and C) Respondents' willingness to use any insecticide on the premises (Y-axes). The percentages (upper graph in each panel) and numbers
(lower graphs) of the X-axis category respondents providing the answers indicated are shown. >>> = very highly significant, >> = very significant, > = significant, with
green signifying a higher than expected percentage/number for a given X-axis category and red denoting a lower than expected percentage/number of respondents for a
given X-axis category. See text for additional details regarding statistical analyses and discussion of significant results.
reported during routine surveillance activities. If drums are indeed the primary breeding sites,
then the survey results suggest that the businesses using larvicides are focusing on treatment of
the most productive containers.
Conversely, significant reductions in the strong agreement that water treatment would
reduce the number of mosquitoes (16 of 43 or 37%, Fig 5A, p<0.0001, Χ2 = 41.2, d.f. = 16) or
disease transmission (17 of 43 or 40%, Fig 5B, p<0.001, Χ2 = 42.6, d.f. = 16) was observed
among the responders who strongly disagreed with larvicide use. Moreover, a significantly
high proportion of individuals (83%; 5 of 6) who strongly disagreed that use of larvicides
would reduce the number of mosquitoes also strongly disagreed that they would use larvicides
on their property (p<0.001, Χ2 = 41.2, d.f. = 16). A significantly higher than expected
proportion of individuals (67% or 4 of 6) who felt that water treatment would not reduce the number
of mosquitoes also strongly disagreed that treating water where mosquitoes breed would
reduce disease transmission (p< 0.00001, Χ2 = 181, d.f. = 16). Thus, reluctance to use larvicides
strongly correlated with a lack of belief that larviciding would reduce the number of
mosquitoes and disease transmission (Fig 5). These statistics reveal opportunities for educational
outreach regarding the benefits of larviciding, as well as open discussion of its challenges. In
support of this, the open-ended responses revealed a vast range of knowledge of larviciding,
with one respondent indicating he/she didn't know much about it and would like to learn
more, while another discussed the challenges of treating cryptic breeding sites.
Finally, the decision to use larvicides correlated significantly with a willingness to use
insecticides (Fig 5C). A significantly higher than expected proportion of individuals who strongly
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agreed with larvicide use also strongly agreed that they would use insecticides on their properties
(Fig 5C, 52% or 13 of 25, p<0.0001, Χ2 = 46, d.f. = 16). A disproportionately high number of
individuals (22 of 31 or 71%) who strongly disagreed with insecticide use also strongly disagreed
that they intended to use larvicides on the premises (p<0.0001, Χ2 = 46, d.f. = 16). These statistics
suggest that some respondents were not specifically opposed to the use of larvicides, but were
more generally opposed to the use of any insecticide on their properties.
Willingness to consider novel mosquito control technologies
The responders were queried regarding their willingness to use new products and technologies
for mosquito control. 53% of the respondents agreed that they would be interested in buying a
new larvicide to be used on the business premises once it had been shown to be safe and
effective (Table 6). When businesses wished to consider switching to a new control product,
product labels and word of mouth were the primary inputs evaluated (Table 6). Of those surveyed
who strongly agreed that they would be interested in a new product, 43% (16 of 37, a
significantly higher proportion than expected) also indicated that they would consider the input of a
salesperson or industry representative (p<0.05, Χ2 = 13, d.f. = 4), and a disproportionately
high percentage of those who somewhat agreed (47% or 16 of 34) indicated that their purchase
choices are influenced by social media (p<0.05, Χ2 = 12.9, d.f. = 4).
Survey questions and the percentages/counts of respondents with the indicated answers are shown.
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Individuals who disagreed with the purchase of a new larvicide product at their businesses
were further assessed. Of the responders who strongly disagreed with their interest in
purchasing a new larvicide product, 68% (15 of 22), a disproportionately high number, also indicated
that they would strongly disagree with using any larvicide on the premises in the next year (Fig
6A, p<0.0001, Χ2 = 47.8, d.f. = 16), while 50% (11 of 22, a disproportionately high number)
strongly disagreed that any insecticide would be used (Fig 6B, p<0.001, Χ2 = 39.7, d.f. = 16). Of
those individuals that strongly disagreed that they would be interested in purchasing a new
larvicide, a significantly lower than expected percentage (27%, 6 of 22) also strongly agreed that
larvicide use would reduce the number of mosquitoes (Fig 6D, p<0.01, Χ2 = 32.7, p<0.01), and
only 32% (7 of 22), a significantly lower percentage, also strongly agreed that it would reduce
disease transmission (Fig 6E, p<0.001, Χ2 = 43.2, d.f. = 16). Thus, a lack of interest in a new
larvicide product correlated with a lack of willingness to use larvicides or insecticides in general
and a lack of agreement that larviciding will reduce the number of mosquitoes or disease
transmission. Moreover, of those business representatives that strongly disagreed with purchasing a
new larvicide, 91% (20 of 22) were associated with eco/sustainable businesses (p<0.01, Χ2 =
13.8, d.f. = 4), a disproportionately high percentage (50% or 11 of 22) strongly disagreed with
the use of any insecticides on their properties (Fig 6B, p<0.001, Χ2 = 39.7, d.f. = 16), and 68%
(15 of 22, also higher than expected) also strongly disagreed that they would use larvicides on
the premises (Fig 6A, p< 0.0001, Χ2 = 47.8, d.f. = 16). Therefore, a lack of interest in a new
larvicide correlated significantly with a general reluctance to use insecticides, which was significantly
linked to whether the business characterized itself as eco/sustainable (see above). The impact of
mosquito control on the environment was a topic mentioned frequently in the open-ended
responses and will be discussed further below.
Recent advances in the use of transgenic release strategies for vector control have highlighted
the critical importance of effective community engagement prior to the use of new mosquito
control technologies, particularly when genetically modified organisms (GMOs) are being
considered [18, 24±27]. Others and we have proposed the use of larvicidal genetically modified
microbes that express interfering RNA [
16, 17, 28, 29
] and recognize the importance of
engaging the communities in which such interventions could potentially be used. To this end, the
survey of economic stakeholders included two questions regarding the potential use of GMO
larvicides, assuming that they were demonstrated to be both safe and effective.
Of those who strongly agreed to consider a new larvicide product, a significantly higher
than expected number (21 of 37 or 57%) indicated that they were also willing to use a GMO as
a larvicide if it were deemed safe and effective (Fig 6C, p<0.00001, Χ2 = 84.7, d.f. = 16). 84%
(21 of 25) of those who strongly agreed with the use of GMO larvicides also strongly agreed
that larviciding could reduce the number of mosquitoes (a higher percentage than expected,
p<0.05, Χ2 = 31.1, d.f. = 16), and 88% (22 of 25) of these business representatives strongly
agreed that treating water could reduce disease transmission (Fig 6E, p<0.05, Χ2 = 31.9, d.f. =
16). Of the respondents willing to try a GMO larvicide, they were most willing to use
genetically modified bacteria (60%, Table 6), a technique which has demonstrated promise in
laboratory studies [
16, 17, 29
]. 54% expressed willingness to use genetically modified algae (Table 6),
which has also been tested in laboratory studies . Finally, 37% were willing to use
genetically modified yeast larvicides (Table 6), which were recently shown to generate up to 100%
larval lethality in laboratory assays [
77% (17 of 22) of those who strongly disagreed with purchasing a new larvicide product
also strongly disagreed with using a GMO larvicide (Fig 6C, p<0.00001, Χ2 = 84.7, d.f. = 16). A
very significantly high proportion (41 of 47 or 87%) of those who strongly disagreed with the
use of GMO larvicides represented eco/sustainable businesses (p<0.01, Χ2 = 17.8, d.f. = 4), but
as discussed above, 90% of these individuals were also significantly opposed to using any
16 / 25
Fig 6. Analysis of respondents willing or not willing to purchase a new larvicide for use on the premises. Likert-scale responses to the question of whether the business
is interested in purchasing a new larvicide for use on the premises (X-axes) vs. A) Willingness to use larvicides on the premises, B) Willingness to use any insecticides on
the premises, C) Willingness to use a GMO-larvicide if it is shown to be safe and effective, D) Agreement that larvicide use will reduce the number of mosquitoes, E)
Agreement that treatment of water where mosquitoes breed will reduce disease, and F) Respondent-provided description of the type of business. The percentages (upper
graph in each panel) and numbers (lower graphs) of the X-axis category respondents providing the indicated answers are shown. >>> = very highly significant, >> =
very significant, > = significant, with green representing a higher than expected percentage/number for a given X-axis category and red representing a lower than expected
percentage/number of respondents for the indicated X-axis category. Additional details regarding the statistical analyses and further discussion of significant results are
provided in the text.
17 / 25
pesticides on the premises. Thus, their opposition to using GMO larvicides may not be specific
to GMO use, but rather to the use of insecticides in general. Furthermore, only 8.7% of women
(6 of 69) strongly agreed with the use of GMO larvicides, while a significantly greater than
expected proportion of men (27%, 16 of 60) strongly agreed that they would be willing to use a
GMO larvicide (p<0.05, Χ2 = 9.94, d.f. = 4). Sex-specific differences in willingness to use
GMOs have been observed in other realms. For example, women have been shown to be less
accepting of genetically modified foods than men [31±34]. While some have reported that
years of education [
31, 34, 35
] and age [
] impact GMO food acceptance, neither of these
variables significantly impacted GMO larvicide acceptance in this investigation.
It should be noted that although the survey respondents were queried regarding their
willingness to use GMO larvicides that were demonstrated to be safe and effective, they were not
provided with any details regarding the GMO larvicides that have been developed to target Aedes in
recent years. Importantly, these larvicides have been designed so that the target sequences of the
interfering RNA molecules are specific to mosquitoes and lack target sites in other organisms [
]. These larvicides may therefore be safer than many chemical pesticides, but such information
was not communicated to respondents in the context of this survey, which sought only to gain
baseline knowledge on feelings towards larviciding and GMO larvicides in Belize. Furthermore,
several studies have demonstrated that bacteria and yeast that have been genetically modified to
express larvicidal interfering RNA are still effective if the microbes are first heat-killed [
]. Thus, the GMO larvicides under consideration are actually dead, not live GMOs, which
could impact user acceptance of this intervention. Moreover, as detailed by Hapairai et al. [
interfering RNA expression cassettes can be inserted into the yeast genome, thereby eliminating
the potential for horizontal transfer or the need to use plasmids with antibiotic resistance
markers, which could also influence user acceptance. In a recent community engagement study in the
Florida Keys [
], when transgenic mosquito releases were under consideration, support was
more commonly reported among those aware of the release, whereas those who were neutral
expressed a desire for more information. Those opposed often expressed concern for the
unintended consequences for disturbing natural ecosystems, while supporters often felt that such
releases represented a more natural means of controlling mosquitoes than the use of insecticides.
It is likely that the use of GMO larvicides may incite similar discussions. Thus, there will be many
opportunities for further education and debate about the use of GMO larvicides.
Product features that influence the purchase of mosquito control products
To gain further insight regarding current mosquito control practices and the development of
new control technologies, the survey respondents were prompted to provide an open-ended
response to the question “When considering different mosquito control products for purchase,
which product features are most important?” The resulting text from 127 responses was assessed
to identify words that occurred most frequently, and these results are summarized in Table 7. At
the top of the list, 64 words related to safety/danger/chemical use were mentioned, with specific
use of the word safe(ty) 47 times, making it the most common word found among all the
responses. In total, 48% of the respondents (61 of 127) commented on product safety. Words
related to environmental concerns were used 47 times, with specific mention of the word
environment (or one of its derivatives) occurring 23 times. Different types of animals or plants were
named 29 times. In total, 41% of respondents (52 of 127) noted concerns for the environment,
animals, or plants. Furthermore, the word effective or one of its derivatives occurred 32 times,
and in total, 33% of respondents (42 of 127) mentioned product efficacy as a predominant driver
of product selection. These analyses suggest that safety of the products, for humans, animals,
and plants, as well as general concerns for the environment, followed by product effectiveness,
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"Safe for humans and my animals."
"Safe for inexperienced handlers of the (chemical) product.º
ªWe try to use products that are a natural base with
as little environmental and human impact as possible.º
"Non harmful to bees or other important creatures."
"Effectiveness and waterproof for longevity."
"Kills most insects that cause personal injury."
Analyses of the product features open-response question, including groups of related words and their frequencies, common words in the group and the number of times
they were repeated, as well as representative quotes for each theme are shown.
are the most critical determinants of product purchases. Such concerns outweighed factors such
as product cost (noted by 12% of respondents; 15 of 127), lasting activity (mentioned by 5% of
respondents; 6 of 127), odor (4% of responses; 5 of 127), and ease of use (3% of responses; 4 of
127). In addition to a summary of these data, quotes that effectively represent each category of
responses are included in Table 7.
It is striking that environmental concerns outweighed concerns for efficacy and cost. It is
likely that the large focus on eco/sustainable tourism in Belize is a major influence on these
responses. Ceballos-Lascurain [
] defined ecotourism as “traveling to relatively undisturbed or
uncontaminated natural areas with the specific objective of studying, admiring, and enjoying the
scenery and its wild plants and animals, as well as any existing cultural manifestations (both past
and present) found in these areas.” As discussed by Blersch and Kangas [
], who assessed the
potential for sustainability of eco-tourism in Belize, this definition has expanded to include
conservation, sustainability, and ethical lines of thought [
] and embraces seven basic tenets
of ecotourism: travel to natural destinations, an emphasis on environmental awareness,
minimal footprints, direct financial benefits for increased conservation, the financial benefit and
empowerment of local people, the respect of their culture, and support for human rights [
Several of these tenets, which are clearly reflected in the open-ended responses (Table 7),
appear to be at the heart of tourist-based economic stakeholders' feelings concerning
acceptable means of mosquito control in Belize. As discussed below, mosquito control is
undoubtedly important for the success of tourist-based businesses, but many of the stakeholders
indicated that such control must have minimal impact on the environment or their health.
Importance of mosquito control for business success
The survey respondents were asked to provide an open-ended response to the question: “Could
you please describe the importance of mosquito control for business success in Belize?” Their responses
were coded on a Likert-like scale, with 1 corresponding to not very important and 5 corresponding
to very important. The average score (of 131 responses) was 4.17+/-0.95, corresponding to
somewhat important. No significant relationships were observed in the coded response scores to this
question vs. responses to any other question. A word frequency analysis was completed for both
positively (score of 4 or 5) and negatively (score of 1 or 2) coded responses. Word count analyses of
the negatively coded responses did not reveal any central themes, likely due to the relatively low
number of negative responses (10 of 131, 8%). Further inspection of the responses indicated that
most individuals with a negatively coded response simply felt that mosquito control was futile
19 / 25
(three of 10, 30%), that mosquitoes are just part of life in Belize (three of 10, 30%), that the negative
impacts on the environment outweighed the positive outcomes (two of 10, 20%), or that
mosquitoes simply were not that big of an issue and are under control (two of 10, 20%).
Textual analysis of the 117 of 131 (89%) positively coded responses revealed three categories
of terms observed most frequently in the responses: (1) tourists/customer-focused concerns,
(2) health and disease, and (3) the environment. A summary of these analyses is presented in
Table 8. Words related to tourists/customers appeared 77 times. The word tourist or one of its
derivatives was included 39 times, making it the most repeated word among the responses. In
total, 55 of the 117 responses (47%) noted concerns for customers. Quotes that represent the
sentiment of these responses are included in Table 8. These quotes illustrate a common theme
among these responses, which centered on concerns for the customers having positive
experiences during their visits to the property. Next, 74 occurrences of terms related to health and
disease were noted, with the word disease(s) being mentioned specifically 26 times. Responses
in this category centered on the concern that mosquito control is necessary for disease
prevention, and 48 of 117 responses (41%) mentioned health related items. Quotes that exemplify the
nature of this category are included in Table 8. These findings are not surprising given that a
majority of the respondents demonstrated reasonable knowledge of mosquito control and
mosquito borne disease transmission (Table 3, Fig 3).
Finally, words related to the impact of mosquito control on the environment/unintended
effects of mosquito control were mentioned 26 times. Quotes from this category (Table 8)
illustrate the sentiment that mosquito control should not negatively impact the environment, a
notion that was included in 21% (25 of 117) of the responses and which was reflected in several
of the other data analyses summarized and discussed above.
Economic effect of Zika vs. other mosquito-borne diseases
The respondents were given the opportunity to provide an open-ended response to the
question “Are the economic effects of Zika different than those of other mosquito-borne diseases to
48 of 117 (41%)
26 of 117 (21%)
ªOur jobs depends on tourist and if the guest is getting eaten alive they
will never come back to the island again.º
"Mosquito control = tourist satisfaction."
ªIf the country is perceived as unsafe (i.e. Zika, dengue, etc.) then our business
"We must protect the Belize citizens and make the tourist feel and know
that steps are in place to help control the mosquito diseases.º
"We believe that mosquitoes can and should be controlled with eco-friendly
products that do not harm the people more than the disease itselfÐwhich is
what we feel about most of the products used to fight mosquitoes today."
"Our natural treasures are what is most important to Belizeans and any
mosquito control that threatens the health of humans, water systems or
animals life should be avoided at all costs.º
Analyses of the mosquito control open-ended response question, including groups of related words and their frequencies, common words in the group and the number
of times they were repeated, as well as representative quotes for each theme are shown.
20 / 25
local businesses?” Their responses were coded on a Likert-like scale, with 1 corresponding to
not very different and 5 corresponding to very different. The average score among the 120
responses was 2.93±1.65 (corresponding to neither different nor not different). Once again, no
significant relationships were observed in the coded scores of the responses to this question vs.
responses to any other question in the survey. Next, the text from negative responses (score of
1 or 2) and positive responses (score of 4 or 5) were analyzed. 49 of 120 (41%) responses were
coded negatively, while 55 of 120 (46%) were scored positively; the remaining 16 responses
(13%) received a score of 3. Only 11 of the 49 negatively coded responses included a textual
explanation of their response (most were just single word answers of ªnoº or ªsameº). Word
count analyses of these 11 responses did not uncover specific themes. However, inspection of
the 11 responses revealed several patterns. Five of 11 (45%) noted that there were few or no
cases of Zika in their area or the country as a whole. 27% of respondents (3 of 11) noted that
the guests had not mentioned Zika or seemed particularly concerned about it. 3 of 11 (27%)
indicated that all mosquito borne illnesses were bad or that Zika was no worse than other
diseases transmitted by mosquitoes. Table 9 shows the results of word counts observed in the
textual analysis of the 55 positively coded responses, as well as representative quotes. Three
primary themes were revealed through textual analysis of the positively coded responses: 1)
concerns for the unborn and 2) strong negative feelings toward the media for their handling of
the Zika crisis, both of which the respondents linked to 3) cancellations resulting from the
Congenital Zika Syndrome, a distinct pattern of birth defects that can result from fetal
infection with Zika, includes several distinct features: severe microcephaly associated with
partial collapse of the skull, decreased brain tissue, eye damage, congenital contractures such as
clubfoot or arthrogryposis, and hypertonia that restricts body movement following birth [
Words related to pregnancy/babies/birth defects appeared 28 times among the positively
coded responses (Table 9). 21 of 55 positive responders (38%) noted concerns for the unborn
as being a primary distinguishing factor of Zika as compared to other mosquito-borne illnesses
(Table 9). The results suggest that the survey responders were well informed about the
potential for Zika to induce birth defects. This is quite likely due to the extensive media coverage of
this topic, which was also noted in the open-ended responses. By April 2017, the time at which
the survey was conducted, the number of confirmed Zika cases reported weekly was 10/week,
with ~20±30 suspected cases reported during this period [
]. 17 occurrences of words related
to the media were noted. Of the 55 positive responses, 15 (27%) mentioned media coverage of
Zika (Table 9). The majority of these responses centered on the notion that media coverage
was sensationalized, and that news coverage of Zika was a primary driver of the negative
impact of Zika on tourism in Belize. 25% of the positive responses (14 of 55) noted the negative
Analyses of the Zika impact open-ended response question, including groups of related words and their frequencies, common words in the group and the number of
times they were repeated, as well as representative quotes for each theme are shown.
21 / 25
impacts on business, which the respondents directly associated with Zika and often with the
extensive media coverage of it (Table 9). Words associated with cancellations and downturns
in rentals were identified 15 times (Table 9). Thus, the results of the survey indicate that
economic losses were incurred among the tourist-associated businesses in Belize.
At the time this survey was conducted, the United Nations Development Program issued a
] which concluded that the Zika epidemic would have substantial economic and
social impacts, both long and short-term, in the Americas. The report noted that the impacts
on countries that have tourist-based economies such as Belize and other countries in the
Caribbean would be particularly strong. More than 80% of the anticipated total losses, which
could reach $9 billion in the Caribbean, are the direct result of reduced revenues from
international tourism. Short-term costs for Belize (2015±2017) were estimated at $35,873,714 (U.S.
dollars). The report estimated that in a high infection scenario, Belize could stand to lose as
much as 1.19% of GDP annually. These findings validate the concerns voiced in the survey
responses. Given these significant losses, many have questioned if the media response to Zika
was over-sensationalized, another clear sentiment of many of the respondents (Table 9).
Gyawali et al. [
] concluded that given the significant capacity for mosquito control in
developed countries, the widespread media concern for the potential of Zika to spread to
epidemic proportions in industrialized nations is difficult to justify. Samuel et al. (2018) reported
that despite extensive coverage of Zika by the media, people in New York City had an overall
poor understanding of Zika virus symptoms, potential complications, modes of transmission,
and guidelines for prevention, and that further intervention is needed to properly educate the
public. Likewise, another study noted that 40% of news articles on Zika mentioned negative
potential outcomes of Zika infection without mentioning ways to prevent infections [
These studies suggest that, in the least, some media coverage could be improved to better
educate the public about Zika prevention. Although many stakeholders in Belize felt that media
coverage of Zika had a direct negative impact on their businesses (Table 9), Chandrasekaran
et al. [
] reported that social media could effectively educate the public on Zika virus,
concluding that young women can use social media as a useful resource on Zika. The benefits and
costs of media coverage of Zika, as well as other infectious disease, will undoubtedly continue
to be debated.
This analysis of the results from an online survey of tourist-based business representatives from
Belize revealed insight into the concerns, current mosquito control practices, and anticipated
future needs of economic stakeholders working in the tourism industry in Belize. Most survey
respondents demonstrated they had reasonable knowledge of mosquito disease vectors and
made some efforts, either through larval source reduction or the use of insecticides, to control
mosquitoes on their business properties. Use of larvicides on the business premises correlated
strongly with a willingness to use insecticides in general, as well as the belief that water
treatment would reduce mosquito densities and disease transmission. Over half of the respondents
agreed that they would be interested in buying a new larvicide to be used on the business
premises once it had been shown to be safe and effective. The safety of such products, for humans,
animals, and plants, and the environment in general, followed by product effectiveness, are the
most critical determinants of product purchase decisions. Although the majority of respondents
agreed that control of mosquitoes and mosquito-borne illnesses was central to the success of
their tourist-based businesses, many of the respondents raised concerns that the Zika epidemic
had been sensationalized by the media, with dire consequences for tourist-based businesses in
Belize. They also voiced concerns that current mosquito control practices, including the use of
22 / 25
chemical pesticides, could have a negative impact on human health and the environment.
Respondents, many of whom worked for eco/sustainable businesses, sought effective mosquito
control interventions that have minimal impact on the environment. This study provided a
framework for further engagement activities in Belize and other Caribbean nations and
uncovered potential areas of concern as well as support for emerging mosquito control technologies,
particularly those that are safe and eco-friendly. The results of this investigation will foster
further debate and guide future educational outreach efforts in Belize and elsewhere.
S1 File. Economic stakeholders' survey. The Qualtrics-formatted survey sent to tourist-based
business representatives in Belize is provided as a pdf file.
S2 File. Spanish translation of economic stakeholders' survey. A Spanish translation of the
survey is provided as a pdf file.
We thank Marla Magana and Donovan Leiva of the Belize Vector and Ecology Center for
facilitating survey invitations and providing feedback to ensure culturally relevant survey
questions. Thanks also to David W. Severson for useful comments on the survey and discussion of
the results, as well as to Victoria Denekes for her assistance with Spanish translation of the
Data curation: Limb K. Hapairai.
Conceptualization: Kathleen K. Eggleson, Nicole L. Achee, John P. Grieco, Limb K. Hapairai.
Formal analysis: Molly Duman-Scheel, Nicole L. Achee, Limb K. Hapairai.
Funding acquisition: Molly Duman-Scheel.
Investigation: Kathleen K. Eggleson, Nicole L. Achee, John P. Grieco, Limb K. Hapairai.
Methodology: Molly Duman-Scheel, Kathleen K. Eggleson, Nicole L. Achee, John P. Grieco,
Limb K. Hapairai.
Project administration: Molly Duman-Scheel, Nicole L. Achee, John P. Grieco.
Writing ± original draft: Molly Duman-Scheel.
Writing ± review & editing: Molly Duman-Scheel, Kathleen K. Eggleson, Nicole L. Achee,
Limb K. Hapairai.
23 / 25
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