188

Journal of Vector Ecology December 2020

Assemblage variation of mosquitoes (Diptera: Culicidae) in different land use and

activity periods within a lowland tropical forest matrix in Campeche, Mexico
Carlos Antonio Abella-Medrano1, David Roiz2, Carlos González-Rebeles Islas1,
Claudia Lorena Salazar-Juárez1, and Rafael Ojeda-Flores1*
1
Universidad Nacional Autónoma de México, Facultad de Medicina Veterinaria y Zootecnia,
C.U. Coyoacan Ciudad de México 04510, Mexico, [email protected]
2
MIVEGEC, University Montpellier, IRD, CNRS, 34090, Montpellier, France

Received 26 February 2020; Accepted 12 May 2020

ABSTRACT: Most mosquito species are active during a certain part of the day, but climatic factors such as light intensity and
relative humidity play an important role in the control of their activity. We selected three types of land use that were sampled
in state of Campeche in 2018 (low semi-evergreen forest, secondary low semi-evergreen forest, and mango plantation), using
ten CDC light traps baited with CO2, that were active during nine hours of three activity periods (dawn, noon, and nightfall). A
GLM was used to investigate changes in the assembly of mosquitoes between different types of land use and temporal variations.
Rank abundance curves were used to detect changes in the spatial and activity period of the mosquitoes and we then calculated
the Exponential Shannon Index. A total of 6,110 mosquitoes belonging to 23 species were captured. The greatest richness and
abundance were found in the secondary low semi-evergreen forest, with greater richness and lower abundance than the mango
plantation which showed more abundance. Of the activity periods, dusk had the greatest abundance and richness followed by
dawn and finally noon. Journal of Vector Ecology 45 (2): 188-196. 2020.

Keyword Index: Culicidae, activity periods, land use types, low semi-evergreen forest, diversity.

INTRODUCTION Ortega-Morales et al. 2019). Most of these species can feed on

humans and other animals (Harbach 2007).
Infectious diseases have significantly influenced human Most mosquito species are active during a certain part
biology and society and have even determined the course of of the day. In previous studies it was mentioned that the
important historical events. Approximately three-quarters onset and cessation of activity were completely controlled by
of the recognized emerging infectious diseases were once climatic factors such as light intensity and relative humidity.
or are currently zoonotic, that is, transmissible between However, circadian rhythms play an important role in the
animals and humans (Wilcox and Gubler 2005). The control control of mosquito activity, governed endogenously by
of zoonotic diseases is one of the most important concerns periods of light and dark. Mosquito activity in search of hosts
in the area of human
​​ health. Recent studies have shown that can be placed into one of four categories: nocturnal, twilight/
most pandemics have originated from zoonoses (Smith et al. nocturnal, twilight/diurnal, and diurnal (Kawada et al. 2005).
2007). Many diseases are typical of wild animals (enzootic Habitat alterations caused by changes in land use have the
cycles) that are spread with the participation of arthropod potential to impact the dynamics of vector-borne disease
vectors (Wilcox and Gubler 2005). Mosquitoes are vectors of directly and indirectly, causing changes in the richness and
several zoonoses, including yellow fever, Venezuelan equine abundance of mosquitoes, modifying hematophagous habits,
encephalitis, dengue, malaria, Chikungunya, and Zika. and even altering activity patterns from dusk to dawn (Ndoen
More than 3,490 mosquito species have been described et al. 2011, Gottdenker et al. 2014, Abella-Medrano et al.
worldwide, of which 195 to 250 have been reported in Mexico. 2018).
Of these species, approximately 43 are of medical importance Research on the periods of mosquito activity in Mexico
and 115 of veterinary interest (Darsie 1996, Harbach 2007). are few, and they do not include the component of land use
As a result of the geographical location and topographic type. This lack of information, coupled with human activities
and vegetation diversity in the state of Campeche, Mexico, within conserved areas such as jungles, can contribute to
it shares a singular fauna with endemic elements with many the increased impact of vector-borne diseases as they could
taxa representing neotropical areas. However, there are few cause changes in the assembly of species and therefore alter
faunistic and ecological studies that have been carried out the trophic interactions, which affects the increased risk
in the state of Campeche, as only 21 species of mosquitoes of transmission (Alcaide et al. 2009, Keesing et al. 2010).
have been reported (Heinemann and Belkin 1977), but in Therefore, knowing changes in the assembly of mosquitoes
neighboring states such as Quintana Roo (81 species) and among different types of land use and at different activity
Tabasco (104 species), many more species have been reported periods might provide valuable information to advance the
due to recent fauna studies (Ortega-Morales et al. 2010, understanding of the dynamics associated with zoonotic
 19487134, 2020, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jvec.12389 by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [05/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Vol. 45, no.2 Journal of Vector Ecology 189

Figure 1. Study areas. Candelaria, (1) Secondary low semi-evergreen forest, (2) low semi-evergreen forest, and Santa Lucía, (3)
Mango plantation (M. indica).

diseases. between them and placed 60 cm above the ground (Silver

2007, Kirkeby et al. 2013). Traps were left active three hours
MATERIALS AND METHODS during the dawn (starting one hour before sunrise, 17:30 to
08:30), at noon (from 12:30 to 15:30), and during nightfall
Study areas (one hour before sunset, 17:30 20:30), for a total of nine hours
Sampling was carried out from 30 July to 9 August 2018. of sampling per day; each site was sampled for two days. We
Three types of land use were sampled in the north of the state used information provided by GPS to determine the exact time
of Campeche, Mexico: low semi-evergreen forest, secondary of sunrise and sunset. Collected mosquitoes were preserved
low semi-evergreen forest, and mango plantation (Mangifera at -20° C. All the material was first placed in Petri dishes
indica). In the Candelaria location, the tropical low forest has and then kept frozen until identification in the laboratory.
primary vegetation with a predominance of Haematoxylum The observation of taxonomic characteristics was performed
campechianum. There is also secondary tropical low forest with a dissecting microscope. Individuals were separated
with a predominance of herbaceous vegetation and H. by location and trap number, taxonomically identified by
campechianum. In Palizada, at the Santa Lucia ranch, there species, and subsequently stored in entomological boxes.
is the mango plantation (M. indica) and H. campechianum Series of each species were mounted on entomological pins
plantation, which is located within a reforestation project following the recommended procedure for their preservation
(Figure 1). (Belkin 1967). We used the morphological nomenclature of
Harbach and Knight (1980).
Mosquito samples
Sampling was conducted within a half-hectare square Statistical analysis
grid (100 × 50 m) at each site using ten CDC miniature Species accumulation curves and the Abundance-based
incandescent light traps (model 512; John W. Hock Company) Coverage Estimator (ACE) and Chao1 were used to determine
baited with CO2 from yeast (Saccharomyces cerevisiae). Traps sample efficiency (Colwell and Coddington 1994, Magurran
were placed in two transects of 100 m, separated 50 m from 2003). This procedure was performed with EstimateS 8.2.0.
each other (five traps per transect), with a distance of 25 m A generalized linear model (GLM assuming a Negative
between traps on the same transect to avoid competition Binomial distribution with log-link function for Abundance
 19487134, 2020, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jvec.12389 by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [05/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
190 Journal of Vector Ecology December 2020

and Richness analysis) was used to investigate changes in has a higher richness (19 spp.) compared to EF (17 spp.),
the assembly of mosquitoes between different types of land the latter has a higher richness than SF during NI but less
use (tropical evergreen forest, secondary tropical evergreen during NO, which is why significant values are reflected
forest, and mango plantation) and the period of activity (Table 2, Figure 3). With respect to abundance, significant
(dawn, noon, and nightfall). Rank abundance curves were effects were detected in each type of land use and in each
used to detect changes in the spatial and activity period of activity period (Table 2). Significant values were found in the
the mosquito assemblage (Magurran 2003) and we then NI and NO periods. There are significant effects of positive
calculated the Exponential Shannon Index using the SPADE interaction between the EF in the NI and NO periods; the
program (Chao and Shen 2010) to determine whether SE site was only significant for the NO period. There were
diversity changes in each of the types of land use. (Jost 2006, no positive interactions at the SF site in the NI due to a very
2010). high abundance (2,390 individuals) with respect to the other
periods of activity (Table 2, Figure 3).
RESULTS
DISCUSSION
Mosquito assemblage description
In 2018, a total of 6,110 adult mosquitoes belonging to This study focused on understanding the responses
nine genera and 23 species was captured during the rainy of a group of mosquitoes in different types of land use and
season in three types of land use and in three periods of periods of activity within a landscape originally dominated
activity. As shown in the species accumulation curve, the ACE by a low semi-evergreen forest matrix. In general, our results
index estimates 23 species, while the Chao1 index estimates showed that the region, regardless of the type of land use,
22 species, suggesting that 100% of the species were obtained was dominated by three species (Aedes taeniorhynchus, Aedes
in the present study. The dominant species were Aedes scapularis, and Culex nigripalpus) and that the communities
taeniorhynchus (36.2%), Culex nigripalpus (29.4%), Aedes were very similar in terms of species richness. More than half
scapularis (18.1%), Culex eastor (9.2%), Aedes angustivittatus of the species were shared between the three types of land
(1.8%), Aedes tormentor (1.4%), and Uranotaenia lowii use and during periods of activity. In terms of abundance,
(1.3%). Rare species occupy 2.6% of the sampling. The the mosquito assembly showed greater variability and less
greatest richness and abundance were found in the secondary similarity between types of land use and periods of activity,
low semi-evergreen forest (SF) (20 spp., 2,954 individuals). indicating that the resources for mosquito development
The low semi-evergreen forest (CF) had greater richness and varied according to space and time.
less abundance (17 spp., 1,045 individuals) than the mango In particular, the hierarchy of dominant species changed
plantation (MP) (11 spp., 2,111 individuals). With respect to in reference to the period of activity within each type of land
the period of activity, dusk (NI) had the greatest abundance use. Being immersed in the same matrix could explain the
and richness (20 spp., 4,380 individuals), followed by dawn similarity in mosquito communities. The flight behavior of
(DA) (14 spp., 1,127 individuals), and finally noon (NO) (12 mosquito species, such as Ae. taeniorhynchus that can fly
spp., 603 individuals) (Table 1, Figure 2). between 8-60 km (Ailes 1998), could explain why it was
found in the three types of land use, and also for Mansonia
Assemblage analysis in types of land use and activity titillans and Coquillettidia perturbans that can fly several
periods kilometers from their oviposition sites (Carpenter and
The structure of the assembly of mosquito species LaCasse 1955, Lounibos and Linley 1987). Therefore, high
changed during our study. There was a variation in the connectivity could be influencing the homogeneity in the
number of species and also with respect to abundance in local landscape and result in shared species in the types of
each type of land use and for each period of activity. There land uses. However, when analyzing the periods of activity,
were three dominant species for all sites and periods of we found subtle differences, since all species are related to a
activity, but the hierarchical position changes for the rest of greater or lesser extent with the cycles of light and dark.
the species (Figure 4). Shannon’s exponential index is higher The abundance and richness of mosquitoes respond
for less pronounced curves and therefore more equitable and mainly to biotic factors (availability of hosts for food, plants
may be a reason that the EF site has the highest value of this as shelter, and oviposition) and to abiotic factors (relative
index. However, similar curves, and therefore values, of the humidity, seasonality, and temperature). However, light
nearby Shannon exponential are shown for periods of activity intensity is an important factor that regulates behavior, such
(Figure 2). as during the twilight period that can establish the beginning
or end of mosquito activity (Forattini et al. 1981, Bona and
Assemblage structure Navarro-Silva 2008). Species like Culex nigripalpus had a
Significant effects were observed in the types of land use greater abundance during the NI period, which coincides
and in the periods of activity with respect to species richness with other publications where it is considered as a nocturnal
(Table 2). Significant values regarding richness were found crepuscular species (Wright and Knight, 1968). On the other
in the nightfall (NI) and noon (NO) periods and between hand, Psorophora ferox presented a greater abundance during
low semi-evergreen forest (CF) in the NI period. Although the NO period, as it is a tropical species that has daytime
the data show that secondary low semi-evergreen forest (SF) activity. Aedes scapularis had its greatest abundance in
 19487134, 2020, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jvec.12389 by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [05/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Vol. 45, no.2 Journal of Vector Ecology 191

Table 1. Species of mosquitoes captured in each land use type and each activity period.

CF SF MP
C
*
Spp Total
DA NO NI DA NO NI DA NO NI
Aedes taeniorhynchus
At 128 77 86 207 28 1,255 94 66 269 2,210
(Wiedemann, 1821)
Aedes scapularis
As 142 95 28 194 79 184 83 148 155 1,108
(Rondani, 1848)
Culex nigripalpus
Cn 30 1 193 10 4 553 141 0 863 1,795
(Theobald, 1901)
Aedes tormentor (Dyar &
Ao 14 28 22 16 0 5 0 0 0 85
Knab, 1906)
Ce Culex eastor (Dyar, 1920) 7 0 50 4 0 273 8 0 219 561
Aedes angustivittatus
Aa 20 15 12 6 0 59 0 0 0 112
(Dyar & Knab, 1907)
Psorophora ferox (Von
Pf 3 25 4 0 2 5 0 4 2 45
Humboldt, 1819)
Uranotaenia lowii
Ul 1 2 27 0 0 27 0 0 25 82
(Theobald, 1901)
Haemagogus regalis
Hr 0 13 0 0 2 2 0 0 0 17
(Dyar & Knab, 1906)
Coquillettidia perturbans
Cp 4 0 3 3 0 4 0 0 0 14
(Walker, 1856)
W Wyeomyia sp 0 4 0 0 0 0 0 7 0 11
Af Aedes fulvus (Ross, 1943) 0 0 2 1 0 5 0 0 0 8
Anopheles
Ap pseudopunctipennis 0 0 2 4 0 4 0 0 0 10
(Dyar & Knab, 1906)
Mansonia titillans
Mt 1 0 1 0 0 0 0 0 24 26
(Walker, 1848)
Psorophora cyanescens
Pc 2 0 0 0 0 1 1 0 0 4
(Coquillett, 1902)
Uranotaenia leucoptera
Ue 0 1 1 0 0 0 0 0 1 3
(Theobald, 1907)
Psorophora ciliata
Pi 1 0 0 2 1 0 0 0 0 4
(Fabricius, 1794)
Anopheles bradleyi (King,
Ab 0 0 0 0 0 4 0 0 0 4
1939)
Anopheles vestitipennis
Av 0 0 0 0 0 4 0 0 0 4
(Dyar & Knab, 1906)
Anopheles albimanus
Al 0 0 0 0 0 2 0 0 1 3
(Wiedemann, 1820)
Psorophora confinnis
Po (Lynch Arribálzaga, 0 0 0 0 0 2 0 0 0 2
1891)
Mansonia indubitans
Mi 0 0 0 0 0 1 0 0 0 1
(Dyar & Shannon, 1925)
Psorophora varipes
Pv 0 0 0 0 1 0 0 0 0 1
(Coquillett, 1904)
  Richness 12 10 13 10 7 18 5 4 9 23
  Abundance 353 261 431 447 117 2,390 327 225 1,559 6,110
CF low semi-evergreen forest, SF secondary low semi-evergreen forest, MP mango plantation, DA dawn,
*

NO noon, NI nightfall, C species code.

19487134, 2020, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jvec.12389 by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [05/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
December 2020

Figure 2. Rank-abundance curve. Numbers above graphs denote Exponential Shannon Index value for land use type (A) and
Journal of Vector Ecology

activity period (B). Species codes (capital letters) are given in Table 1.
192
19487134, 2020, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jvec.12389 by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [05/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
193

Figure 3. Mosquito richness and abundance in different land use type and activity periods. CF=low
semi-evergreen forest, SF=secondary low semi-evergreen forest, MP=mango plantation, DA=dawn,
Journal of Vector Ecology

NO=Noon, NI=nightfall activity period.

Vol. 45, no.2
 19487134, 2020, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jvec.12389 by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [05/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
194 Journal of Vector Ecology December 2020

Table 2. A generalized linear model (GLM) assuming a Negative Binomial distribution with logit link function for Abundance
and Richness analysis. Significant P values are in boldface and non-significant trends in italics.

Abundance
Components Estimate SE z-value P-value
Intercept 3.79549 0.1441 26.34 < 2e-16
Low semi-evergreen forest (CF) -0.22596 0.20517 -1.101 0.270771
Secondary low semi-evergreen forest (SF) -0.29596 0.20567 1.439 0.150159
Nightfall (NI) 1.68181 0.19924 8.441 < 2e-16
Noon (NO) -1.31058 0.2182 -6.006 1.90E-09
CF:NI -1.49714 0.28616 -5.232 1.68E-07
SF:NI -0.06575 0.28346 -0.232 0.81658
CF:NO 0.99915 0.30217 3.307 0.000945
SF:NO 0.83634 0.30417 2.75 0.005968
Richness
Components Estimate SE z-value P-value
Intercept 1.4816 1.51E-01 9.828 < 2e-16
Low semi-evergreen forest (CF) 2.76E-01 2.00E-01 1.382 0.167036
Secondary low semi-evergreen forest (SF) -1.21E-01 2.20E-01 -0.548 0.58336
Nightfall (NI) 7.04E-01 1.84E-01 3.822 1.32E-04
Noon (NO) -6.49E-01 2.57E-01 -2.521 0.011699
CF:NI -5.02E-01 2.56E-01 -1.965 0.049364
SF:NI 6.28E-02 2.67E-01 0.235 0.814308
CF:NO 6.14E-01 3.18E-01 1.928 0.053875
SF:NO 3.17E-01 3.57E-01 0.889 0.374269

the SF site, but in the MP it was more abundant in the NO could cause mosquito species to adapt and therefore increase
period. This may be due to the ability of this species to adapt their abundance. For example, Ae. scapularis are attracted to
to regenerating sites or with intense changes, such as on a humans and pets and feed on them, and in turn are a potential
plantation (Orlandin et al. 2017). vector of Venezuelan equine encephalitis and yellow fever. On
With respect to the type of land use, Haemagogus regalis the other hand, Cx. nigripalpus had a greater abundance in the
had its greatest abundance in EF during the NO period, MP site that may be due to the proximity to the Usumacinta
possibly influenced by the presence of epiphytic plants such River, and as a consequence, environments are created for
as bromeliads which are used as a site for oviposition (Berlin oviposition in permanent and semi-permanent water.
1969, Lane 1953). Species in the genus Anopheles had mostly We show that land use types and periods of activity
crepuscular activity (Astaiza et al. 1988) in the NI period influence the structure of the mosquito assembly. However,
except for An. pseudopunctipennis that was captured in the DA our results also show that the assemblage of mosquitoes,
period. In turn, they had a greater presence and abundance in despite being immersed in the same matrix and presenting
the SF site as some species of this genus have a predilection three dominant species, is quite heterogeneous (that is,
for disturbed sites (Rodríguez et al. 1996). structure of different richness and abundance), which
Some species of mosquitoes exhibit a high degree of suggests that biotic and abiotic conditions are different for
specialization in their host selection and oviposition site, each type of land use. In turn, the periods of activity influence
while others are generalists and opportunistic (Bentley and the presence of the species. Regenerating sites could host a
Day 1989). Changes in host abundance due to anthropogenic greater abundance of species that could be disease vectors
impacts can affect both host choice and habitat, especially (Ae. taeniorhynchus and Ae. scapularis), but conserved sites
if the species are generalists (Takken and Verhulst 2013, could be more diverse. Finally, our work generates important
Abella-Medrano et al. 2015). Environments with some degree information to understand the diversity of mosquitoes in
of disturbance, such as the SF and MP, can have a negative reference to changes in land use in different periods of activity.
influence on biodiversity due to habitat loss, defaunation, We consider it a potentially useful tool in the development of
and introduction of domestic fauna (Alberti 2008), that epizootiological planning and surveillance programs focused
 19487134, 2020, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jvec.12389 by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [05/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Vol. 45, no.2 Journal of Vector Ecology 195

mainly on species of mosquitoes of medical and veterinary Revisión del género neotropical Howardina de Aedes.
importance. Contrib. Am. Entomol. Inst. 4: 1-190.
Brown, B.V., A. Borkent, J.M. Cumming, D.M. Wood, N.E.
Acknowledgments Woodley, and M. Zumbado. 2009. Manual of Central
American Diptera: Volume 1. Canadian Sci. Publ. (NRC
We thank Simon Pierre Mokondoko-Delgadillo, Paulina Research Press). 714 pp. 
Walbey,  Citlali López,  Brenda Maya, Guillermo Orta and Bona, A.A. and M.A. Navarro-Silva. 2008. Diversidade de
Adrián Serrano for their assistance during fieldwork. We Culicidae durante os períodos crepusculares em bioma de
thank landowners (Roberto Calzada, Roberto Uribe Jacinto, Floresta Atlântica e paridade de Anophles cruzii (Diptera:
Juan Carlos Garcia Martinez, and Sebastián Montejo Culicidae). Rev. Brasileira Zool. 25: 40-48. http://dx.doi.
Narváez) for allowing us to work on their private properties. org/10.1590/S0101-81752008000100007.
Rafael Ojeda-Flores was supported by Consejo Nacional de Carpenter, S.J. and W.J. LaCasse. 1955. Mosquitoes of North
Ciencia y Tecnología (CONACYT Problemas Nacionales America. Univ. Calif. Press. 360 pp.
#219), and Carlos Antonio Abella-Medrano was supported Chao, A. and T.J. Shen. 2010. Program SPADE (Species
by a post-doctoral fellowship grant (DGAPA Dirección Prediction and Diversity Estimation). http://chao.stat.
general de asuntos del personal académico, Departamento nthu.edu.tw.
de Fortalecimiento Académico, Programa de Becas Colwell, R.K. and J.A. Coddington. 1994. Estimating
Posdoctorales, Universidad Nacional Autónoma de México terrestrial biodiversity through extrapolation. Phil. Trans.
UNAM). R Soc. B. 345: 101–118.Darsie Jr., R.F. 1996. A survey and
bibliography of the mosquito fauna of Mexico (Diptera:
REFERENCES CITED Culicidae). J. Am. Mosq. Contr. Assoc. 12: 298-306.
Forattini, O.P., A.C. Gomes, J.L.F. Santos, E.A.B. Galati, E.X.
Abella-Medrano, C.A., S. Ibáñez-Bernal, I. MacGregor-Fors, Rabello, and D. Natal. 1981. Observações sobre atividade
and D. Santiago-Alarcon. 2015. Spatiotemporal variation de mosquitos Culicidae, em mata residual no Vale do
of mosquito diversity (Diptera: Culicidae) at places with Ribeira, São Paulo, Brasil. Rev. Saúde Públ. 15: 557-586.
different land-use types within a neotropical montane Gottdenker, N.L., D.G. Streicker, C.L. Faust, and C.R. Carroll.
cloud forest matrix. Parasit.Vectors 8: 487. 2014. Anthropogenic land use change and infectious
Abella-Medrano, C.A., S. Ibáñez-Bernal, P. Carbó-Ramírez, diseases: a review of the evidence. EcoHealth 11: 619-
and D. Santiago-Alarcon. 2018. Blood-meal preferences 632.
and avian malaria detection in mosquitoes (Diptera: Harbach, R.E. 2007. The Culicidae (Diptera): a review of
Culicidae) captured at different land use types within a taxonomy, classification and phylogeny. Zootaxa 1668:
neotropical montane cloud forest matrix. Parasitol. Intl. 91-538.
67: 313-320. Harbach, R.E. and K.L. Knight. 1980. Taxonomists’ Glossary of
Alberti, M. 2008. Advances in Urban Ecology: Integrating Mosquito Anatomy: Plexus Publishing Inc. Marlton, NJ.
Humans and Ecological Processes in Urban Ecosystems. 415 pp.
Springer, NY, 366 pp. Heinemann, S.J. and J.N. Belkin. 1977. Collection records of
Alcaide, M., C. Rico, S. Ruiz, R. Soriguer, J. Munoz, and J. the project “Mosquitoes of Middle America.” 7. Costa
Figuerola. 2009. Disentangling vector-borne transmission Rica (CR). Mosq. Syst. 9: 237-287.
networks: a universal DNA barcoding method to identify Jost, L. 2006. Entropy and diversity. Oikos 113: 363–375.
vertebrate hosts from arthropod bloodmeals. PLoS ONE Jost, L. 2010. The relation between evenness and diversity.
4: e7092. doi:10.1371/journal.pone.0007092. Diversity 2: 207–232.
Ailes, M.C. 1998. Failure to predict abundance of saltmarsh Kawada, H., S.Y. Takemura, K. Arikawa, and M. Takagi.
mosquitoes Aedes sollicitans and Ae. taeniorhynchus 2005. Comparative study on nocturnal behavior of Aedes
(Diptera: Culicidae) by using variables of tide and aegypti and Aedes albopictus. J. Med. Entomol. 42: 312-
weather. J. Med. Entomol. 35: 200-204. 318.
Astaiza, R., C. Murillo, and P. Fajardo. 1988. Biología de Keesing, F., L.K. Belden, P. Daszak, A. Dobson, C.D. Harvell,
Anopheles (Kerteszia) neivai HD&K (Diptera: Culicidae) R.D. Holt, P. Hudson, A. Jolles, K.E. Jones, C.E. Mitchell,
en la costa pacífica de Colombia. Rev. Saude Publ. 22: S.S. Myers, T. Bogich, and R.S. Ostfeld. 2010. Impacts
101-108. of biodiversity on the emergence and transmission of
Belkin, J.N., S.J. Heinemann, and W.A. Page. 1970. The infectious diseases. Nature 468: 647-652.
Culicidae of Jamaica. Contrib. Am. Entomol. Inst. 6: Kirkeby, C., K. Græsbøll, A. Stockmarr, L.E. Christiansen,
1-458 pp. and R. Bødker. 2013. The range of attraction for light
Bentley, M.D. and J.F. Day. 1989. Chemical ecology and traps catching Culicoides biting midges (Diptera:
behavioral aspects of mosquito oviposition. Annu. Rev. Ceratopogonidae). Parasit. Vectors 6: 67.
Entomol. 34: 401–421. Lane, J. 1953. Neotropical Culicidae. Volumes I & II. Univ. Sao
Berlin, O.G.W. 1969. Mosquito studies (Diptera, Culicidae) Paulo, Brazil. 1,112 pp.
XII. A revision of the neotropical subgenus Howardina of Lounibos, L. and J. Linley. 1987. A quantitative analysis of
Aedes. Estudios sobre zancudos (Diptera, Culicidae) XII. underwater oviposition by the mosquito Mansonia
 19487134, 2020, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jvec.12389 by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [05/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
196 Journal of Vector Ecology December 2020

titillans. Physiol. Entomol. 12: 435-443. Rodriguez, A.D., M.H. Rodriguez, J.E. Hernandez, S.W.
Magurran, A.E. 2003. Measuring Biological Diversity. Wiley. Dister, L.R. Beck, E. Rejmankova, and D.R. Roberts.
264 pp. 1996. Landscape surrounding human settlements and
Ndoen, E., C. Wild, P. Dale, N. Sipe, and M. Dale. 2011. Dusk Anopheles albimanus (Diptera: Culicidae) abundance in
to dawn activity patterns of anopheline mosquitoes in Southern Chiapas, Mexico. J. Med. Entomol. 33: 39-48.
West Timor and Java, Indonesia. SE Asian J. Trop. Med. Smith, K.F., D.F. Sax, S.D. Gaines, V. Guernier, and J.F. Guégan.
Publ. Hlth. 42: 550. 2007. Globalization of human infectious disease. Ecology
Orlandin, E., E.B. Santos, M. Piovesan, M.A. Favretto, A.H. 88: 1903-1910.
Schneeberger, V.O. Souza, G.A. Muller, and G. Wagner. Silver, J. B. 2007. Mosquito Ecology: Field Sampling Methods.
2017. Mosquitoes (Diptera: Culicidae) from crepuscular Springer. 1,477 pp.
period in an Atlantic Forest area in Southern Brazil. Takken, W. and N.O. Verhulst. 2013. Host preferences of
Brazilian J. Biol. 77: 60-67. blood-feeding mosquitoes. Annu. Rev. Entomol. 58: 433-
Ortega Morales, A.I., P. Mis Avila, A. Elizondo-Quiroga, R.E. 453.
Harbach, Q.K. Siller-Rodríguez, and I. Fernández-Salas. Wright, R.E. and K.L. Knight. 1968. Evening crepuscular
2010. Los mosquitos del estado de Quintana Roo, México activity of some Iowan mosquitoes (Diptera: Culicidae).
(Diptera: Culicidae). Acta Zoológ. Mexicana 26: 33-46. J. Kansas Entomol. Soc. 45-47.
Ortega‐Morales, A. I., R. Méndez‐López, J.A. Garza‐ Wilcox, B.A. and D.J. Gubler. 2005. Disease ecology and the
Hernández, V.H. González‐Álvarez, I. Ruiz‐Arrondo, global emergence of zoonotic pathogens. Environ. Hlth.
H. Huerta‐Jiménez, L.M. Rodríguez‐Martínez, and Prev. Med. 10: 263-272.
M.A. Rodríguez‐Pérez. 2019. The mosquitoes (Diptera:
Culicidae) of Tabasco, Mexico. J. Vector Ecol. 44: 57-67.